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Asparagine endopeptidase regulates MOG antigen presentation by modulation of
cathepsin L activity
Mira Tohmé*1,2,3, Renaud Colisson*4, Kamel Benlagha5, Stephen Anderton6, Cécile
Delarasse7, Mauro Teixera8 and Bénédicte Manoury&1,2
1 INSERM, Unité 1013, 75015, Paris, France
2 Université Paris Descartes, Sorbonne Paris Cité, Faculté de médecine, 75015 Paris,
France
3 INSERM, Unité 932, Institut Curie, 75005, Paris, France
4 INSERM U851, Université de lyon, 21 Av Tony Garnier 69365 Lyon cedex 07
5 U580 Hôpital saint-vincent de paul 75013 Paris, France,
6 University of Edinburgh, Institute of Immunology and Infection Research, School of
Biological Sciences, Kings Buildings, West Mains Road, Edinburgh EH9 3JT UK,
7 University of Paris Sud, Institut de Biochimie et Biophysique Moléculaire et Cellulaire, Unité
Mixte de Recherche 8619, Centre National de la Recherche Scientifique, 91400 Orsay,
France
8 Universidade Federal de Minas Avenida Antonio Carlos Belo Horizonte 31270-0901 Brazil
Running Title: AEP-dependent MOG antigen presentation
Key words: AEP, MHC class II presentation/processing, cathepsin L, MOG
&Corresponding author: Dr Bénédicte Manoury, INSERM, Unité 1013, Hôpital Necker-Enfants
malades, 149 rue de Sèvres, 75743 Paris cedex 15, France, Phone: +33 (0) 1 44 49 53 75;
Fax: + 33 (0) 44 49 53 82; Email: [email protected]
* both authors contributed equally to the work
"
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9-(7'%*'(/"645"()"/(&$%"+$6$1"
"
"
"
"
"
"
+
+
LN AEP wt
LN AEP ko
0
50000
100000
150000
200000
1 10 100
MOG concentration (µg/ml)
CP
M (
Th
ymid
ine
inco
rpo
ratio
n) B A
0
5000
10000
15000
20000
0 60 120 240
Time (min)
MOG antigen
CD4+ AEP wt
CD4+ AEP ko
P!""
"
QCPE>G+-+
"
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SP
C
?AEP
Heavy chain Light chain
Procathepsin L
Single chain
Propeptide
Processing of cathepsin L
DSNKN
S
33
21
52
0 30min 3h o/n
WT
Proform
HeavyChain
Single Chain
+ AEP
inhibitor
0 3h
A
IP:CatL
D
B
Activecathepsin L
AEPWT
AEPKO
BMDCs
33
21
Single Chain
Heavy Chain
52
KOWTKOWT
BMDCs sDCs
SD1 cells - +
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"
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"
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+
+
+
+
+
+
+
+
IL-2
re
lea
se (
ng
/ml)
0
80
160
240
320
0 60 120 180 240 Time (min) Time (min)
0
70
140
210
280
350
0 60 120 180 240
α-Galcer Gal α1,4 gal αCer A B
P?""
"
+
+
QCPE>G+<+
+
QCPE>G+<@+!$5+OG[CJCGB?+VCJG+OA+BA?+OG]GIAH+$!$+=[?G>+4(9+CBaGJ?CAB+NFGB+JAVH=>GO+?A+X'+VCJG,+
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" "
0 5 10 15 20 25 30 35
-15
-10
-5
0 WT KO
Days after EAE induction
∆ i
n B
od
y w
eig
ht
(%)
10 15 20 25 30 35 0
1
2
3
4
Days after EAE induction D
ise
ase
Sco
re
A B
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! "!
Intracellular Toll-like receptors recruitment and cleavage in
endosomal/lysosomal organelles
Mira Tohmé1,2,3 and Bénédicte Manoury1,2,&
1 INSERM, Unité 1013, 75015, Paris, France
2 Université Paris Descartes, Sorbonne Paris Cité, Faculté de médecine, 75015 Paris,
France
3 INSERM, Unité 932, Institut Curie, 75005, Paris, France
&Corresponding author: Dr Bénédicte Manoury, INSERM, Unité 1013, Hôpital Necker-
Enfants malades, 149 rue de Sèvres, 75743 Paris cedex 15, France, Phone: +33 (0) 1 44
49 53 75; Fax: + 33 (0) 44 49 53 82; Email: [email protected]
! #!
Abstract
Microbial pathogens are recognized through multiple, distinct receptors such as
intracellular Toll like receptors (TLRs 3, 7, 8, 9 and 13) which reside in the endosomes and
lysosomes. TLRs are sensitive to chloroquine, a lysomotropic agent that neutralizes acidic
compartments indicating a role for endo/lysosomal proteases for their signalling. Indeed,
upon stimulation, full length TLR7 and 9 are cleaved into a C-terminal fragment and this
processing is highly dependent on a cysteine protease named Asparagine Endopeptidase
(AEP) in dendritic cells. A recruitment and a boost in AEP activity, which was induced
shortly after TLR7 and 9 stimulation, are shown to promote TLR7 and 9 cleavage and
correlate with an increased acidification in endosomes and lysosomes. Moreover, mutating
a putative AEP cleavage site in TLR7 or 9 strongly decreases their signalling in DCs
suggesting perhaps a direct cleavage of TLR7 and 9 by AEP. These results demonstrate
that TLR7 and 9 require a proteolytic cleavage for their signalling and identified a key
endocytic protease playing a critical role in this process.
! $!
Introduction
Toll like receptors (TLRs) are molecules, which recognize conserved molecules from
microorganisms and in dendritic cells (DCs), they are crucial in linking innate to adaptive
immunity. TLRs contain several leucine rich repeats (LRR) in an extracellular loop, a trans-
membrane domain and a cytosolic domain and are expressed either at the plasma
membrane or in the endosomal/lysosomal organelles. TLR stimulation is linked to MyD88
or TRIF-dependent signaling pathways that regulate the activation of different transcription
factors, such as NF-kB (Janeway and Medzhitov, 2002). Specific interaction between
TLRs and their ligands activates NF-kB resulting in enhanced inflammatory cytokine
responses, induction of DC maturation and expression of chemokine receptors. TLRs
expressed at the plasma membrane recognized Gram-negative bacteria and endosomal
TLRs sense viral and bacterial nucleic acids such as double/single-stranded RNA or DNA.
Endogenous ligands called DAMPs (for damage associated molecular patterns) may also
activate TLRs during self-tissues or cell damage. Recent findings have described the
importance of proteolysis for endosomal TLRs function (Ewald et al., 2008; Park et al.,
2008; Garcia-Cattaneo et al., 2012) and TLRs activation have been shown to boost MHCI
cross presentation in DCs (de Brito et al., 2011; Sathe et al., 2011). Upon stimulation, full-
length (FL) TLR9 is cleaved into a C-terminal (C-ter) fragment sufficient for signalling. This
cleavage is realized by several cathepsins in different cells, including macrophages, while
in DCs this cleavage is performed mainly by cathepsin K (CatK) and Asparagine
Endopeptidase (AEP). In CatK deficient DCs, TLR9 signaling is abrogated and in DCs
lacking AEP, TLR9 cleavage in phagosomal compartments as well as CD4+ antigen
specific T cell proliferation was greatly reduced upon CpG stimulation (Asagiri et al., 2008;
Sepulveda et al., 2009). TLR7 is also subjected to similar proteolytic maturation and
requires AEP for proper signaling (Maschalidi et al., 2012). Altogether these results
indicate that endosomal proteases, which are key players in generating peptides for the
MHC class II pathway (Riese et al., 1996; Nakagawa et al., 1999; Manoury et al., 1998;
Moss et al., 2005), play also an important role in intracellular TLRs activation
! %!
Purification of endosomes and lysosomes
Sucrose gradient fractionation !
All procedures, unless otherwise indicated are carried out at 4°C
1. 108 dendritic cells (DCs) are generated from mouse bone marrow by culturing
precursors for 7–10 days in Iscove’s Modified Dulbecco’s Medium (IMDM, Sigma,
I3390) supplemented with 10 FBS, 1% PS, 1% GLN and 10 ng/ml GM-CSF (Peprotech,
315-03).
2. Detach BMDCs (bone marrow derived dendritic cells) with PBS-EDTA 5 mM (10
minutes at 37°C).
3. After two washes in PBS, and one wash in Homogeneization Buffer (HB : 3 mM
imidazole, 8% sucrose, 1 mM DTT, 1 mM EDTA supplemented with 1 tablet of
proteases inhibitor coktail (Roche), pH 7.4), cells are homogenised with a cell craker in
HB buffer through a ball of 0,006 mm of clearance (ball number 6) in order to have 80%
of mortality.
4. Postnuclear supernatant (PNS) is prepared by centrifugation (1000 g for 10 min).
5. PNS is adjusted with 62% of sucrose solution in order to have a final concentration of
40.6% of sucrose.
6. A gradient of sucrose is prepared following this order from the bottom to the top:
2 mL of PNS containing endosomes and lysosomes
3 mL of 35% of sucrose
2 mL of 25% of sucrose
4 mL of HB
7. After ultracentrifugation for 90 minutes with no brake using the SW41 rotor, fractions are
collected. The interface/ring between the 35% and 25% sucrose corresponds to the
early endosomes while the one between the 25% of sucrose and the HB buffer
corresponds to the late endosomes.
8. The fractions are concentrated by ultracentrifugation using the TLA110 rotor for 30
minutes at 35000 rpm.
9. Pellets are resuspend in 50 µL of PBS and can be either frozen or used immediately for
a western blot.
! &!
Percoll gradient fractionation (lysosome purification)
Lysosomes purification !
1. DCs are prepared and homogenised as described in 2.1.1 and 1.2.
2. The homogenate is centrifuged at 2000 rpm for 10 min and the PNS is recovered and
underlaid with 23mL of 27% of percoll.
3. After centrifugation for 60 min at 23 000 rpm using the Ti45 rotor, fractions were
collected by upward displacement using a fractions collector.
4. Fractions are collected and assayed for β-hexosaminidase activity (check 2.2.2).
5. Positive fractions corresponding to lysosomes are pooled and centrifuged for 60 min at
40 000 rpm using the Ti70.2 rotor.
6. The ring obtained is recovered with a pasteur pipette and is subjected to one more
centrifugation using the TLS-55 rotor at 50 000 rpm for 60 min.
7. Pellet containing concentrated lysosomes is collected and frozen.
β-hexosaminidase assay
!1. Add 20 µL of the sample (fractions collected in 2.2.1.3) or the blank (27% percoll) to
80 µL of Homogeneisation Buffer HB, prewarmed at 37°C.
2. Prepare the standard curve using the 4-methylumbelliferone, starting concentration
at 1nmol.
3. Add 100 µL of substrate (4-methylumbelliferyl n-acetyl β-D-glucosamide)
4. Incubate 10 min at 37°C
5. Stop the reaction by adding 100 µL of stop buffer (0,1M glycine, pH 10.3), store in the
dark
6. Read fluorescence on a fluorimeter: excitation 360 nm, emission 450 nm
Endosomes and lysosome purification using magnetic beads
1. Detach BMDCs with PBS-EDTA 5 mM (10 minutes at 37°C).
2. Wash the cells with PBS 2x.
3. Resuspend the cells in 15 ml falcon tube (10.108 cells/1 ml) in IMDM alone.
4. Add 60 µL of magnetic nanoparticles (turbobeads of 20 nm of diameter, 10mg/mL)
for 30 min at 4° C.
5. The cells are incubated 20 minutes (pulse) in the water bath at 37°C
6. Stop the reaction by adding 10 ml cold PBS-BSA 0.1% and centrifuge for 10 min at
! '!
1300 rpm at 4°C.
7. Repeat step 6 3 times.
8. Resuspend the cells in 2 ml of complete IMDM medium and split the cells in 2
falcon tubes of 15 ml (1ml of cells each).
9. Add 10 ml cold PBS-BSA 0.1% for t=0 (pulse) and leave on ice, put the other tube
at 37°C for 100 minutes (chase).
10 T=0 correspond to early endosomes (20 minutes of pulse), t=120 minutes
correspond to lysosomes.
11 At the end of the chase, centrifuge the cells.
12 Now, perform the end of the experiment on ice.
13 Wash the cells in HB buffer.
14 Resuspend the cells in 1ml of HB buffer.
15 Break the cells using a 1ml syringe and a 22g needle. You need about 30 flushes to
break the cells. Check the breaking of the cells under a microscope (about 80% of
the cells should be dead).
16 Transfer the breaking cells into cold eppendorf tubes and place the eppendorf tubes
on the magnetic stand on ice.
17 Leave 5 minutes; aspirate the supernatant with a thin tip. Keep the SNT aside.
18 Wash the beads carefully with 1ml PBS-BSA 0,1% and repeat step 18 8x.
19 Resuspend the beads in 50 µL of lysis buffer (50 mM Tris pH 7.4, 150 mM NaCl
0.5% NP40, 2 mM MgCl2, and a tablet of a cocktail of proteases inhibitors) and
leave on ice for 15 minutes.
20 Centrifuge at 12000 rpm for 15 min and freeze the supernatant.
Proteases assays
1. Buffer: 50 mM citrate buffer, pH 5.5, 1 mM DTT.
2. Protease activity assays are performed on a Mithras LB940 (Berthold
technologies) by measuring the release of fluorescent N-Acetyl-Methyl-Coumarin
(Nhmec) in citrate buffer (pH 5.5) at 37°C. Specific substrates are the following:
AEP: Z-Ala-Ala-Asn-NHMec for AEP, Z-Arg-Arg-NHMec for CatB, Z-Phe-Arg-
NHMec for CatB/L, Z-Val-Val-Arg-NHMec for CatS and Z-Gly-Pro-Arg-NHMec for
CatK.
3. Activity of the proteases is assessed using specific fluorometric substrates. 1 µg
of early or late endosomes are incubated with the different specific substrates
! (!
(see below) for different times. To calculate the specific activity of each protease
(µmole of substrate release per minute), a standard curve is obtained using
different concentrations of NHmec (from 0.2 to 2 µM).
4. Same assays are performed with purified endosomes or lysosomes from BMDCs
stimulated with intracellular TLRs ligands.
Intracellular TLRs processing
To check the purity of the endosomes and lysosomes obtained and to study TLR9
cleavage, proteins expressed in the endosomes and lysosomes are subjected to a
Western Blot (Burnette 1981).
1. Protein concentration is measured with a Colorimetric assay kit (Biorad )
2. Samples (5 µg of endosomes or lysosomes) are heated at 80°C for 10 minutes in
the reducing buffer (10 µl of 4X Laemli buffer supplemented with 8%of β-mercapto
ethanol).
3. Following electrophoresis, proteins are transferred on a PVDF membrane, pore
size 0,45 µm and they are stained with antibodies specific for the target proteins :
Rab 5 for early endosomes and cathepsin D for late endosomes. TLR9 cleavage is
also monitored (see Figure 1 Below).
! )!
Figure 1: Purity of endocytic compartments and TLR9 expression in endosomes.
Endosomes from wt (wild type) and AEP deficient BMDCs (AEP-/-
) were magnetically purified after 20 or 120
minutes. Protein expressed in total lysate (TL) or in endosomes (5 mg) were resolved by SDS-PAGE. TLR9
proteins in early (EE) and late (LE) endosomes from WT and AEP deficient BMDCs were detected by
immunoblot.
Immunodetection of early (Rab5) and late (Rab7) markers in endosomes.
FL TLR9: ful length TLR9
TLR9 N-ter: fragment corresponding to the N-terminal part of TLR9
! *!
References
!
Asagiri, M., T. Hirai, T. Kunigami, S. Kamano, H. J. Gober, K. Okamoto, K. Nishikawa, E. Latz, D. T. Golenbock, K. Aoki, K. Ohya, Y. Imai, Y. Morishita, K. Miyazono, S. Kato, P. Saftig, and H. Takayanagi. (2008). Cathepsin K-dependent Toll-like receptor 9 signaling revealed in experimental arthritis Science 319, 624-627.
Burnette WN. (1981). “Western blotting”: electrophoretic transfer of proteins from sodium dodecyl sulfate—polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A". Analytical Biochemistry 112, 195–203.
de Brito, C., Tomkowiak, M., Ghittoni, R., Caux, C., Leverrier, Y., and Marvel J. (2011) CpG promotes cross-presentation of dead cell-associated antigens br pre-CD8+alpha dendritic cells. J. Immunol. 186, 1503-1511.
Ewald, S. E., B. L. Lee, L. Lau, K. E. Wickliffe, G. P. Shi, H. A. Chapman, and G. M.
Barton. (2008). +,-!-./0102345!06!+0778749-!:-.-;/0:!*!4<!.7-3=-1!/0!>-5-:3/-!3!6?5./40537!:-.-;/0:@Nature 456:658-662.
Garcia-Cattaneo, A., F. X. Gobert, M. Muller, F. Toscano, M. Flores, A. Lescure, E. Del Nery, and P. Benaroch. (2012). Proc Natl Acad Sci U S A 109, 9053-9058.
Janeway, CA., and Medzhitov, R. (2002). Innate immune recognition. Annu Rev Immunol. 20,197-216.
Manoury, B., Hewitt, E.W., Morrice, N., Dando, P.M., Barrett, A.J., and Watts, C. (1998) An asparagynil endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396, 695-699.
Maschalidi S, Hässler S, Blanc F, Sepulveda F, Tohme M, Chignard M, van Endert P, Si-Tahar M, Descamps D and Manoury B. Asparagine Endopeptidase Controls Anti-Influenza Virus Immune Responses through TLR7 Activation. 2012 PLOS Pathog. Aug;8(8):e1002841 Moss, C.X., Villadangos, J.A., and Watts, C. (2005). Destructive potential of the
aspartyl protease cathepsin D in MHC class-restricted antigen processing. Eur J Immunol 35, 3442-3451.
Nakagawa, T., Roth, W., Wong, P., Nelson, A., Farr, A., Deussing, J., Villadangos, J.A., Ploegh, H., Peters, C., and Rudensky, A.Y. (1998). Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280, 450-453.!
Park, B., Brinkmann, M.M., Spooner, E., Lee, C.C., Kim, Y.M., and Ploegh; H.H. (2008).
A:0/-07B/4.!.7-3=3>-!45!35!-5107B<0<0237!.02;3:/2-5/!4<!:-C?4:-1!60:!3./4=3/405!06!
+0778749-!:-.-;/0:!*@ Nat Immunol 9,1407-1414. Riese R.J, Wolf, P.R., Bromme, D., Natkin, L.R., Villadangos, J.A., Ploegh, H.L., and
Chapman, H.A. (1996). Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 4, 357-366.
Sathe, P., Pooley, J., Vremec, D., Mintern, J., Jin, J.O., Wu, L., Kwak, J.Y., Villadangos, J.A., and Shortman, K. (2011). The acquisition of antigne cross-presentation function by newly formed dendritic cell. J. Immunol. 186, 5184-5192.
Sepulveda F, Maschalidi S, Colisson R, Heslop L, sakka E, Ghirelli, C, Lennon-dumenil AM, Amigorena S, Cabanie L and Manoury B. Critical Role for Asparagine
Endopeptidase in endocytic TLR signalling in dendritic cells. 2009 Immunity Nov 20, 31 731-748.
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1
In Vitro Digestion With Proteases Producing MHC Class II Ligands
Running title: MHC class II peptides generation
Mira Tohmé1,2,3, Sophia Maschalidi1,2 and Bénédicte Manoury1,2
1Institut National de la Santé et la Recherche Médicale, Unité 1013, 75015
Paris, France
2Université Paris Descartes, Sorbonne Paris Cité, Faculté de médecine
René Descartes, 75015 Paris, France
3Institut Curie, Institut National de la Santé et la Recherche Médicale, Unité
932, 75005 Paris, France
Corresponding author :
Bénédicte Manoury, INSERM U1013, Hôpital Necker, 149 rue de Sèvres
75743 Paris cedex 15, France
E-mail address :
[email protected] Tel. +33144495375, Fax : +33144495382
2
i.Summary
Proteases generate peptides that bind to MHC class II molecules to
interact with a wide diversity of CD4+ T cells. They are expressed in
dedicated organelles: endosomes and lysosomes of professional antigen
presenting cells (pAPCs) such as B cells, macrophages and dendritic cells.
The identification of endosomal proteases which produce antigenic peptides
is important for example for better vaccination and to prevent autoimmune
diseases. Here, we describe a panel of technics (in vitro digestion assays of
protein with recombinant proteases or purified endosomes/lysosomes, T cell
stimulation) to monitor the production of MHC class II ligands.
ii. Key words
MHC-II. Proteases. Endosomes/Lysosomes. Antigen processing. pAPCs.
I.Introduction
MHC class II molecules associate in the endoplasmic reticulum with a
chaperone protein: the invariant chain (1). Ii has many functions; one of
them is to deliver MHC class II complexes to endosomal/lysosomal
compartments (2). In these compartments, which also receive exogenous
antigens, proteases must perform two tasks: the generation of peptides that
will be loaded on MHC class II molecules and the proteolysis of Ii. Proteolytic
enzymes release amino acids and peptides from proteins and can be
grouped in different families based on their catalytic activities. They belong
to three major classes: aspartic, serine and cysteine families and are usually
dependent on acidic pH for their activities (3). The main enzymes present in
the endosomal/lysosomal pathway are the cathepsins (cathepsins B, C, D,
E, F, H, K, L, S) and AEP for asparagine endopeptidase. Processing of Ii is
mainly performed by cathepsin S in pAPCs (4, 5) and cathepsin L in cortical
thymic epithelial cells (6). For antigen processing, it appears that there is no
clear dependency on a single protease to generate a dedicate peptide but it
remains to be fully elucidated (7). Nonetheless, few exceptions have shown
that for example toxin tetanus C-fragment (TTCF) processing requires AEP
3
(8). Proteases instead of generating peptides can also have the opposite
effect which is to destroy MHC class II ligands. Indeed, the immunodominant
peptide of a self antigen, myelin basic protein, is destroyed by AEP and a
myoglobin epitope is cleaved by cathepsins D (9, 10). Here, in this chapter,
we demonstrate that the production of MHC class II ligands generated by in
vitro digestion with proteases either purified or from lysosomes can be tested
by incubating fixed APCs together with recombinant or radiolabelled
antigens predigested with proteases and T cells.
2- Materials
We will take the example of TTCF and use the CD4+ T cell hybridomas as
readout but in principle any antigen with the specific T cell hybridoma can be
used with the same method.
2-1 Soluble antigens
Recombinant proteins such as TTCF or ovalbumin are either bought or
purified from E. Coli using standard procedures (11, 12).
2-2 T cell hybridoma
CD4+ T cells hybridoma are generated from standard procedures (13). For
example, TTCF specific T cell hybridomas were obtained by fusion between
spleens from TTCF injected mice and a thymoma lacking the expression of
the T cell receptor (14).
2-3 In vitro Digestion assays
TNT T7 or SP6 quick Coupled Transcription/Translation system
(Promega) and 35S methionine (Perkin Elmer).
Digestion buffer: 50 mM citrate buffer at pH 5.5 (mix 23.25 mL of 0.05 M
citric acid pH 5.5 with 76.75 mL of 0.05 M trisodium citrate pH 5.5), 0.1%
CHAPS, 1 mM DTT.
4
2-4 Fluorometric assays
Recombinant proteases are supplied from Calbiochem.
Buffer: 50 mM citrate buffer, pH 5.5, 1 mM DTT.
Substrates: Protease activity assays are performed on a Mithras LB940
(Berthold technologies) by measuring the release of fluorescent N-Acetyl-
Methyl-Coumarin (Nhmec) in citrate buffer (pH 5.5) at 37°C. Specific
substrates for AEP (Z-Ala-Ala-Asn-NHMec), CatB (Z-Arg-Arg-NHMec),
CatB/L (Z-Phe-Arg-NHMec), CatG (Suc-Ala-Ala-Ala-Pro-Phe-NHMec), CatH
(Z-Arg-NHMec) and CatS (Z-Val-Val-Arg-NHMec) are from Bachem.The
substrate for CatK (Z-Gly-Pro-Arg-NHMec) is from Peptide Institute Inc.
2-5 Purification of endosomes and lysosomes
Magnetic nanoparticles are from Turbobeads.
Homogenization buffer (HB): 3 mM imidazole, 8% sucrose, 2 mM DTT and 5
µg/ml of DNase.
Wash buffer: PBS, 0.1% BSA.
Lysis buffer: 50 mM Tris PH7.4, 150 mM NaCl, 0.5% NP40, 2 mM MgCl2
and a tablet of cocktail inhibitors (Roche).
Magnetic stand for eppendorf tubes (Eppendorf).
2-6 10% Acrylamide Gels for SDS-PAGE
Buffer Lower TRIS 4X: 1.5 M Tris, 0.4% SDS, pH 8.8.
Buffer Upper TRIS 4X: 0.5 M Tris, 0.4% SDS, pH 6.8.
Poor resolving gel (10%): mix 6.7 ml (Stock Acrylamide/Bis 30%/0.8%) with
5 ml Lower 4X, 8.3 ml water, 70 µl Amonium persulfate (AP) 10% and 10 µl
Teemed. Add EtOH on top of the gel. It should take 30 minutes to
polymerise at room temperature. Once resolving gel is set, pour off EtOH.
Rinse with DI water. Poor stacking gel: mix 1.7 ml (Stock Acrylamide/Bis
30%/0.8%) with 1.25 ml Upper 4X, 7 ml water, 60 µl AP 10% and 20 µl
5
Teemed. Load stacking solution onto the top of the resolving gel. Insert gel
comb carefully. It should take about 10-15 minutes to polymerize at room
temperature.
Running buffer: Tris 10 g, Glycine 144 g, SDS 10 g, in 1L of water.
2-7 Staining/Destaining buffer
Staining buffer: dissolve 0.6g of blue coomassie (Sigma) in 195 ml of
water and add 75 ml of propanol-2 together with 30 ml acetic acid.
Destained buffer: 10% acetic acid, 20% propanol-2 and 70% water.
3- Methods
3-1 cDNAs (0.5 µg) encoding the protein of interest are in vitro translated
with TNT mix, T7 buffer, T7 RNA polymerase, rabbit reticulocytes and 10 µCi
of methionine labeled with S35. Alternatively recombinant purified proteins
can be used as substrates.
3-1 Activity of the proteases is assessed using specific fluorometric
substrates. 10 ng of cathepsins B, D, G, K, B/L, S or AEP are incubated with
their specific substrates (see Materials) respectively for different times. To
calculate the specific activity of each protease (µmole of substrate release
per minute), a standard curve is obtained using different concentrations of
NHmec (from 0.2 to 2 µM).
3-3 Endosomes and lysosomes are purified using magnetic nanoparticles of
20 nm of diameter. 107 dendritic cells are incubated with 60 µl of magnetic
nanoparticles (10 mg/ml) for 30 minutes at 4°C, pulsed for 20 min at 37°C in
1ml of IMDM medium alone and chased for 100 min in 3 ml of complete
medium supplemented with 10% FCS and 10 ng/ml of rGM-CSF. Cells are
then washed 3 times with cold PBS, 0.1% BSA and resuspend in 1 ml of HB.
Cells are mechanically disrupted by passing them through a 25G needle for
about 30 times in order to have 80% mortality. Endosomes and lysosomes
6
are purified by magnetic separation at 4°C on a magnetic eppendorf stand.
They are washed 10 times with cold PBS supplemented with a tablet of
cocktail inhibitors (Roche) and lysed in 50 µl of lysis buffer for 20 min on ice.
The endosomes/lysosomes are then centrifuged at 12000rpm at 4°C for 10
min to get rid of the magnetic particles and can be either frozen or used
immediately.
3-4 Radiolabelled proteins (5 µl of the reaction) or recombinant purified
proteins (10 µg )are incubated with proteases (1 to 15 U) or with purified
endosomes/lysosomes (1µg) from wild type cells or cells lacking different
cathepsins (B or D or G or K or L or S or AEP etc!) for 2 to 4 h in a final
volume of 30 µl in 50 mM citrate buffer pH 5.5, supplemented with 0.1%
CHAPS and 1mM DTT. The reaction is stopped by addition of lysis buffer
(10 µl of 4X Laemli buffer supplemented with 8%ofβ-mercapto ethanol).
3-5 Heat aliquots at 95°C for 10 min. Load samples
3-6 Following electrophoresis, open the gel plates with a spatula. For
radiolabelled samples, rinse the gel with water and incubate in a fixation
solution (staining buffer without coomassie) for 30 min to 1h. Rinse the gel
again with DI water and add the enhancer solution (Perkin Elmer) for 30 min.
Rinse the gel and dry it for 1h at 80°C. Develop the autoradiographic film
after few hours or an overnight exposure at -80°C. For recombinant proteins
digested in vitro, the gels are incubated in the staining buffer for 2h and
wash extensively with distained buffer.
3-7 In vitro digestion assays are stopped by adding the respective protease
inhibitors (20 µM MVO 26630 for AEP; 10 nM LHVS for cathepins B, L,S; 10
µM Boc-Phe-Leu-NHNH-CO-NHNH-Leu-Z for cathepsin K;10 µM inhibitor I
cat: 219372 for cathepsin G , 10 µM pepstatin A for cathepsins D, E). 2x106
of pAPCs (dendritic cells for example) are fixed with 200 µl of 0.1%
glutaraldehyde-PBS for 30 seconds at 37°C and the reaction is stopped by
adding 200µl of 0.2M Glycine, pH 7.4. Cells are extensively washed with a
7
solution of RPMI 1640 supplemented with 1% FCS. They are then
distributed in 96 well plates (Flat bottom) at 5x104 cells in 50 µl per well. The
invitro digestion assays are added to the antigen presenting cells (50 µl)
together with100 µl of 105 T cells (ratio 2:1) for 24h. Stimulation of T cells is
measured by release of interleukine 2 using an ELISA kit (e-biosciences).
4- Notes
Note 1: To assess that the protease inhibitor you have used is indeed
specific for the protease you want to block, you can use the Fluorometric
assay to test it (see Materials 2-4).
Note 2: The in vitro digestion assays are most of the times performed in an
acidic pH (citrate buffer, pH 5.5). When added to the pAPCs, it can kill them.
To avoid this problem, you have to raise the pH of your buffer by adding few
drops of NaCl.
5- Ackowledgements
This work was supported by INSERM (ANR 2010 MIDI 008 01), an ARC
Ph.D. fellowship to S.M and an Institut Curie Ph.D. fellowship to M.T.
6- References
1- Kvist S, Wiman K, Claesson L, Peterson P.A, Dobberstein B (1982)
Membrane insertion and oligomericasselbly of HLA-DR histocompatibility
antigens. Cell 29: 61-69.
2- Lotteau V, Teyton L, Peleraux A, Nilsson T, Karlsson L, Schmid S.L,
Quaranta V, Peterson P.A (1990) Intracellular transport of class II MHC
molecules directed by invaraint chain. Nature 348: 600-605.
3- Rawlings N.D,Barret A.J (1993) Biochem J 290:205-218.
4- Nakagawa T, Brissette W.H, Lira P.D, Griffiths R.J, Petrushova N, Stock
J, McNeish J.D, Eastman S.E, Howard E.D, Clarke S.R.M, et al (1999)
Impaired invariant chain degradation and antigen presentation and
8
diminished collagen induced arthritis in cathepsin S null mice. Immunity 10:
207-217.
5- Riese R.J, Wolf P.R, Bromme D, Natkin L.R, Villadangos J.A, Ploegh H.L,
Chapman H.A (1996) Essential role for cathepsin S in MHC class II-
associated invariant chain processing and peptide loading. Immunity 4: 357-
366.
6- Nakagawa T, Roth W, Wong P, Nelson A, Farr A, Deussing J, Villadangos
J.A, Ploegh H, Peters C, Rudensky A.Y (1998) Cathepsin L: critical role in Ii
degradation and CD4 T cell selection in the thymus. Science 280: 450-453.
7- C Watts (2011) The endosome-lysosomes pathway and information
generation in the immune system.Biochem etBiophysActa 8: 4-6.
8- Manoury B, Hewitt E.W, Morrice N, Dando P.M, Barrett A.J, Watts C
(1998) An asparagynil endopeptidase processes a microbial antigen for
class II MHC presentation. Nature 396: 695-699.
9- Manoury B, Mazzeo D, Fugger L, Viner N, Ponsford M, Streeter H, Mazza
G, Wraith D.C, Watts C (2002) Destructive processing by asparagine
endopeptidase limits presentation of a dominant T cell epitope in MBP. Nat.
Immunol 3:169-174.
10- Moss C.X, Villadangos J.A, Watts C (2005) Destructive potential of the
aspartyl protease cathepsin D in MHC class-restricted antigen processing.
Eur J Immunol 35: 3442-3451.
11- Schein C.H (1989) Production of soluble recombinant proteins in
bacteria. Nat Biotech 7: 1141-1149.
12- Mitraki A, King J (1989) Protein folding intermediates and inclusion
bodies formation. Nat Biotech 7: 690-697.
13- Lai M.Z, Ross D.T, Guillet J-G, Briner T.J, Gedter M.L, Smith J.A (1987)
T lymphocyte response to bacteriophage l repressor cI protein . recognition
of the same peptide presented by Ia molecules of different halotypes. J.
Immunol 139:3973-3977.
14- Matthews S.P, Werber I, Deussing C, Peters C, Reinheckel T, Watts C
(2010) Distinct proteases requirement for antigen presentation in vitro and in
vivo. J Immunol 184: 2423-2431.
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Asparagine Endopeptidase Controls Anti-Influenza VirusImmune Responses through TLR7 Activation
Sophia Maschalidi1,2, Signe Hassler1,2, Fany Blanc3,4, Fernando E. Sepulveda2,5, Mira Tohme1,2,6,
Michel Chignard3,4, Peter van Endert1,2, Mustapha Si-Tahar7,8, Delphyne Descamps1,2,
Benedicte Manoury1,2*
1 INSERM, Unite 1013, Paris, France, 2Universite Paris Descartes, Sorbonne Paris Cite, Faculte de Medecine, Paris, France, 3Unite de Defense Innee et Inflammation,
Institut Pasteur, Paris, France, 4 INSERM, Unite 874, Paris, France, 5 INSERM, Unite 768, Paris, France, 6 INSERM, Unite 932, Institut Curie, Paris, France, 7 INSERM, Unite 1100,
Tours, France, 8 Faculte de Medecine F. Rabelais, Tours, France
Abstract
Intracellular Toll-like receptors (TLRs) expressed by dendritic cells recognize nucleic acids derived from pathogens and playan important role in the immune responses against the influenza virus (IAV), a single-stranded RNA sensed by differentreceptors including TLR7. However, the importance of TLR7 processing in the development of anti-viral immune responsesis not known. Here we report that asparagine endopeptidase (AEP) deficient mice are unable to generate a strong anti-IAVresponse, as demonstrated by reduced inflammation, cross presentation of cell-associated antigens and priming of CD8+ Tcells following TLR7-dependent pulmonary infection induced by IAV. Moreover, AEP deficient lung epithelial- or myeloid-cells exhibit impaired TLR7 signaling due to defective processing of this receptor. Indeed, TLR7 requires a proteolyticcleavage by AEP to generate a C-terminal fragment competent for signaling. Thus, AEP activity is critical for TLR7 processing,opening new possibilities for the treatment of influenza and TLR7-dependent inflammatory diseases.
Citation: Maschalidi S, Hassler S, Blanc F, Sepulveda FE, Tohme M, et al. (2012) Asparagine Endopeptidase Controls Anti-Influenza Virus Immune Responsesthrough TLR7 Activation. PLoS Pathog 8(8): e1002841. doi:10.1371/journal.ppat.1002841
Editor: Andrew Pekosz, Johns Hopkins University - Bloomberg School of Public Health, United States of America
Received March 15, 2012; Accepted June 19, 2012; Published August 16, 2012
Copyright: ß 2012 Maschalidi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. This study was supportedby grants from INSERM (ANR 2010 MIDI 008 01 to B. M and ANR 2008 NKTVir to M. S), an ARC PhD fellowship to S. M, an Institut Curie Ph.D. fellowship to M. T, FRMand ANR post-doc support respectively to S. H and D. D.
Competing Interests: The authors declare no competing financial interests..
* E-mail: [email protected]
Introduction
Influenza is a common respiratory disease where viral virulence
can either cause just a moderate sickness or a severe pathology
leading to hospitalisation or even death. There are studies
demonstrating that IAV infection induces severe and aggressive
innate response, manifested with excessive cytokine production by
alveolar macrophages and respiratory epithelial cells [1,2]. This
innate immune response triggers the activation of professional
antigen-presenting cells (APCs) leading to the initiation of adaptive
immunity to eradicate the virus. Thus, CD8+ T cell priming to
IAV requires antigen presentation by activated dendritic cells
(DCs) that express co-stimulatory molecules and promote T cell
differentiation and activation. Recent work has shown that tissue
resident DCs from the lung are responsible for the presentation of
exogenous antigens and subsequently the cross priming of T cells
in a Toll like receptor 7 (TLR7)-dependent fashion [3,4]. TLR7
senses single-stranded RNA from influenza viruses within the
endosomes and has been shown to be essential in the induction of
anti-viral immune responses to IAV [1,5,6,7,8].
Toll like receptors (TLRs) detect a wide variety of microbial
products and in DCs they are crucial in linking innate to adaptive
immunity [9]. TLRs contain several leucine rich repeats (LRR) in
an extracellular loop, a trans-membrane domain and a cytosolic
domain and are expressed either at the plasma membrane or in
the endosomal/lysosomal organelles. TLR stimulation is linked to
MyD88 or TRIF-dependent signaling pathways that regulate the
activation of different transcription factors, such as NF-kB [10].
Specific interaction between TLRs and their ligands activates NF-
kB resulting in enhanced inflammatory cytokine responses,
induction of DC maturation and expression of chemokine
receptors [11]. Little is known about how intracellular TLRs
(TLR3, 7, 9) and their ligands are targeted to the endocytic
pathway. Intracellular TLRs are sensitive to lysomotropic agents
that neutralize acidic compartments such as chloroquine or
concanamycin B indicating a role for endo/lysosomal proteases
for their signaling. Indeed, recent findings have described the
importance of proteolysis for TLR9 function [12,13]. It has been
shown that murine TLR9 is non functional until it is subjected to
proteolytic cleavage in the endosomes. Upon stimulation, full-
length (FL) TLR9 is cleaved into a C-terminal (C-ter) fragment
sufficient for signaling. Many proteases, mainly cathepsins, have
been shown to participate in this process in macrophages and in
different cell lines [12,13,14]. However, in primary DCs, cathepsin
K (CatK) and asparagine endopeptidase (AEP) are important in
TLR9 processing. In CatK deficient DCs, TLR9 signaling was
totally abrogated and in DCs lacking AEP, TLR9 cleavage in
phagosomal compartments as well as CD4+ antigen specific T cell
proliferation was greatly reduced upon CpG stimulation [15,16].
Still, it is unclear whether TLR7 is also subject to proteolysis
[12,13,17] and whether TLR7 processing is an important criterion
for the immune response to influenza infection
PLOS Pathogens | www.plospathogens.org 1 August 2012 | Volume 8 | Issue 8 | e1002841
Here, we describe for the first time that a protease, AEP, plays
an important role in anti-influenza virus immune responses.
Indeed, AEP-dependent TLR7 activation mediates inflammation,
cross presentation of cell-associated antigens and cross priming of
CD8+ T cells upon lung IAV infection. We demonstrate that AEP
activity is critical for TLR7 processing in vitro and signaling in vivo.
Altogether, these data indicate that endosomal processing is a
prerequisite for intracellular TLR signaling and identify AEP as a
major actor in anti-viral immunity.
Results
TLR7-dependent influenza virus inflammation and crosspresentation of cell associated antigens require AEPTo address the contribution of AEP in the innate immune
response to influenza virus-infection, wild type (wt) and AEP
deficient mice (AEP2/2) were infected with a sub-lethal dose of IAV
(100 pfu) and the inflammation was monitored in the lungs at days 4
and 8 post-infection [18]. In AEP2/2 mice, significant inhibition of
cytokine and chemokine secretion associated with influenza virus-
induced pneumonia, including keratinocyte chemo-attractant (KC),
interleukin 6 (IL-6), and interleukin 12 (IL-12), was detected
compared to wt mice (Figure 1A). In addition, interferon gamma
(IFN-c) and interferon alpha (IFN-a) production was also reduced in
AEP2/2 mice infected with IAV (Figure 1A and Figure S1A). No
difference in IFN-bmRNA expression was detected between wt and
AEP deficient mice (Figure S1B).
As NF-kB is the major pro-inflammatory transcriptional factor
and regulates the induction of most inflammatory cytokines [19],
we thus analyzed the contribution of the NF-kB pathway during
the in vivo IAV infection. We used an adenovirus containing an
NF-kB response element linked to a luciferase reporter gene (Ad-
NF-kB-luc) [20]. Control WT or AEP2/2 mice infected with Ad-
NF-kB-luc alone presented weak but similar bioluminescence
scores (data not shown). Wt mice co-infected with the Ad-NF-kB-luc and IAV developed an important inflammatory reaction in
lung tissue with a peak of NF-kB-activity at day 3, corresponding
to the maximum of viral replication. In contrast AEP2/2 mice
showed a moderate NF-kB activity (Figure 1B). Yet, the absence of
AEP did not diminish the accumulation of innate inflammatory
infiltrate characterized as macrophages/monocytes, granulocytes,
and dendritic cells upon IAV administration (Figure S1C).
Nonetheless, we noticed that the myeloperoxidase activity, which
mirrored the neutrophil degranulation, was decreased in the
broncho-alveolar lavage (BAL) of AEP2/2 mice compared to wt
mice (Figure S1D). To ascertain whether the difference in
inflammation we observed between wt and AEP2/2 mice was
due to a deficit in viral clearance, viral titers of influenza were
quantified either by mRNA expression of the M2 viral protein
(Figure 1C) and by plaque assays (Figure 1D) in the lungs on days
4 and 8 post infection. No significant difference was detected
between wt and AEP2/2 mice.
TLR7 has previously been shown to sense single-stranded RNA
from viruses including IAV [7]. To confirm the role of TLR7 in the
infectious model of IAV, we performed similar experiments in
TLR72/2mice.We found reduced level of proinflammatory cytokines
in the BAL of TLR72/2 infected mice and to a similar level as in
AEP2/2 infected mice in comparison to wt mice (Figure S2A).
Recently, studies have shown that cross presentation and cross
priming of CD8+ T cells can be enhanced by signaling through
TLRs expressed by DCs. Thus, we tested the hypothesis that
reduced antigen specific T cell proliferation will be detected in AEP
deficient cells and mice following IAV infection. We infected
splenocytes from Balb/C mice (H-2d) electroporated or not with
ovalbumin with the influenza virus PR8, and incubated them with
wt, AEP2/2 or TLR72/2 DCs together with T cells specific for
ovalbumin (OT-I cells). T cell proliferation was analyzed 3 days
later. To exclude that OVA processing was dependent on AEP, we
incubated splenocytes expressing OVA alone with wt or AEP2/2
DCs together with OT-I cells. As shown in Figure S3, OT-I
proliferation was comparable between wt and AEP2/2 cells. In wt
cells, T cell stimulation was increased when DCs were incubated
with IAV infected cells expressing OVA (Figure 2A, upper panel
and Figure S3) but not with BSA-electroporated cells. In contrast,
very weak proliferation of OT-I T cells was seen with AEP2/2 and
TLR72/2 DCs (Figure 2A, middle and lower panel). Similar results
were obtained when a synthetic ligand of TLR7 (imiquimod) instead
of IAV was used to trigger DCs activation (Figure 2A and Figure
S2). In the three cell types (wt, AEP2/2, TLR72/2) tested, OVA
control peptide (SIINFEKL) triggered similar proliferation
(Figure 2A). In addition, a synthetic ligand of TLR3 (poly(I:C))
did also elicit proliferation of OT-I T cells but to the same extent in
wt and AEP2/2 DCs (Figure S3).
To address in vivo whether antigens captured in the lungs could be
cross-presented and prime CD8+ T cells in the mediastinal lymph
nodes (mLNs) after influenza virus infection, we transferred CFSE
labeled OT-I cells specific for ovalbumin into wt or AEP2/2 mice
that had been previously infected with IAV. The mice were then
challenged with ovalbumin or PBS intranasally and 3 days later
proliferation of OT-I T cells in the draining lymph nodes (mLNs) and
in the spleen was analyzed. We detected OT-I T cells proliferation in
OVA-treated mice but not in PBS-treated mice (Figure 2B). T cells
proliferation was stronger in OVA-treated wt mice whereas OT-I
cells proliferate significantly less when injected in AEP2/2 (Figure 2B)
and TLR72/2 mice (data not shown). We conclude that AEP and
TLR7 have a critical role in cross presentation, cross priming and
cytokine secretion upon IAV infection.
Reduced TLR7 signaling in dendritic cells and in micedeficient for AEPThe findings that both AEP2/2 and TLR72/2 mice infected
with IAV secreted less proinflammatory cytokines and had a defect
Author Summary
Influenza A virus, a negative stranded RNA, can causesevere illness in humans and animals and stimulates manyreceptors including Toll like receptors 7 (TLR7). TLRsignaling induces maturation of dendritic cells and theproduction of a variety of inflammatory cytokines that arecrucial for both innate and adaptive immunity. TLR7 is anintracellular receptor, which resides in endosomes andsenses viruses to trigger host defence. Previous data haveshown that TLR9 requires proteolysis to be functional butit is unclear whether other intracellular TLRs (TLR3 andTLR7) are also subject to degradation. Here, we used aprotease deficient mouse model to show the in vivo
importance of TLR7 processing in influenza infection.Inflammation monitored by cytokine release and adaptiveimmunity measured by cross priming of CD8+ T cells wassignificantly reduced in infected protease-deficient animalsin comparison to control animals. We showed that TLR7requires a proteolytic cleavage by a cysteine endopepti-dase in order to be functional. Our findings indicate thatTLR7 processing mediated by a protease, asparagynilendopeptidase, is critical for inducing robust anti-influenzaimmune responses. Given our results, targeting TLR7response in the lungs through proteases may offer newtherapeutic potential in pulmonary infection.
Anti-IAV Immune Response Requires AEP
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in cross priming suggested that AEP might interfere with TLR7
signaling. To test this hypothesis, AEP2/2 and wt immune cells
from myeloid and non-myeloid origins were generated and TLR7
response was monitored. Wt, TLR7 and AEP deficient lung
epithelial cells, which are the first cells that will encounter IAV
after infection, were purified and stimulated with imiquimod or
IAV. Imiquimod response was totally abrogated in TLR72/2
epithelial cells demonstrating the expression of TLR7 in these
cells. In contrast, TLR72/2 epithelial cells were still able to secrete
cytokines following IAV infection probably because TLR7 also
respond to IAV via RIG-I (Figure S2B). Yet, AEP2/2 lung
epithelial cells showed a significant decrease in IL-6 and KC
production upon imiquimod or IAV infection as compared to wt
cells (Figure 3A). We further purified mouse plasmacytoid
dendritic cells (pDCs), key cells involved in the secretion of IFN-
a during viral infection. Upon imiquimod stimulation or IAV
infection, mouse AEP2/2 pDCs showed a significant reduction in
IFN-a production (Figure 3B). As expected, IAV stimulation was
dependent on TLR7 (Figure S4A). To address the role of other
proteases in TLR7 signaling, bone marrow derived DCs (BMDCs)
from AEP2/2, CatB2/2, CatK2/2, CatL2/2 and CatS2/2 mice
were generated and stimulated with TLR4 or TLR7 agonists. We
observed a significant decrease in IL-6 secretion by BMDCs
lacking AEP compared to wt cells upon intracellular TLR7
engagement (Figure 3C), but not when BMDCs deficient for CatB,
CatK, CatL and CatS were stimulated (Figure S4B). Similar
results were obtained in AEP2/2 DCs when IL-12p40 and tumor
necrosis a (TNF-a) were measured or when other TLR7 agonists
Figure 1. Reduced inflammation in IAV-infected AEP2/2 mice. (A) Broncho-alveolar lavage (BAL) fluid levels of KC, IL-6, IL-12 and IFN-c in wtand AEP deficient mice before (NI), 4 d and 8 d after intranasal injection of IAV PR8 strain (100 pfu/mice). (n = 8 animals; graphs show mean6 SEM oftwo independent experiments, * p,0.05, ** p,0.01). (B) NF-kB activity in the lungs of WT or AEP deficient mice infected with IAV. Mice were co-infected at d 0 with IAV (100 pfu) and Ad-NF-kB-luc (2.56108,pfu). Bioluminescence was measured after instillation of 50 ml of luciferine (500 mg/mL)and photon emission was captured at different times post-infection using the IVIS system. Graph shows fold increase of NF-kB activity that representsthe average radiance (photons/sec/cm2) of IAV+Ad-NF-kB-luc infected mice relatively to the average radiance corresponding to Ad-NF-kB-lucinfected mice (n = 7–10 animals, mean6 SEM of three independent experiments, * p,0.05). (C–D) Viral titers in lungs of wt and AEP2/2 mice 4 d and8 d post-viral challenge were determined by qRT-PCR performed on M2 viral protein (C) or by plaque assay (D). (pfu, plaque-forming units, n = 8animals; graphs show mean 6 SEM of two independent experiments).doi:10.1371/journal.ppat.1002841.g001
Anti-IAV Immune Response Requires AEP
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were used (Figure 3C). In addition, no differences in IL-6
production were detected between wt and cathepsin- or AEP-
deficient cells when plasma membrane TLR4 was triggered
(Figure S4C). AEP was shown to regulate cathepsin B, H, K and L
maturation [16,21,22]. We have previously reported that the
activity of these cysteine proteases is either not changed or
increased at the steady state in the absence of AEP [16].
Nevertheless, to be sure that the diminution in TLR7 signaling
we detected in AEP2/2 DCs was not influenced by reduced
cathepsin activity, we monitored cathepsins B, K, L and S
activities in the presence of imiquimod in wt and AEP2/2 cells.
Using fluorogenic substrates selective for CatB, CatB and CatL,
CatK or CatS, we found an increase in the activity of these
cysteine proteases in AEP2/2 DCs in comparison to wt cell
(Figure S4D). These data indicate that impaired TLR7 signaling in
AEP deficient DCs is not associated with reduced activity of other
cathepsins. In contrast, in cathepsin K deficient DCs, AEP activity
was decreased (Figure S4E) which might explain the weak but not
significant reduction of TLR7 signaling detected in cells lacking
CatK. Together these results demonstrate that cells from different
origins lacking AEP have diminished cytokine secretion upon
TLR7 activation and IAV infection.
To investigate the role AEP plays in TLR7-stimulation of DCs
in vivo, we next assessed the ability of AEP-deficient DCs to mature
phenotypically and to secrete pro-inflammatory cytokines. It was
previously reported that DCs are the main target of TLR
stimulation after two hours of TLR ligands injection in mice
[23]. DC maturation in the spleen was examined after intravenous
Figure 2. Impaired cross presentation in AEP deficient DCs and mice following IAV infection. (A) Proliferation of OT-I T cells cultured withDCs from wt, AEP2/2 or TLR72/2 incubated with splenocytes from Balb/C mice (H-2d) electroporated with OVA or BSA and infected with PR8 virus orstimulated with imiquimod. SIINFEKL was used as an OVA-peptide control. Results are representative of three independent experiments. (B)Proliferation of OT-I T cells in the mLNs and the spleen 72 h after adoptive transfer of CFSE-labeled (CD45.1) OT-I T cells into IAV-infected wt orAEP2/2 mice (CD45.2) and intranasal treatment with PBS (gray histogram) or 120 mg of OVA (white histogram) 24 h later. Cells are gated on CD45.1and histograms are representative of one mouse per group (left panel) and right panel represents the percentage of OT-I proliferating cells (n = 4animals, mean 6 SEM, * p,0.05, ** p,0.01).doi:10.1371/journal.ppat.1002841.g002
Anti-IAV Immune Response Requires AEP
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injection with imiquimod or LPS. In control mice, both LPS and
imiquimod induced an increased expression of CD40 and CD86
in the CD11c+ spleen cells. These responses were compromised in
AEP2/2 mice injected with imiquimod (Figure 4A). In addition,
we consistently observed attenuated IL-6 and IL-12p40 secretion
in the serum of AEP2/2 mice following TLR7 stimulation as
compared to wt mice (Figure 4B). To further investigate that the
decrease in TLR7 signaling observed in vivo was specific to AEP,
Figure 3. AEP activity is required for full cytokine production following TLR7 stimulation. (A, B) IL-6, KC or IFN-a secretions insupernatants of AEP+/+ (white bars) or AEP2/2 (black bars) lung primary epithelial cells (A) or pDCs activated (B) with 10 mg/mL of imiquimod or withthe IAV virus PR8 heat killed (HK) or live at a multiplicity of infection= 1 or 5 for 16 h or 24 h. (n = 2–3; mean 6 SEM, * p,0.05, ** p,0.01,*** p,0.001). (C) BMDCs from AEP2/2 mice (black bars) and from their wild type littermates (white bars) were stimulated with different TLR ligandsfor 16 h and secretion of IL-6, IL-12p40 and TNF-a in supernatants was measured by ELISA. (n = 2–6, mean6 SEM, * p,0.05, ** p,0.01, *** p,0.001).doi:10.1371/journal.ppat.1002841.g003
Anti-IAV Immune Response Requires AEP
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we performed the same experiments in CatB deficient mice as we
have noticed a little reduction in TLR7 stimulation in BMDCs
lacking CatB (Figure S4B). We noticed similar or even increase
expression of costimulatory molecules in spleen CD11c+ cells
purified from CatB2/2 mice and similar IL-6 secretion in the
serum of CatB2/2 mice, as compared to wt mice (Figures S5A and
S5B). We conclude that, in vivo, AEP is required for the secretion of
inflammatory cytokines and for the phenotypic maturation of
CD11c+ cells induced by TLR7 engagement.
AEP generates a TLR7 C-ter fragmentWe next addressed whether AEP could process TLR7 in vitro.
Radiolabelled mouse TLR7 was incubated with different recom-
binant cysteine (cathepsins B, K, L, S) and aspartic proteases
(cathepsin D) harboring the same enzymatic activity. Upon
incubation of TLR7 with different doses of recombinant AEP,
TLR7 FL was degraded to produce one major band of 60 kDa
size (Figure 5A). In vitro translated TLR7 digested with a higher
concentration of AEP showed two distinct bands migrating
approximately around 60 and 30 kDa (TLR7 fragments, Figure
S6A). As shown in Figure S6A, cathepsin L (CatL) and cathepsin S
(CatS) were also able to degrade totally full-length (FL) TLR7.
However, when decreasing CatL and CatS concentrations were
used to digest FL TLR7, no defined processing products were
detected (data not shown). In vitro digestion assays using human
TLR7 also showed processing of full-length TLR7 by AEP and
cathepsins L and S (Figure S6B). To verify whether the fragment
generated upon AEP digestion had the same size as a putative C-
terminal (C-ter) fragment, we predicted a candidate cleavage site
in TLR7 by homology with TLR9 [12] (Figure 5B) and translated
this C-ter cDNA in vitro (Figure 5C). Indeed, the putative candidate
TLR7 C-ter fragment migrated approximately at the same size as
the TLR7 product observed after TLR7 digestion by AEP
(Figures 5A and 5C). We next assessed if the TLR7 C-ter
fragment was produced in cells. We transfected fibroblasts with
cDNAs encoding HA-tagged full length or HA-tagged C-terminal
TLR7 and 48 hours later, transfected cells were lysed and blotted
with an antibody directed against HA. In cells stimulated with
imiquimod for 1 h, TLR7 full-length was detected as well as two
fragments migrating around 80 kDa and 60 kDa (Figure 5D). The
60 kDa processing fragment, which appeared upon imiquimod
incubation, migrated at the same size as the TLR7 C-ter we
designed in vitro (Figures 5C and 5D). In addition, to assess whether
the TLR7 C-ter fragment was produced in primary DCs, we
purified phagosomes from wt and AEP2/2 cells fed with magnetic
particles. At the steady state, TLR7 FL and C-ter were observed in
early (20 minutes) and late (120 minutes) phagosomes. In the
presence of imiquimod, TLR7 cleavage occurs more rapidly and
was already detectable after 20 min (Figure S7A).
Figure 4. Decreased cytokine and co-stimulatory molecule expression in AEP2/2 DCs in vivo upon TLR7 ligand sensing. (A) FACSanalysis of in vivomaturation of spleen CD11c+ cells 4 h after i.v. injection of 10 mg of imiquimod (left panel) or 1 mg of LPS (right panel) compared tono TLR ligand stimulation equivalent to 1. (B) IL-6 (left panel) and IL-12p40 (right panel) secretion were measured in serum of AEP+/+ or AEP2/2 mice2 h after i.v. injection with imiquimod or PBS. (n = 9 animals for imiquimod; n = 2 animals for PBS; mean 6 SEM for A and B, ** p,0.01, *** p,0.001).doi:10.1371/journal.ppat.1002841.g004
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Figure 5. AEP generates a TLR7 C-ter fragment in vitro and in primary DCs. (A) In vitro transcription and translation of mTLR7 FL followed by2 h digestion of radiolabelled mTLR7 FL with different doses of rAEP (3.25 to 15U) (left panel). ImageJ software quantification of TLR7 digestion with15U rAEP (right panel). Mean of three different experiments normalized to undigested TLR7. *** p,0.001 (ND: non-digested). (B) Schematicrepresentation of TLR7 protein and its cleavage fragments. (C) In vitro transcription and translation of mTLR7 FL and C-ter cDNAs labeled with S35. (D)Fibroblast were transfected with cDNAs encoding for HA-tagged TLR7 FL or C-ter together with UNC93B1. 48 h later, cells were stimulated withimiquimod for 1 h and western blot was performed with an anti-HA antibody. (E) Anti-TLR7 and MyD88 immunoblot of HPLC fractions of lysates fromAEP+/+ (left panel) or AEP2/2 BMDCs (right panel) treated with imiquimod (5 mg/mL) for 60 min. (C–E) Representative data from three independentexperiments. (F) Detection of MyD88 and TLR7 interaction using DuoLink in situ with anti-MyD88 and anti-TLR7 specific mAbs on AEP+/+ or AEP2/2
BMDCs stimulated or not with imiquimod for 30 min. PLA signals are shown in green and the nuclei in blue. Quantification of mean fluorescenceusing Image J software (n = 11), *** p,0.001.doi:10.1371/journal.ppat.1002841.g005
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To investigate whether the TLR7 C-ter fragment is generated in
AEP2/2 cells and recruits the adaptor molecule MyD88, we
stimulated wt or AEP2/2 BMDCs with imiquimod and fraction-
ated TLR7 and MyD88 on the basis of size exclusion chroma-
tography as we previously did for TLR9 [16]. Similar chroma-
tography profiles were obtained for both cell types (data not
shown). After 60 min of imiquimod stimulation in wt cells, two
TLR7 products migrating around 80 kDa and 60 kDa (Figure 5E,
left panel) were detected. As before, the 60 kDa product had a
similar size as the TLR7 C-ter fragment we observed in the in vitro
translation assay (Figures 5C and 5D). In the absence of AEP, no
TLR7 processing fragment of 60 kDa was detected (Figure 5E,
right panel). We then monitored if MyD88 co-eluted with the C-
ter form of TLR7. Indeed, in wt cells we could detect MyD88 in
fraction 47 where TLR7 C-ter product was present (Figure 5E, left
panel). To look at MyD88-TLR7 interaction, we used the
DuoLink method that gives a signal if two different antibodies
are localized within 40 nm of each other. This method allows us to
detect and visualize TLR7 conjugated to MyD88. We could
confirm association between MyD88 and TLR7 in wt cells only
when the cells were stimulated with imiquimod (Figure 5F, upper
panel). In AEP2/2 cells, significatively less signal was detected
(Figure 5F, lower panel).
In conclusion, AEP generates a TLR7 processing fragment,
which is produced in wt cells upon imiquimod stimulation but not
in AEP2/2 DCs. In addition, a reduced association between
cleaved TLR7 and the adaptor protein MyD88 is observed in
AEP2/2 cells.
TLR7 C-terminal fragment is competent for signaling andis dependent on acidic pHWe next assessed whether the TLR7 C-ter fragment is
functional. TLR9 C-ter fragment containing a part of the ecto-,
trans-membrane and cytoplasmic domains has been shown to be
fully competent for signaling at a similar level as FL TLR9 [12].
We next wondered whether the same was true for TLR7. Indeed,
the C-terminal fragment of TLR7 was sufficient to initiate
signaling and even to a higher level than full-length TLR7 when
expressed in TLR72/2 DCs upon different doses of imiquimod
stimulation (Figures 6A, left panel, S7B and S7C). Neither the
empty vector nor the TLR7 N-ter fragment could restore
signaling in DCs lacking TLR7 (Figure 6A, left panel). As
expected, LPS-stimulated cells transfected with the same
constructs secreted similar amount of IL-6 (Figure 6A, right
panel). In addition, cells pretreated with the specific AEP
inhibitor (MV026630) failed to restore cytokine secretion in FL
TLR7-transfected TLR72/2 DCs (Figure 6B). On the contrary,
TLR7 C-terminal fragment did not require any further process-
ing because its signaling was not reduced when AEP was
inhibited (Figure 6B).
We next tested whether the C-terminal fragment of TLR7 could
restore full TLR7 signaling in DCs lacking AEP. AEP2/2 cells
were transfected with the cDNAs encoding TLR7 full-length
vector or the recombinant C-terminal TLR7 product. After TLR7
stimulation, diminished IL-6 secretion, as expected, was detected
when DCs lacking AEP were transfected with the cDNA encoding
full length TLR7 as compared to wt cells (Figure S8A, left panel).
On the contrary, TLR7 C-terminal fragment restored signaling in
AEP2/2 cells to the same level as in wt cells after imiquimod
stimulation as indicated by IL-6 secretion (Figure S8A, left panel).
As a control, LPS-stimulated cells transfected either with full-
length or C-terminal TLR7 plasmids produced same amount of
IL-6 (Figure S8A, right panel). However, we noticed that the
difference in TLR7 response between wt and AEP2/2 DCs
transfected with the cDNA encoding for the FL TLR7 was not as
significant as when AEP2/2 DCs were stimulated with imiqui-
mod. We suspect this might be due to the overexpression of the
TLR7 protein in these experiments. In summary, our results
suggest that TLR7 processing fragment is sufficient and necessary
for TLR7 activity.
AEP is a cysteine protease that requires acidic pH, like most of
the other cysteine and aspartic proteases, for its optimum activity
[24]. We and others have previously shown that the endosomal
pH of DCs is rather neutral and decreases only in lysosomal
compartments [16,25]. We then decided to monitor the pH in
endosomes (where most likely TLR7 traffics) and lysosomes of
DCs upon imiquimod stimulation using specific probes [25,26]. A
drastic drop of endosomal pH was detected upon imiquimod
stimulation, which persisted upon time and was also detected in
lysosomes, in comparison to unstimulated cells (Figure S8B). The
drop of pH upon imiquimod stimulation was also observed in
AEP deficient DCs (Figure S6B). This increase in endosomal/
lysosomal acidification correlates with a boost in AEP activity
measured in total cell lysate (Figure S8C). This enhancement of
AEP activity (about 2 fold) was particularly striking in phago-
somes where most likely cleavage of TLR7 occurred after
imiquimod stimulation (Figure S8D). Cathepsins B, K, L and S
activities were also increased upon TLR7 stimulation (Figure
S8E) indicating that it was not specific for AEP. To verify the
importance of endosomal acidification in TLR7 signaling, we
treated cells with concanamycin B (a drug interfering with pH
acidification by blocking the recruitment of the Vo subunit of the
V-ATPase complex) and measured IL-6 secretion after imiqui-
mod stimulation. Treatment with concanamycin B completely
abrogated TLR7 signaling but not TLR4 response as expected
(Figure 6C). Furthermore, endosomal acidic pH was still required
for the TLR7 C-ter product to signal suggesting that optimal
ligand receptor binding might occur at low pH [27] (Figure 6D)
and/or acidification might be required for a change of
conformation allowing the TLR7 C-ter fragment to bind the
adaptor molecule MyD88 and to signal. Thus, TLR7 processing
requires low pH and AEP activity.
Mutation of AEP cleavage site between LLR 14–15abrogates TLR7 signalingAEP cleaves native antigens at asparagine sites [28]. So, it is
tempting to speculate that AEP cleaves directly TLR7. Indeed,
the residues 450–479 in TLR7 situated between the two leucine
rich-regions (LRR 14–15) described to be susceptible for
proteolysis and to be a target for AEP cleavage in TLR9
[12,13,16], contain also an asparagine that can be a putative
cleavage site for AEP. To test this hypothesis, we mutated
asparagine residue 478 to glutamine. We first investigated the
intracellular localization of this mutant and wt TLR7 when
expressed in transfected in fibroblasts. To allow proper TLR
trafficking, wt or mutated TLR7 cDNAs were transfected
together with a cDNA encoding for the chaperone molecule,
UNC93B1 [29]. At the steady state, both wt and mutated TLR7
reside in the ER (Figure 7A, upper panel). Indeed, we could
observe colocalisation between UNC93B1 (an ER marker) and
both TLR7 constructs (Figure 7B, left panel). Upon imiquimod
stimulation, wt and mutated TLR7 traffic to LAMP positive
lysosomal compartments (Figure 7A, lower panel). No difference
in intracellular localization was observed between TLR7 wt and
the N478Q mutant suggesting that trafficking of TLR7 mutant is
not impaired (Figure 7B, right panel). We then tested whether this
mutant was able to signal following imiquimod stimulation when
expressed in fibroblasts and TLR72/2 DCs. We observed 70% to
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90% of decrease in IL-6, KC and IL-12p40 secretion when
TLR7 mutant was activated with imiquimod but not with LPS
compared to wt TLR7 (Figures 7C, 7D and S7D). Transfection
efficiency assessed by cytometry was the same for both constructs
(20% in DCs and 90% in fibroblasts). Altogether these results
suggest a direct cleavage of TLR7 by AEP generating a C-
terminal fragment fully competent for signaling.
Discussion
Influenza A virus is the agent of one of the most common
infectious diseases and remains a major public health burden.
Numerous studies have shown that the main cause of death after
IAV infection is due to a ‘‘cytokine storm’’ or excessive secretion of
proinflammatory cytokines [1]. Indeed, pharmacological interven-
tion in order to limit cytokine responses and thus to reduce the
immunopathogenicity of influenza virus has been shown to be
beneficial for the host [1,30,31]. Signaling pathways in host IAV
infected cells can be induced by a variety of viral components,
among them double- and single-stranded RNA which are sensed
by the cytosolic RNA helicases, RIG-I, and the TLR family
members TLR7 and TLR3 [6,32,33,34]. So far, the therapeutic
approaches have targeted these last receptors.
Based on our previous results showing the critical role of AEP in
the processing and signaling of another intracellular TLR, TLR9,
it was tempting to speculate that AEP might be involved in TLR7
activation upon IAV infection. Interestingly, mice lacking AEP
were unable to generate a strong antiviral immune response when
challenged with the influenza virus strain PR8 described
previously to be recognized by TLR7 [5,6,7,8]. This was not
due to a deficit in viral clearance because the viral titers of IAV
remain the same in wt and AEP deficient mice. By contrast, lung
epithelial cells, that provide the first spatial barrier against this
respiratory virus, from AEP deficient mice responded much less to
that viral challenge. Moreover, plasmacytoid dendritic cells that
lack AEP expressed reduced amount of IFN-a compared to wt
cells, demonstrating that the response of the very first sentinels
upon viral infection is reduced in the absence of AEP. Besides this
attenuated innate immune response, we were able to observe that
the adaptive immune response in AEP deficient mice was also
severely impaired. CD8+ T cell priming to IAV requires antigen
presentation by activated DCs that express costimulatory mole-
cules, which in turn promote T cell-differentiation and activation.
We demonstrate that in AEP deficient mice the ability to initiate
an immunogenic CD8+ T cell response to an exogenous antigen
that is not synthetized by the antigen presenting cells was severely
Figure 6. TLR7 C-ter is functional and requires acidic environment. (A) IL-6 secretion in TLR72/2 BMDCs transfected with pcDNA3.1, FL, C-teror N-ter TLR7 cDNAs and stimulated with 5 mg/mL of imiquimod or 10 ng/mL of LPS for 16 h. (n = 3–4; mean 6 SEM, * p,0.05, ** p,0.01). (B) IL-6secretion in TLR72/2 BMDCs transfected with FL or C-ter TLR7 and stimulated with imiquimod as above and treated with or without 25 mMMV026630 (AEP inhibitor). (n = 3; mean 6 SEM, * p,0.05). (C) IL-6 secretion in BMDCs activated with either 5 mg/mL imiquimod or 10 ng/mL LPS for16 h, in the presence or not of 20 nM of concanamycin B. (n = 3; mean 6 SEM, ** p,0.01, *** p,0.001). (D) IL-6 secretion in TLR72/2 BMDCstransfected with FL or C-ter TLR7 and stimulated with imiquimod and treated as above. (n = 3; mean 6 SEM, * p,0.05).doi:10.1371/journal.ppat.1002841.g006
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compromised. We ruled out the contribution of TLR3 [18] in our
work because TLR3 signaling does not require AEP (data not
shown) and we did not observe difference between wt and AEP2/
2 DCs in OVA cross presentation when TLR3 was stimulated
(Figure S3). Also, we cannot exclude the importance of the
inflammasome in IAV infection [33,35]. In our model, no
difference in IL-1b secretion was detected between wild type
and AEP deficient mice when the IAV PR8 strain was
administered, suggesting that AEP does not play a role in the
activation of the inflammasome (data not shown).
Figure 7. Mutating a putative AEP cleavage site abrogates TLR7 signaling. (A) Immunofluorescence microscopy of resting (top) orimiquimod activated (bottom) fibroblast co-transfected with FL or N478Q TLR7 HA-tagged and UNC93B1-cherry cDNAs and stained for TLR7 (green),LAMP1 (red) and UNC93B1 (red). One representative experiment out of three shown. (B) Quantification of colocalization using Image J software(n = 8). (C) KC secretion in fibroblasts transfected with FL or N478Q TLR7and stimulated overnight with 10 mg/mL imiquimod. (n = 2; mean 6 SEM,* p,0.05). (D) IL-6 secretion in TLR72/2 BMDCs transfected with FL or N478Q TLR7 and stimulated with TLR ligands as above. (n = 4; mean 6 SEM,** p,0.01).doi:10.1371/journal.ppat.1002841.g007
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Recent results have shown that TLR7 is also subject to
proteolytic degradation [17] but the proteases involved in this
process have not been identified and the functionality of this
product has not been determined. Indeed, no difference was
observed between control DCs and DCs lacking different single
cathepsins (Cathepsins B, K, L and S) in cytokines production
following TLR7 stimulation [12,13]. Furthermore, using Z-FA-
fmk, a broad inhibitor of cysteine proteases and caspases, in a
macrophage cell line, partial inhibition (about 30%) in TLR7
response was reported [17]. This altered signaling was not
observed when AEP was blocked. We have not tested macrophage
cell lines. However, using primary alveolar macrophages, we have
not observed any difference in cytokine secretion between AEP-
deficient macrophages and control cells following TLR7 stimula-
tion. Indeed, we and others have shown that DCs behave
differently from macrophages because they have evolved distinctly
to regulate endosomal acidification at the steady state and upon
TLR stimulation [16,25,36,37]. The experiments presented in this
paper establish that TLR7 processing is dependent on AEP in DCs
and epithelial cells. The in vitro cleavage of TLR7 by AEP, the
impaired cytokine secretion in DCs and in mice deficient for AEP
following TLR7 stimulation or in DCs expressing a TLR7 mutant
lacking the AEP cleavage site at position 478 support this
conclusion. Interestingly enough, both TLR7- and TLR9-
processing and -signaling depend on AEP. These two intracellular
TLRs necessitate UNC93B1 for their trafficking [29,38], share
sequence homology [39], have similar expression in certain DC
subtypes and both contribute to the development of some
autoimmune diseases like systemic lupus erythematous [40].
In conclusion, AEP plays a major role in TLR7 signaling in
primary epithelial and dendritic cells and contributes to the
induction of inflammation and CD8+ T cell activation during
influenza virus infection (Figure S9). Given our findings, targeting
TLR7 response in the lungs through AEP may offer new
therapeutic potential in pulmonary infection. Indeed, a specific
inhibitor of AEP (MV026630) is available and could be tested in
such inflammatory diseases.
Material and Methods
Ethics statementAnimals were housed in the Institut Pasteur animal facilities
accredited by the French Ministry of Agriculture to perform
experiments on live mice in appliance of the French and European
regulations on care and protection of the Laboratory Animals (EC
Directive 86/609, French Law 2001-486 issued on June 6, 2001).
Protocols were approved by the veterinary staff of the Institut
Pasteur animal facility (permit number 99.174) and were
performed in compliance with the NIH Animal Welfare Insurance
A5476-01 issued on 02/07/2007.
MiceAEP2/2 mice were generated in C. Peters’ lab (Freiburg) and
backcrossed 11 times on B6 background. Animals were bred in a
pathogen-free environment in accordance with the Institut Curie
guidelines. Cathepsin B, L, S deficient mice were a kind gift from
A.M. Lennon (Paris, France) and mice lacking cathepsin K were
kindly donated by P. Saftig (Germany).
Influenza virusInfluenza A/Puerto Rico/8 [mouse adapted] P2.3 (H1N1, PR8)
virus was generously provided by N. Naffakh (CNRS URA 3014,
Institut Pasteur, Paris, France), was prepared as previously
described [18] and the titer was expressed as plaque forming
units (pfu)/mL [41].
Cells and stimulationsFibroblasts were obtained from the skin of C57Bl/6J mice
following the protocol as previously described [42]. Bone marrow
derived DCs were generated from AEP2/2, CatB2/2, CatK2/2,
CatL2/2, CatS2/2, TLR72/2 mice and their wt littermates as
previously described [16]. Cell differentiation was controlled by
FACS (anti-CD11c, HL3, and anti-CD11b, M1/70, BD biosci-
ences). Splenic pDCs were isolated using mPDCA-1 selection kit
(Miltenyi Biotech, 90% of purity as determined by FACS).
Epithelial cells were isolated from the mouse lung as previously
described [43]. Plated cells in 96-well plate were treated
overnight with the TLR ligand (LPS (Sigma-Aldrich), Imiqui-
mod, poly(I:C), Resiquimod, or Gardiquimod, CL097 (Invivo-
gen)). In some experiments BM-DCs were pre-incubated with
ConB (20 nM, Sigma) for 20 min or for 1 h with the AEP specific
inhibitor: MV026630 (25 mM, laboratory of H. Overkleeft)
before adding the TLR agonist. Cytokines were measured in
supernatants using home-made (IFN-a) or commercial (TNF-a,
IL-6, IL-12p40, KC, IFN-c, RANTES, eBioscience or R&D
Systems) ELISA.
In vivo IAV modelMale mice were anesthetized by ketamine-xylazine and infected
intranasally with 50 ml of PBS containing 100 pfu of PR8 virus.
Airways were washed 460.5 mL of PBS, and the BAL was
collected to further determine cell differential counts (Beckman
Coulter) and FACS. Different cytokines were measured in BALs.
IFN-b protein expression was quantified by quantitative real-time
RT-PCR in total RNA extracted from lung tissue using the
RNeasy Mini Kit (Qiagen). Primer sequences were for murine
IFN-b gene F: 59CACAGCCCTCTCCATCAACT-39 and R: 59-
TCCCACGTCAATCTTTCCTC-39. In other experiments, re-
combinant adenovirus encoding for NF-kB-luciferase (Ad-NF-kB-
luc, Gene Transfer VectorCore, University of Iowa) was
intranasally co-injected (2.56108 pfu) with PR8 virus (100 pfu)
in order to analyze NF-kB activation in the lungs. Photon emission
of the luminescent construct transduced in the lungs was
quantified using the IVIS system (Xenogen Biosciences) after
intranasal injection of luciferine (50 ml, 500 mg/mL) as previously
described [20].
FACS analysisBAL cells were stained with Live/Dead fixable near-IR dead
cell stain kit (Invitrogen) in PBS for live/dead discrimination. Cells
were then incubated with anti-CD16/32 in PBS-1% BSA and
stained with PerCP-Cy5.5-anti-CD11b (clone M1/70), APC-anti-
CD11c (clone HL3), PE-Cy7-anti-Gr-1 (Ly-6G and Ly-6C, clone
RB6-8C5) (BD Biosciences). Cells were fixed with paraformalde-
hyde 2% and analyzed using a CYAN ADP cytometer (Beckman
Coulter) and with FlowJo software.
Quantification of M2 viral protein and particlesTotal RNA was extracted from lung tissue using the RNeasy
Mini Kit (Qiagen) and the M2 viral protein quantification
performed by quantitative real-time RT-PCR as previously
described [20]. Total proteins were extracted from lung tissue in
PBS in order to quantify the remained IAV by determining pfu
present in lung lysates with the method previously described
[41].
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In vitro, in vivo cross-presentation and In vivo DCsstimulationIn vitro cross-presentation assays were performed as previously
described [44]. Briefly, splenocytes from Balb/C mice (H-2d) were
electroporated with 0.5 mg OVA or BSA and infected with PR8
virus (10 pfu) or stimulated with 10 mg/mL imiquimod or 100 mg/
mL poly(I:C) before irradiation (10 Gy) and incubation with DCs.
Then, CFSE labeled OT-I T cells were added to the culture and
the proliferation of T cells was monitored 3 days later. DCs
incubated with SIINFEKL (100 ng/mL) were used as a prolifer-
ation control. In vivo cross-presentation assays were performed as
previously described [4]. Briefly, CFSE labeled CD8+ T cells from
OT-I RAG (CD45.1+) mice were intravenously injected at day 4
into IAV-infected CD45.2+ recipient mice, a day later OVA or
PBS were administered intranasally and mice were sacrificed at
day 8 to monitor proliferation of T cells in the mLNs. Mice were
injected intravenously with TLR agonist or PBS alone and bled
2 h later. Serum cytokine was assessed by ELISA and splenic DCs
were stained with anti-CD11c-APC (HL3), anti-CD86-PE (GL1)
or anti-CD40-PE (3/23) (BD Biosciences) for flow cytometry
analysis.
Size chromatography exclusion, immunodetection andprotease activity506106 BM-DCs were stimulated with Imiquimod (10 mg/mL)
for 60 min. Cells were then lysed in a buffer (50 mM Tris pH 7.4,
150 mM NaCl, 5 mM MgCl2) with 0.5% NP40 for 30 min on ice
and centrifuged at 90000 rpm. The extract was applied to a G-200
Sephadex size exclusion column (Pharmacia). Fractions were
eluted using the previously buffer and 5 mg of protein were
immunoblotted for TLR7 (Imgenex) and MyD88 (Abcam)
expression. Protease activities were assayed on a Mithras LB940
(Berthold technologies) by measuring the release of fluorescent N-
Acetyl-Methyl-Coumarin in citrate buffer (pH 5.5) at 37uC as
previously described [16].
Endosomal pH measurementEndosomal pH measurement has been described [16]. Briefly,
cells were pulsed with 1 mg/mL of FITC- and Alexa-647-labelled
40 kDa dextrans (Molecular Probes) for 10 min at 37uC and
washed with cold PBS-1% BSA. Cells that have endocytosed the
probes were analyzed by FACS at different times.
Phagosome preparation506106 BMDCs were pulsed for 20 min at 37uC with magnetic
particles (Invitrogen) and then chased at 37uC for 100 min in the
presence or absence of imiquimod (10 mg/mL). Cells were then
washed with PBS and mechanically disrupted by passing them
through 25 g needle. Phagosomes were purified by magnetic
separation, washed, and lysed. Equal amounts of proteins were
submitted to separation on a 4–12% SDS NuPAGE Bis-Tris gels
(Invitrogen). Proteins were transferred on a PVDF membrane and
TLR7 immunodetection was realized with rabbit pAb anti-TLR7
(Imgenex).
ConstructsMurine TLR7 constructs (described in Table 1) containing
either the FL sequence, the C-terminal (aa 480–1052) or the N-
terminal part (aa 1–449) followed by a HA-tag were cloned into
pcDNA3.1 by PCR of the pUNO mTLR7-HA plasmid (Invivo-
gen). The full-length mTLR7 construct was mutagenized in its Asn
478 into Gln using the Quick change mutagenesis kit (Stratagene).
35S-labelling of TLR7 protein, digestion assays andtransfection in DCsTLR7 pcDNA3.1 plasmid was transcribed and translated in vitro
using TNT T7 quick Coupled Transcription/Translation system
(Promega) and 10 mCi 35S-methionine (Perkin Elmer). Digestion
assays were performed as previously described [16]. 106 BM-DCs at
day 6 were transfected with 1 mg of cDNA coding for TLR7-FL, -C-
ter or -N-ter using the mouse DC Amaxa kit (Lonza, Germany).
48 h later, cells were harvested and stimulated with TLR agonists.
ImmunofluorescenceCells were fixed with 4% paraformaldehyde for 10 min at RT,
and quenched in 100 mM glycine for 20 min. Fixed cells were
permeabilised and incubated with anti-HA (homemade) and anti-
CD107a LAMP1 (eBIO1, clone D4B) antibodies in PBS-0.2%
BSA-0.05% saponin. Immunofluorescence images were acquired
on a Leica confocal microscope.
Table 1. Sequences of primers used to TLR7 constructs.
Primer name Sequence
TLR7 Not I forward 59-ATA AGA ATG CGG CCG CAC CAT GGT GTT TTC GAT GTG GACA-39
TLR7 C-terminal Not I forward 59-ATA AGA ATG CGG CCG CGG AGC CAC CTT CTT TCT TGCC-39
HA Xho I reverse 59-CCG CTC GAG CGG TTA GGC GTA GTC TGG CAT GG-39
TLR7 N-terminal reverse (first step PCR) 59-AGT TTG AGC ATT AGG ACA AAAG-39
TLR7 N-terminal reverse (second step PCR), 59-CCG CTC GAG TTA GGC GTA GTC TGG CAC ATC ATA GGG GTA AGT TTG AGC AT-39
MHC class I leader sense 59-GGC CGC ACC ATG GTC CCG TGC ACG CTG CTC CTG CTG TTG GCA GCC GCC CTG GCTCCG ACT CAG ACC CGG GCC GGT ACC GC-39
MHC class I leader antisense 59-GGC CGC GGT CCG GCC CGG GTC TGA GTC GGA GCC AGG GCG GCT GCC AAC AGCAGG AGC AGC GTG CAC GGG ACC ATG GTGC-3
primers TLR7 mutant sense 59-TTG CAA ACT TTA ACA CAG GAA ACA TTT GTG TCA-39
TLR7 mutant antisense 59-TGA CAC AAA TGT TTC CTG TGT TAA AGT TTG CAA-39
The N-terminal insert was generated by two PCRs in order to add a HA-tag, using the first PCR product as template for the second PCR. In order to target the C-terminalconstructs to the ER, the leader sequence from murine MHC class I was added by synthesis. The leader-coding oligonucleotide was subsequently inserted in front of theC-terminal previously cloned into pcDNA3.1. The full-length mTLR7 construct was mutagenized in its Asn 478 into Gln using the Quick-change mutagenesis kit(Stratagene).doi:10.1371/journal.ppat.1002841.t001
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DuolinkDuolink (OLINK) was performed according to the manufac-
turer’s instructions. Briefly, DCs were grown on coverslips and
then fixed in 4% paraformaldehyde for 10 min before permea-
bilization in PBS/0.05% saponin/0.2% BSA for 10 min. Cells
were then blocked in 3% BSA/PBS and primary antibodies were
incubated (anti-MyD88 and anti-TLR7). After washing the cells,
PLA probes were added, followed by hybridization, ligation, and
amplification for 90 min at 37uC. Nucleus (DAPI labelling) and
MyD88-TLR7 interactions (green) were visualised after incubation
with the detection solution. Slides were analyzed by confocal
microscopy. Quantification of mean fluorescence using Image J
software.
Statistical analysisStatistical significance was determined by unpaired t-test or two-
way ANOVA.
Supporting Information
Figure S1 The innate inflammatory infiltrate of IAV-infected lungs was not altered by the absence of AEP. (A)BAL fluid levels of IFN-a in wt or AEP2/2 mice before (NI), 4 d
or 8 d post-viral infection. (n = 4 animals; graphs show mean 6
SEM, * p,0.05). (B) IFN-b protein expression was quantified by
quantitative real-time RT-PCR in total RNA extracted from lungs
of wt or AEP2/2 mice before (NI), 4 d or 8 d post-viral infection.
(n = 4–8 animals; graphs show mean 6 SEM). (C) Flow cytometry
analysis of single-cell suspensions of wt or AEP2/2 mice-BAL
fluids before (NI), 4 d or 8 d post-viral infection. We analysed the
presence of macrophages/monocytes (CD11b+/Gr1Inter), neutro-
phils (CD11b+/Gr1high) and dendritic cells (CD11b+/CD11c+) in
BALs (n = 8 animals; graphs show mean 6 SEM of two
independent experiments). (D) Myeloperoxidase (MPO) activity
measured in BAL fluids from wt or AEP2/2 mice 4 d and 8 d
post-viral infection. (n = 8 animals; graphs show mean 6 SEM of
two independent experiments, ** p,0.01).
(TIF)
Figure S2 Reduced TLR7 response in mice- or lungepithelial cells- lacking TLR7 infected with IAV virus. (A)BAL fluid levels of cytokines (KC, IL-6, IL-12p40 and IFN-c) in wt
or TLR72/2 mice before (NI), 4 d or 8 d after intranasal injection
of IAV PR8 virus (100 pfu/mice). (n = 3–4 animals; graphs show
mean 6 SEM, * p,0.05, ** p,0.01). (B) IL-6 and RANTES
secretion in supernatants of wt (white bars) or TLR72/2 (gray
bars) lung primary epithelial cells activated with 5 mg/mL of
imiquimod or with the IAV PR8 (10 pfu) for 16 h or 24 h.
(TIF)
Figure S3 Similar cross presentation of OVA in WT orAEP2/2 DCs with or without TLR3 stimulation. Prolifer-ation of OT-I T cells cultured with DCs from wt or AEP2/2
incubated with splenocytes from Balb/C mice (H-2d) electropo-
rated with OVA and stimulated or not with 100 mg/mL poly(I:C)
or PR8 (10 pfu). Results are representative of two independent
experiments.
(TIF)
Figure S4 Cytokine production by AEP and cathepsindeficient pDCs, BMDCs upon TLR7 and TLR4 ligandstimuli. (A) IFN-a secretion in supernatants of AEP+/+, AEP2/2
or TLR72/2 pDCs activated with the IAV strain PR8 heat killed
(HK) or live at a multiplicity of infection= 1 or 5 for 16 h or 24 h.
(n = 2–3; mean 6 SEM). (B, C) BMDCs from AEP2/2, CatB2/2,
CatK2/2, CatL2/2, CatS2/2 mice (black bars) and from their
wild type littermates (white bars) were stimulated with increasing
concentrations of TLR agonist: imiquimod or resiquimod (B) for
TLR7 and LPS for TLR4 (C) for 16 h and secretion of IL-6 were
measured by ELISA. (n = 2–6, mean 6 SEM). (D) Protease
activities using specific substrates for CatB, CatB and CatL, CatK
and CatS were measured in protein lysates of imiquimod
stimulated DCs from wt (white symbols) and AEP-deficient mice
(black symbols). (n = 2–3). (E) Protease activity of different
cathepsins in total lysates from CatK2/2 and CatK+/+ BMDCs
was measured using specific fluorescent substrates.
(TIF)
Figure S5 Cytokine and co-stimulatory molecule ex-
pression in CatB2/2 and CatB+/+ DCs in vivo upon TLR7
sensing. (A) FACS analysis of in vivo maturation of spleen
CD11c+ cells 4 h after i.v. injection of 10 mg of imiquimod (left
panel) or 1 mg of LPS (right panel) compared to no TLR ligand
stimulation equivalent to 1. (B) IL-6 (left panel) and IL-12p40
(right panel) secretion were measured in serum of CatB+/+ or
CatB2/2 mice 2 h after i.v. injection with imiquimod or PBS.
(n = 7 animals for imiquimod; n = 2 animals for PBS; mean 6
SEM for A and B).
(TIF)
Figure S6 TLR7 is digested in vitro by AEP or cathep-
sins L or S. In vitro transcription and translation of murine (A) or
human (B) TLR7 FL followed by 2 h digestion of radiolabelled
TLR7 FL with 15 U of rAEP and cathepsins (ND: non-digested).
Data are representative of three experiments.
(TIF)
Figure S7 TLR7 C-ter is functional and its generation is
AEP-dependent. (A) Immunodetection of TLR7 proteins in
early (20 min) and late (120 min) phagosomes from wt BMDCs
unstimulated or stimulated with 10 mg/ml of imiquimod. (B)
TLR7 deficient DCs were transfected with cDNAs encoding for
the empty vector (pcDNA3.1), TLR7 FL or C-ter TLR7 fragment.
After 48 h, cells were stimulated with imiquimod for 16 h and IL-
12p40 was measured in the supernatants. The amount of IL-
12p40 produced by unstimulated cells was subtracted from
imiquimod-stimulated cells. (Graphs show mean 6 SEM, n= 3).
(C) IL-6 and IL-12p40 secretion in TLR72/2 BMDCs transfected
with pcDNA3.1, FL or C-ter TLR7 fragment and stimulated with
increasing concentrations of imiquimod for 16 h. (n = 4; mean 6
SEM). (D) IL-12p40 secretion in TLR72/2 BMDCs transfected
with FL or N478Q TLR7 and stimulated with 5 mg/mL
imiquimod for 16 h. (n = 4; mean 6 SEM, * p,0.05).
(TIF)
Figure S8 TLR7 C-ter fragment restores TLR7 response
in AEP2/2 DCs and TLR7 stimulation induces acidic pH.
(A) AEP deficient (black bars) and wt (white bars) DCs were
transfected with cDNAs encoding for the empty vector
(pcDNA3.1), TLR7 FL or C-ter TLR7 fragment. After 48 h,
cells were stimulated with imiquimod or LPS for 16 h and IL-6
was measured in the supernatants. The amount of IL-6 produced
by unstimulated cells was substracted from imiquimod-stimulated
cells. Graphs show mean 6 SEM, n=3, * p,0.05. (B) Kinetic of
endo/lysosomal pH in AEP+/+ and AEP2/2 BMDCs in the
presence or not of 10 mg/ml imiquimod and chased for different
times. (n = 2–5; mean 6 SEM, * p,0.05). (C, D) AEP activity in
total lysate (C) or in phagosomes (D) from wt BMDCs treated or
not with imiquimod (5 mg/mL) for the indicated time. (n = 3–4;
mean 6 SEM, ** p,0.01, *** p,0.001). (E) Protease activities
using specific substrates for CatB, CatB and CatL, CatK and CatS
were measured in protein lysates of imiquimod stimulated DCs
Anti-IAV Immune Response Requires AEP
PLOS Pathogens | www.plospathogens.org 13 August 2012 | Volume 8 | Issue 8 | e1002841
from wt mice (n = 2–3; mean 6 SEM, * p,0.05, ** p,0.01, ***
p,0.001).
(TIF)
Figure S9 Model for TLR7 processing and signaling.Single stranded RNA of viral origin (IAV) or chemical compounds
(imiquimod) are sensed by the intracellular receptor TLR7. After
binding on the cell surface, IAV is internalized into endosomes
where its genome is release in an acidic pH dependent fashion.
Following TLR7 ligand stimulation, which induces a drop of pH
in the endosomes and the recruitment of AEP, TLR7 translocates
with the help of UNC93B1 from the ER to the endosomes. In the
endosomes, TLR7 is cleaved in a C-terminal fragment where after
a conformational change binds the adaptor molecule MyD88.
This binding triggers the activation of NF-kB or IRF, their
translocation to the nucleus, and subsequently the production and
release of cytokines and chemokines in DCs.
(TIF)
Acknowledgments
We are grateful to S. Akira (Osaka, Japan) and N. Doyen (Institut Pasteur,
France) for providing the TLR72/2 mice and to the animal facility of the
Institut Curie for hosting AEP2/2 mice. We thank L. Saveanu for critical
reading of the manuscript and A. Bourhane who participated in the early
work on TLR7. The adenovirus containing the NF-kB response element
was kindly given by J.M Sallenave (Institut Pasteur, France). We also thank
V. Balloy and M. A Nicolas (Plateforme d’Imagerie Dynamique
Imagopole, Institut Pasteur, France) for the help with the IVIS system.
Author Contributions
Conceived and designed the experiments: SM SH FB FES DD BM.
Performed the experiments: SM SH FB FES DD. Analyzed the data: SM
SH FB FES DD. Contributed reagents/materials/analysis tools: MT MC
PVE MST. Wrote the paper: BM SM SH DD. BM supervised the project,
helped designed the experiments and edited the paper.
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Toll-like receptor 5 (TLR5), IL-1β secretion, andasparagine endopeptidase are critical factors foralveolar macrophage phagocytosis and bacterial killingDelphyne Descampsa,b, Mathieu Le Garsa,b,c, Viviane Balloya,b, Diane Barbiera,b, Sophia Maschalidid,e,f, Mira Tohmed,e,f,g,Michel Chignarda,b, Reuben Ramphala,b,h, Bénédicte Manouryd,f,1, and Jean-Michel Sallenavea,b,c,1
aUnité de Défense Innée et Inflammation, Institut Pasteur, 75724 Paris, France; bInstitut National de la Santé et de la Recherche Médicale (INSERM) U874,75724 Paris, France; cUniversité Paris Diderot, Sorbonne Paris Cité (Cellule Pasteur), 75013 Paris, France; dINSERM U1013, Hôpital Necker-Enfants Malades,75015 Paris, France; eEcole Doctorale Gc2iD, Université Paris Descartes, 75006 Paris 5, France; fUniversité Paris Descartes, Sorbonne Paris Cité, Faculté deMédecine, 75015 Paris, France; gInstitut Curie, INSERM U932, 75005 Paris, France; and hDepartment of Medicine, University of Florida, Gainesville, FL 32610
Edited* by Ruslan Medzhitov, Yale University School of Medicine, New Haven, CT, and approved December 16, 2011 (received for review May 27, 2011)
A deficit in early clearance of Pseudomonas aeruginosa (P. aerugi-
nosa) is crucial in nosocomial pneumonia and in chronic lung infec-
tions. Few studies have addressed the role of Toll-like receptors
(TLRs), which are early pathogen associated molecular pattern
receptors, in pathogen uptake and clearance by alveolar macro-
phages (AMs). Here, we report that TLR5 engagement is crucial for
bacterial clearance by AMs in vitro and in vivo because unflagel-
lated P. aeruginosa or different mutants defective in TLR5 activa-
tion were resistant to AM phagocytosis and killing. In addition, the
clearance of PAK (a wild-type P. aeruginosa strain) by primary AMs
was causally associated with increased IL-1β release, which was
dramatically reduced with PAK mutants or in WT PAK-infected pri-
mary TLR5−/− AMs, demonstrating the dependence of IL-1β produc-
tion on TLR5. We showed that this IL-1β production was important
in endosomal pH acidification and in inducing the killing of bacteria
by AMs through asparagine endopeptidase (AEP), a key endosomal
cysteine protease. In agreement, AMs from IL-1R1−/− and AEP−/−
mice were unable to kill P. aeruginosa. Altogether, these findings
demonstrate that TLR5 engagement plays a major role in P. aeru-
ginosa internalization and in triggering IL-1β formation.
flagellin | interleukin-1 | lysosomal protease
The opportunist Gram-negative bacterium, Pseudomonas aer-uginosa, is particularly important in nosocomial pneumonia
and in chronic lung diseases such as cystic fibrosis (1). Alveolarmacrophages (AMs) lie at the forefront of lung defense againstpathogens such as P. aeruginosa. The main function of AMs isto clear pathogens (2), and a deficiency in early recognition ofP. aeruginosa by AMs has been suspected in these pathologies(3, 4). Research has shown that pathogen-associated molecularpatterns (PAMPs) are recognized by specific Toll-like receptors(TLRs) at the surface of phagocytes and mucosal epithelial cells.Surprisingly, although numerous studies have associated the li-gand-induced TLR engagement to cytokine and chemokineproduction from phagocytes (5, 6), comparatively fewer studieshave investigated the importance of TLRs in pathogen phago-cytosis and killing. Furthermore, these studies have mostly usedmacrophages from bone marrow-differentiated cells (BMDMs),few have used live bacteria, and even fewer have used flagellatedbacteria such as P. aeruginosa. Moreover most studies have usedprimed phagocytes (with LPS, zymosan) to boost pathogen up-take. Despite these caveats, the recruitment of membrane TLRsto phagosomes upon phagocytosis has been demonstrated (7–10), except for TLR5. TLR2, TLR4, and the adaptor moleculeMyD88 have been shown to be important molecules in pro-cessing of heat-killed Escherichia coli and Staphylococcus aureusby BMDMs in late endosomes and lysosomes (9–11), suggestingthat a blockade in phagosome maturation was occurring inphagocytes deleted for these molecules.
TLR5 is thought to be one of the key receptors implicated inthe recognition of P. aeruginosa (5, 8), but no information isavailable about whether this molecule is important for bacterialphagocytosis. Here, we sought to investigate specifically the in-volvement of TLR5 in P. aeruginosa phagocytosis and killing byAMs. We describe a pathway linking P. aeruginosa engagementto TLR5 through MyD88, followed by IL-1β release and theinvolvement of a lysosomal cysteine protease (asparagine endo-peptidase, AEP), all events concurring to AM-mediated P. aer-uginosa phagocytosis and bacterial killing.
Results
TLR5 Engagement Is Required for P. aeruginosa Clearance. To de-termine whether the TLR5 ligand flagellin/flagella were involvedin P. aeruginosa clearance by AMs, we infected murine alveolarMH–S cells with either WT P. aeruginosa strain PAK or PAKmutants deficient in the expression of flagellin, the primary fla-gellar subunit (the unflagellated PAKΔfliC), or expressing a fla-gellin monomer mutated in the TLR5-recognition site (PAKL88and PAKL94; Table S1). FACS analysis indicated that MH–Scells expressed TLR5 (Fig. S1A). In the first part of our study,both AM supernatants and cell lysates were pooled for P. aeru-ginosa numeration (killing assays). In that context, MH–S cellssignificantly killed PAK, whereas no clearance of PAKΔfliC orflagellin-mutated PAKL88 or PAKL94 was observed, regardlessof the duration of infection or the multiplicity of infection (MOI)used (Fig. 1A and Fig. S1B). These results were confirmed inprimary WT AMs (Fig. 1B). In all of these experiments, thebacterial counts of all mutants continued to increase, in contrastto WT PAK. Moreover, AMs from TLR5−/−mice were unable tokill PAK, compared with WT AMs (Fig. 1C), whereas the bac-terial clearance ability of AMs from TLR4−/− mice was not im-paired. Importantly, MyD88−/− mice, the TLR5 mRNA levels ofwhich were comparable to those of WT mice (Fig. S1C), werealso unable to eliminate bacteria, underscoring the role ofMyD88 in TLR5 signaling.The resistance of unflagellated PAKΔfliC to AM killing clearly
pointed to the P. aeruginosa flagellum as the organelle mainlyimplicated in AM stimulation (12). However, our data did notrule out that the flagellin monomer might be responsible for AM
Author contributions: D.D., M.C., R.R., B.M., and J.-M.S. designed research; D.D., M.L.G.,
V.B., D.B., S.M., M.T., and B.M. performed research; S.M., M.T., R.R., B.M., and J.-M.S.
contributed new reagents/analytic tools; D.D., M.L.G., S.M., M.T., M.C., B.M., and J.-M.S.
analyzed data; and D.D., B.M., and J.-M.S. wrote the paper.
The authors declare no conflict of interest.
*This Direct Submission article had a prearranged editor.
1To whom correspondence may be addressed. E-mail: [email protected] or
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1108464109/-/DCSupplemental.
www.pnas.org/cgi/doi/10.1073/pnas.1108464109 PNAS | January 31, 2012 | vol. 109 | no. 5 | 1619–1624
IMMUNOLO
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induction of bacterial killing. We, therefore, used an unflagel-lated PAK mutant, PAKD (Table S1), which, unlike PAKΔfliC,is still able to release high amounts of flagellin in the supernatant(Fig. S2A). Fig. 1D shows that PAKD, despite its ability to signalthrough TLR5 (TNFα output, 1201 ± 454 pg/mL vs. 2473 ± 487pg/mL for WT PAK), was completely resistant to primary AMkilling. Bacteria centrifuged onto cells to force bacteria–cellcontact, did not increase PAKD killing by primary AMs, rein-forcing the importance of specific functional flagellum–TLR5interaction for P. aeruginosa clearance.The implication of TLR5 recognition in P. aeruginosa clear-
ance was further confirmed in vivo. Following intratrachealP. aeruginosa administration, we showed that 67% of theWT PAKinoculum was recovered in WT mice bronchoalveolar lavage(BAL) 2 h postinfection, whereas 101% of the same inoculumremained after mouse TLR5−/− infection (Fig. 1E). Moreover,all of the original PAKL94 inoculum remained and continued toproliferate after infection of WT mice (124%), suggesting a delayin bacterial clearance, compared with WT PAK. Importantly,these differences cannot be attributed to variations in the cellularcomposition of the airspaces (97−100% of AMs and 0−3% ofneutrophils), and the total cell counts were not significantlydifferent regardless of the bacteria strains used, thereby impli-cating solely the AMs in the events described.
TLR5/MyD88 Signaling Is Important for P. aeruginosa Phagocytosis.
Because bacterial clearance could not be explained either bybactericidal activity of AM-infected supernatants (Table S2) orby AM cytotoxicity, we assessed whether the differential killingbetween WT and PAK mutants was attributable to different AMuptake. MH–S cells were incubated with bacteria for 1 h, fol-lowed by antibiotic treatment, and then the amount of phago-cytosed bacteria was determined in cell lysates only. Fig. 2Ashows a deficit in phagocytosis for PAKL88 and PAKL94 com-pared with WT PAK, whereas mutant CFU counts increased insupernatants. Using FITC-labeled bacteria (Fig. 2B), FACSanalysis showed a near complete absence of labeling in MH–Scells with PAKΔfliC-FITC, i.e., an almost complete deficit ofphagocytosis, whereas PAKL88-FITC and PAKL94-FITC pre-sented an intermediate phenotype of AM uptake, with PAKL88-
FITC being less phagocytosed than PAKL94-FITC. To confirmthat the P. aeruginosa uptake is dependent upon flagellum–TLR5(and not flagellin–TLR5) interaction, we performed phagocyto-sis assays with PAKD. In Fig. S2B, PAKD (despite high levelsof secreted flagellin; Fig. S2A) was less phagocytosed than WTP. aeruginosa, even when bacteria–cell contact was increasedby centrifugation, demonstrating that bacterial internalization isnot attributable to flagellin/TLR5 engagement. Immunoblottingof intracellular flagellin also reflected differences in bacterial
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Fig. 1. P. aeruginosa clearance by AMs is dependent on efficient TLR5-Flagella interaction. MH–S cells (A) or primary AMs (B) were infected for 4 h with WT
PAK, PAKΔfliC, PAKL88, or PAKL94 mutants [MOI: 0.1 (B) or 10 (A)]. (C) Primary WT, TLR5−/−, TLR4−/−, or MyD88−/− AMs were infected for 4 h with WT PAK
(MOI: 0.1). (D) Primary AMs were infected for 4 h with either WT PAK or PAKD (MOI: 0.1) with or without centrifugation. (A–D) CFU were quantified in AM
supernatants pooled with cell lysates. Results are means ± SD of three experiments (**P < 0.01; ***P < 0.001) and are expressed as percentages as follows:
(CFU counts recovered without AMs − CFU counts recovered after AM infection) × 100. (E) WT or TLR5−/− mice were infected intratracheally with 105 CFU
of PAK or PAKL94. BALs were performed 2 h later and plated on LB agar plates to quantify total CFU counts. Results are means ± SD of three experiments
(*P < 0.05; ***P < 0.001) and are expressed as percentage of surviving bacteria in BAL = (total CFU counts in BAL/ CFU counts of inoculum) × 100.
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Fig. 2. Phagocytosis of P. aeruginosa by AMs is dependent on TLR5-MyD88
signaling. (A and C) MH–S cells were infected for 1 h with WT PAK, PAKL88,
or PAKL94 mutants (A), or primary WT, TLR5−/−, MyD88−/−, or TLR4−/− AMs
were infected with WT PAK (MOI: 10) for 1 h (C). After stimulation, cells
were washed and treated with tobramycin and the number of ingested
bacteria was determined by counting CFU from AM lysates on LB agar plates.
Results are means ± SD of three experiments (***P < 0.001) and are
expressed as percentages of relative phagocytosis index = (CFU counts in
mutant PAK-treated cells/CFU counts in WT PAK-treated cells) × 100. (B)
FACS analysis of MH–S cells following 1 h infection with FITC-labeled WT or
FITC-mutant P. aeruginosa strains. Results are representative of three in-
dependent experiments.
1620 | www.pnas.org/cgi/doi/10.1073/pnas.1108464109 Descamps et al.
uptake (Fig. S2A). Phagocytosis was shown to be TLR5 receptor-specific, because centrifugation did not significantly abolish dif-ferences in AM uptake between WT PAK and mutants (Fig. S2B–D). Moreover, competition experiments with P. aeruginosaflagellin significantly reduced PAK binding (Fig. S2E). Finally,such a deficit in P. aeruginosa phagocytosis was shown in TLR5−/−
and MyD88−/− primary AMs (Fig. 2C). In contrast, TLR4 wasshown to play no role in P. aeruginosa internalization by primaryAMs. Taken together, these observations established the impor-tance of flagellum/TLR5–MyD88 engagement for P. aeruginosaphagocytosis of primary AMs.
IL-1β Production Is Dependent on TLR5 Signaling.Although PAKL94was not killed, it was shown to be better phagocytosed thanPAKL88, suggesting that other intracellular PAMP receptorsmight be important in the detection and the killing of P. aeru-ginosa by AMs. Because the intracellular PAMP receptor ICEprotease-activating factor (IPAF) participates in the processingof pro-IL-1β to IL-1β through caspase-1/inflammasome-de-pendent activation in P. aeruginosa-infected macrophages (13,14), we measured mature secreted IL-1β levels in primary AMsupernatants as a potential index of inflammasome involvement.We observed that high levels of IL-1β were associated with AM-mediated PAK killing and low IL-1β levels were detected withPAKL94 infection (Fig. 3A). The reduction of IL-1β by PAKL94-treated AMs was associated with a delay and a reduction in pro-IL-1β (31 kDa) production, leading to an important inhibition inmature IL-1β conversion (17 kDa) 4 h postinfection (Fig. 3B).We have demonstrated that purified flagellin was able to inducethe pro-IL-1β synthesis but not the caspase-1 p10 and, therefore,was not involved in the mature IL-1β generation (Fig. S3 A–C).The dependence of IL-1β production on TLR5 was furtherdemonstrated by using PAK-infected primary TLR5−/− AMs.Indeed, for these cells, a significant reduction of IL-1β secretionwas observed, compared with WT AMs, caused by a delay in pro-IL-1β production 2 h postinfection and a decrease in mature IL-1β conversion (Fig. 3 C and D).
Importantly, the deficiency in mature IL-1β conversion ob-served in PAKL94-infected WT AMs was correlated with a re-duction in mature caspase-1 p10 production (Fig. S4A), whereasthis was not the case with PAK-infected TLR5−/− AMs, com-pared with WT AMs (Fig. S4B).
IL-1β Is Required for P. aeruginosa Bacterial Killing. To examine theconnection between IL-1β production and bacterial killing, westudied AM infection with PAKΔpscF, a PAK mutant deficientin the type III secretion system (T3SS) (14), which has beendescribed to block the caspase-1-dependent processing of IL-1β(15). Whereas TNFα secretion was similar between WT PAK-and PAKΔpscF-infected AMs, released IL-1β levels were un-detectable in supernatants after infection of primary AMs withthis mutant (Fig. 4A). Western blot analysis showed that, al-though PAKΔpscF induced high levels of pro-IL-1β, mature IL-1β was not produced (Fig. 4B). This is likely attributable to itsinability to activate caspase-1, as evidenced by the absence of thecaspase-1 p10 subunit in PAKΔpscF-infected AMs 4 h post-infection (Fig. S4C). Importantly, although PAKΔpscF was asefficiently phagocytosed by AMs (125% ± 28%) as WT PAK(100% ± 25%), this nonmature IL-1β producer was not killedby primary AMs (Fig. 4C), validating a link between defectivekilling and a major reduction of IL-1β secretion.Importantly, Fig. 4D showed that exogenously added IL-1β
restored PAKL94 killing to levels equivalent to that of WT PAK.We also demonstrated that IL-1 receptor antagonist (IL-1RA),an inhibitor of IL-1β signaling, was able to inhibit MH–S cellkilling of WT PAK (Fig. 4E), without affecting IL-1β release(3867 ± 649 pg/mL with IL-1RA vs. 3393 ± 309 pg/mL withoutIL1-RA; 5 × 105 AMs). To reinforce that point, we performedadditional experiments on primary AMs from IL-1R1−/− mice.Fig. 4F clearly demonstrated that primary IL-1R1−/− AMs wereunable to kill WT P. aeruginosa, compared with WT AMs. Fur-thermore, we measured the same amount of IL-1β in AMs fromIL-1R1−/− (333 ± 144 pg/mL) and WT (271 ± 34 pg/mL) mice,demonstrating the autocrine feedback of IL-1β on P. aeruginosaclearance by primary AMs.
IL-1β-Induced Bacterial Killing Is Dependent on AEP. Because bac-terial fate is ultimately determined in acidic phagolysosomecompartments, we then set out to determine the mechanismsresponsible for PAK killing in AMs. We showed that blockingphagolysosome acidification by bafilomycin A (BafA) treatment(Fig. S5A), an inhibitor of vacuolar type H+-ATPase, inhibitedsignificantly PAK killing in primary AMs (Fig. S5B), whereas IL-1β release was unaffected (Fig. S5C). Using specific probes tomeasure the pH in endolysosomes, we showed that exogenousadministration of IL-1β significantly reduced the pH in MH–Scell endosomes (Fig. 5A), suggesting that IL-1β-mediated acidi-fication of AM phagolysosomes may be a key element in thecontrol of bacterial killing.Because most of the lysosomal cysteine proteases are de-
pendent on a low pH for their activities, we chose to study therole of the protease AEP in PAK clearance. Using confocalmicroscopy, AEP staining was detected in endosomal EEA1+
vesicles in noninfected primary AMs. In contrast, AEP labelingwas significantly decreased upon PAK challenge, whereas a re-duction of staining was much less pronounced in PAKL94-infected AMs (Fig. 5B). Immunoblotting (Fig. 5C) and enzy-matic activity assays using AEP-specific fluorogenic substrate(Fig. 5D) confirmed a significant AEP consumption in WT PAK-infected AMs 4 h postinfection, whereas this was not the casewith PAKL94-infected primary AMs. However, exogenouslyadded IL-1β restored AEP consumption in PAKL94-infectedAMs 3 h postinfection (Fig. 5 C and D). AEP consumptionwas associated with mature IL-1β secretion but was independentof bacterial uptake, because PAKΔpscF, which is efficiently
0
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Fig. 3. IL-1β production in primary AMs is dependent on TLR5. A total of 105
primary AMs fromWT (A and B) or TLR5−/− (C and D) mice were infected with
WT PAK, PAKL88, or PAKL94 (MOI: 1). IL-1β secretion was measured in
supernatants 4 h postinfection (A and C). Results are means ± SD of three
experiments (***P < 0.001). NI, noninfected cells; nd, not detected. Lysates
obtained from primary WT (B) or TLR5−/− (D) AMs infected with bacteria
were analyzed by immunoblotting for pro-IL-1β processing. Equal loading
was controlled for by β-actin detection. Results are representative of three
independent experiments.
Descamps et al. PNAS | January 31, 2012 | vol. 109 | no. 5 | 1621
IMMUNOLO
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phagocytosed but unable to produce IL-1β, did not affect AEPexpression during infection (Fig. S6A).Furthermore we showed that recombinant AEP can exert
a dose-dependent direct lytic activity on P. aeruginosa at pH 6(Fig. S6B). Finally, the importance of AEP activity in AM-mediated bacterial killing of P. aeruginosa was confirmed inprimary AEP−/− AMs. Although PAK was phagocytosedat comparable levels in primary AEP−/− AMs and WT AMs(Fig. S6C), we observed that primary AEP−/− AMs were un-able to kill PAK, compared with WT AMs (Fig. 5E). Theabsence of killing by primary AEP−/− AMs was not caused bya deficiency in pro-IL-1β processing, because these cells didnot secrete less mature IL-1β compared with WT AMs (Fig. S6D and E).
Discussion
Using nonopsonic conditions, thus mimicking resting and naïveconditions in the alveolar space, we show that TLR5 and MyD88(but not TLR4) are of paramount importance for P. aeruginosaphagocytosis and killing. Indeed, P. aeruginosa mutants for theTLR5-recognition site of flagellin monomer domain D1 [PAKL88or PAKL94 (16, 17)] were resistant to AM killing, and primaryTLR5−/− AMs were unable to clear P. aeruginosa. Importantly, inthese unprimed conditions, bacterial flagellum was shown to bekey for AM–P. aeruginosa interaction because unflagellatedmutants, PAKΔfliC or PAKD (the latter secreting flagellin in thesupernatant), were equally resistant to AM killing. Crucially, theimportance of flagellum/TLR5 interaction on bacterial killing was
IL1
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Fig. 4. IL-1β secretion is required for AMs to kill P.
aeruginosa. (A) Primary WT AMs (105) were infected
with WT PAK or PAKΔpscF mutant (MOI: 1) for 4 h. TNFα
or IL-1β was measured in supernatants. Results are
means ± SD of three experiments. NI, noninfected cells;
nd, not detected. (B) Lysates from infected AMs were
assessed for pro-IL-1β processing. Equal loading was
controlled by β-actin detection. Results are representa-
tive of three independent experiments. (C) Primary WT
AMs were infected with WT PAK or PAKΔpscF (MOI: 0.1)
for 4 h. (D and E) MH–S cells were infected with WT PAK
or PAKL94 mutant (MOI: 0.1) for 4 h in the presence or
not of IL-1β or IL-1 receptor antagonist (IL-1RA). (F) Pri-
mary WT or IL-1R1−/− AMs were infected for 4 h with WT
PAK (MOI: 0.1). (C–F) CFU were quantified in super-
natants pooled with cell lysates. Results are means ± SD
of three experiments (*P < 0.05; **P < 0.01) and are
expressed as in Fig 1.
A B
C D E
Fig. 5. AEP protease is essential for P. aeruginosa killing by primary AMs. (A) Kinetics of endolysosomal pH in MH–S cells ± IL-1β (10 ng/mL) was measured.
Results are means ± SD of three experiments. (B) Confocal microscopy of AEP was measured in primary WT AMs infected or not for 3 h with WT PAK or
PAKL94. Quantification was performed using Image J software (n = 5). (C) Immunoblotting AEP expression in lysates from WT PAK- or PAKL94-infected
primary WT AMs (MOI: 1) with or without IL-1β. Equal loading was controlled by β-actin detection. Results are representative of three independent
experiments. (D) AEP activity was measured in lysates fromWT PAK- or PAKL94-infected MH–S cells (MOI: 10) with a fluorometer by assessing the hydrolysis of
the specific substrate for AEP. (A–D) Unpaired t test (*P < 0.01; **P < 0.005; ***P < 0.0001). NI, noninfected cells. (E) Primary WT or AEP−/− AMs were infected
with WT PAK (MOI: 0.1) for 4 h. CFUs were quantified in supernatants pooled with cell lysates. Results are means ± SD of three experiments (***P < 0.001) and
are expressed as in Fig 1.
1622 | www.pnas.org/cgi/doi/10.1073/pnas.1108464109 Descamps et al.
confirmed by using primary TLR5−/−, TLR4−/−, or MyD88−/−
AMs, as well as in vivo, where we demonstrated that 2 h post-infection, TLR5 expression on AMs was the most important factorin clearing bacteria and in containing pulmonary infection.Flagellum/TLR5-mediated killing was not related to AM-se-
creted antimicrobial activity, but was associated with TLR5-de-pendent intracellular entry, because PAK mutants for the TLR5-recognition sites L88 and L94 were less phagocytosed by MH–Scells than WT PAK. The necessity of TLR5/MyD88 engagementfor P. aeruginosa phagocytosis was also confirmed by using pri-mary TLR5−/− and MyD88−/− AMs. Importantly, TLR4 signal-ing did not play any role in P. aeruginosa uptake by primary AMs.Loss of bacterial motility (18) was not a relevant factor in ourmodel. Indeed, PAKL88 and PAKL94 are fully motile bacteria(16); however, none of the mutants was killed by AMs. More-over, after centrifugation to force bacteria–cell contact, flagellin-mutated bacteria or unflagellated mutants were still considerablyless phagocytosed than WT bacteria, demonstrating that thephagocytic phenotype was not attributable to a mobility-deficit orflagellin/TLR5 engagement but was related to diminished spe-cific flagellum/TLR5 interaction.Unexpectedly, the use of PAKL88 and PAKL94 revealed
differences in P. aeruginosa phagocytosis and killing. Indeed,although both mutants were equally resistant to AM killing,PAKL88 stayed mostly extracellular, whereas PAKL94 was bet-ter phagocytosed by AMs, albeit not as efficiently as WT PAK.Although a short stretch of 10 aa (N-88-LQRIRDLALQ-97) inthe flagellin monomer was known to be crucial for TLR5 rec-ognition (16–18), our data demonstrate that the L88 residue isimportant for binding/recognition by TLR5 and intracellularentry, whereas the L94 residue may be more important for in-tracellular downstream events. Indeed, Franchi et al. (14) dem-onstrated that PAKL94 was much less efficient at inducingmature IL-1β than WT PAK in BMDMs, presumably because ofa reduced interaction of bacteria with the intracellular receptorIPAF. These data demonstrated that L94 was a critical residuefor the engagement of the inflammasome via IPAF, in additionto residues present at the C terminus of the D0 domain of fla-gellin monomer (14, 17, 19). Alternatively, other Nod-likereceptors such as Naip5 (19, 20) may also be involved in thedifferential binding of flagellin L94.Another important finding of our study is that TLR5 is im-
portant for production of IL-1β in AMs. The latter result con-trasts with that of Franchi and coworkers (14, 21), who studied P.aeruginosa and Salmonella infection of BMDMs and showed,without studying the effect on phagocytosis and bacterial killing,that TLR5 was redundant and that IPAF and ASC were thetwo inflammasome constituents regulating IL-1β synthesis. Twothings may explain this discrepancy: first, whereas these authorsused BMDMs, we have used AMs; second, and crucially,whereas they primed BMDMs with LPS before bacterial in-fection to increase pro-IL-1β production, our protocol did notinvolve priming, and the production of mature IL-1β occurredfollowing a single event of P. aeruginosa infection (4 h). In ourstudy, TLR5 is essential for bacterial internalization, production,and processing of pro-IL-1β (presumably through IPAF). In thestudy mentioned above (14, 21), BMDM priming with LPSprobably bypassed the need for TLR5 through other receptors(e.g., TLR4) for pro-IL-1β generation. The latter events in-volving inflammasome activation most likely occurred in a simi-lar fashion in both studies.The role of inflammasome has been mainly investigated using
intracellular bacteria (Legionella, Shighella) (22, 23), but rela-tively few studies have addressed this issue in AMs infected withextracellular bacteria (e.g., P. aeruginosa). How can P. aerugi-nosa, then, activate the inflammasome if this bacterium fate isdestruction in the phagolysosome? No system to evade thephagolysosome has been described for P. aeruginosa. However,
a cytosolic leakage/transport of bacterial constituents is a possi-bility. The main vector for this transfer may be the T3SS, andthe main ligand may be flagellin itself, although most studiesused, for their demonstration, elegant but artificial transfectionmethods to introduce flagellin in the cytosol to activate IPAF.Indeed, we showed that extracellularly added flagellin, althoughable to produce pro-IL-1β, is unable to activate procaspase-1and, consequently, to induce the mature IL-1β secretion.Moreover, PAKΔpscF, a mutant deficient in T3SS unable toengage IPAF (13, 14), was not killed by AMs and completelyfailed to induce the mature IL-1β production (although pro-IL-1β was produced), despite the presence of flagellum and itsproper internalization. This demonstrates that IL-1β processingneeds both the flagellum and T3SS to activate the inflamma-some. Crucially, IL-1β production is not merely a bystander inthe killing process but is causative because WT AMs treated withIL-1RA or AMs from IL-1R1−/− mice could not kill P. aerugi-nosa. This clearly demonstrates the existence of an autocrineloop, involving IL-1β production, IL-1β/IL-1R interaction, andsubsequent P. aeruginosa clearance. It has been shown recentlythat the IL-1β processing (procaspase-1/pro-IL-1β) may, in fact,be operative in lysosomes (24, 25), bringing this machinery inclose contact with incoming bacteria and, presumably, decreasingthe time of reaction for mature IL-1β production upon bacterialcontact. Moreover, this vesicular localization of procaspase-1/caspase-1 may explain why IL-1β release precedes cell lysis, be-cause in the time frame of our experiments, no pyroptosis/celllysis was observed. However, it is possible that AMs may beinherently more resistant to pyroptosis because this cell typeperforms a crucial sentinel role within tissues. Interestingly,Carvalho et al. have shown that IL-1RA is produced by AMs inresponse to flagellin after 4 h, suggesting that this counter-regulatory molecule is only secreted at a late time point in thephagocytic process and may not impair bacterial clearance (26).We went a step further in the dissection of the mechanism by
showing that IL-1β increased phagolysosomal acidification. Be-cause the latter is critical for the activation of cysteine proteasesinvolved in bacterial degradation (27), we studied specificallyone of them, AEP, which controls the activation of other lyso-somal cysteine proteases (28). By using three independenttechniques, we observed a reduction of AEP levels upon in-fection with WT PAK, but not with PAKL94 or PAKΔpscF orpurified flagellin (Fig. S3D). AEP was shown to be a key factorparticipating in AM-mediated P. aeruginosa killing becauseAEP−/− AMs were unable to kill WT PAK.In summary (Fig. S7), we describe a phagocytic pathway,
demonstrating the role of TLR5 in AM phagocytosis after P.aeruginosa early infection. This occurs in a T3SS-dependentfashion, leading to caspase-1 and IL-1β maturation. The latterinduces, after acidification of the phagolysosome, the consump-tion of AEP, a protease that we demonstrate to be a key factor inP. aeruginosa killing. Our results give a mechanistic insight intoearly events following P. aeruginosa infection of AMs in the lungand extend our understanding of the crucial role of TLR5 in thedefense of the lung against this important pathogen (29, 30–32).
Materials and MethodsMouse Primary AMs and MH–S Cells. TLR4−/−, TLR5−/−, MyD88−/− (S. Akira,
Osaka University, Osaka, Japan), and IL-1R1−/− mice (CDTA) were back-
crossed 8 times with C57BL/6J. C57BL/6J mice (Janvier) were used as control
mice. Care and use of the mice was in accordance with Institut Pasteur
guidelines in compliance with the European Animal Welfare regulations.
Mouse primary AMs were isolated after lung washing with PBS (33). AMs
were plated in complete RPMI medium (supplemented with 2 mM L-gluta-
mine, 1% antibiotic, and 5% inactivated FBS). After 2 h, medium was re-
moved and AMs were incubated overnight with fresh medium. Mouse AM
cell line MH–S (CRL-2019; ATCC) was maintained in complete RPMI medium
supplemented with 1% sodium pyruvate. Primary AMs or MH–S cells were
placed into serum- and antibiotic-free RPMI for 5 h before infection.
Descamps et al. PNAS | January 31, 2012 | vol. 109 | no. 5 | 1623
IMMUNOLO
GY
Bacterial Strains.WT strain PAK (from S. Lory, HarvardMedical School, Boston,
MA) is a commonly studied P. aeruginosa strain. All modified mutants used
were derived from PAK (Table S1). Bacteria were grown overnight in LB
broth at 37 °C and then transferred to fresh medium and grown by shaking
at 100 rpm for 4–5 h to mid-log phase. The culture was centrifuged at 3,000
× g and the pellet was washed and resuspended in PBS. The OD600nm was
adjusted to give the desired inoculum. Inoculum was verified by serial
dilutions plated on LB agar to determine the number of colony-forming unit
(CFU). Bacterial growth of each PAK strain used in this study was shown to
be identical.
Bacterial Clearance Assay. A total of 105 AMs were infected with bacteria
(MOI: 0.1). After 2–4 h, supernatants were collected and cells were lysed with
0.1% Triton X-100 (a concentration that did not affect PAK viability) in H2O
in sequential washes to harvest total bacteria. To quantify total viable
bacteria, pooled cell supernatants and lysates were diluted and plated on LB
agar to determine CFU scores. Results are expressed as percentages as fol-
lows: (CFU counts recovered without AMs − CFU counts recovered after AM
infection) × 100. For specific experiments, centrifugation was performed (80
× g; 4 min) to ensure synchronous contact between WT or nonmotile
P. aeruginosa and AMs. To test bacterial clearance in vivo, mice were anes-
thetized by ketamine-xylazine intramuscular injection, and then infected
intratracheally with 105 CFU (50 μL). Mice were euthanized 2 h later. BAL
fluids (2 × 250 μL pooled) were performed, diluted, and plated on LB agar
plates to quantify total CFU counts. The percentage of surviving bacteria in
BAL was assessed as follows: (total CFU counts in BAL/CFU counts of in-
oculum) × 100. Total cell counts were measured with a Coulter Beckman
Counter. Cell differential counts were determined after cytospin centrifu-
gation and staining with Diff-Quik products (Medion Diagnostics).
Phagocytosis Assay. A total of 5 × 105 AMs were infected with bacteria (MOI:
10) to 1 h. Free and adherent bacteria were removed by washing cells with
PBS and were killed with tobramycin treatment (40 μg/mL; 30 min). Then, cells
were washed and lysed in H2O containing 0.1% Triton X-100. The number of
bacteria in lysates was determined by counting CFU on LB agar plate. The
percentage of relative phagocytosis index was assessed as follows: (CFU
counts in mutant PAK-treated cells/CFU counts in WT PAK-treated cells) × 100.
In other experiments, bacteria were labeled with 0.1 mg/mL FITC (Sigma) in
Na2CO3 buffer, pH 9.5, at 37 °C while shaking at 100 rpm for 1 h. After in-
cubation and treatment as described above, cells were resuspended in PBS-
EDTA 2 mM, and then fixed in 3% PFA. To quantify phagocytosed bacteria,
fixed cells were used for FACS analysis of cell-associated fluorescence.
ELISA. IL-1β and TNFα were assayed after stimulation using DuoSet ELISA
(R&D Systems). Recombinant murine IL-1β and IL-1RA were purchased from
Peprotech.
Endosomal pH Measurement. Endosomal pH measurement assays have been
described previously (28). MH–S cells were pulsed with 1 mg/mL FITC- and
Alexa-647-labeled 40-kDa dextrans (Molecular Probes) for 10 min at 37 °C
and washed with PBS with 1% BSA. Cells were chased and analyzed by FACS,
via a FL1/FL4 gate selective for cells that have endocytosed the probes.
AEP Protease Activity. Protease activity assays were performed on a FluoStar
Optima (BMG Labtech) by measuring the release of fluorescent N-acetyl-
methyl-coumarin in citrate buffer (pH 5.5) or PBS (pH 7.4) at 37 °C after
incubation of AEP or total lysates with its specific substrate (Z-Ala-Ala-Asn-
NHMec; Bachem).
AEP Immunofluorescence. Primary AMs were seeded on poly-L-lysine-coated
glass coverslips. Cells were infected with bacteria (MOI: 10) for 3 h, washed,
fixed with 4% PFA, and quenched by adding 0.1 M glycine. Cells were per-
meabilized in PBS/0.05% saponin/0.2% BSA, washed, and then incubated
with anti-AEP Ab. The coverslips were mounted with Fluoromount G and
were analyzed by confocal microscopy (Zeiss confocal microscope LSM 700).
For Z-stack acquisition, several images were acquired.
Statistics. Data are presented as means ± SD. A one-way ANOVA with
Fischer’s protected least significant difference test was conducted.
ACKNOWLEDGMENTS. We acknowledge B. Solhonne for her assistance,Prof. Z. Xing (Centre for Gene Therapeutics, McMaster University, Hamilton,Canada) for useful discussions, and Bernhard Ryffel for providing IL-1R1−/−
mice (Unité Mixte de Recherche 6218, Centre National de la Recherche Sci-entifique, Orléans, France). We thank Vaincre la Mucoviscidose for fundingthis work.
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