From the Institut Pasteur, Unité de
Génétique Mycobactérienne, 28 rue du Dr Roux, 75724 Paris Cedex 15,
Institut de Pharmacologie et de Biologie
Structurale du CNRS, UMR 5089, 205 route de Narbonne, 31077 Toulouse
Cedex, ** Hôpital Saint-Louis, Service de
Microbiologie, 1 avenue Claude Vellefaux, 75010 Paris, and
Institut Pasteur, Unité
d'Immunologie Virale, 28 rue du Dr Roux, 75724 Paris Cedex 15, France
Received for publication, October 23, 2002, and in revised form, December 12, 2002
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ABSTRACT |
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Interactions between dendritic cells (DCs)
and Mycobacterium tuberculosis, the etiological
agent of tuberculosis, most likely play a key role in
anti-mycobacterial immunity. We have recently shown that M. tuberculosis binds to and infects DCs through ligation of the
DC-specific intercellular adhesion molecule-3-grabbing nonintegrin
(DC-SIGN) and that M. tuberculosis mannose-capped lipoarabinomannan (ManLAM) inhibits binding of the bacilli to the
lectin, suggesting that ManLAM might be a key DC-SIGN ligand. In the
present study, we investigated the molecular basis of DC-SIGN ligation
by LAM. Contrary to what was found for slow growing mycobacteria, such
as M. tuberculosis and the vaccine strain
Mycobacterium bovis bacillus Calmette-Guérin,
our data demonstrate that the fast growing saprophytic species
Mycobacterium smegmatis hardly binds to DC-SIGN. Consistent
with the former finding, we show that M. smegmatis-derived
lipoarabinomannan, which is capped by phosphoinositide residues
(PILAM), exhibits a limited ability to inhibit M. tuberculosis binding to DC-SIGN. Moreover, using enzymatically
demannosylated and chemically deacylated ManLAM molecules, we
demonstrate that both the acyl chains on the ManLAM
mannosylphosphatidylinositol anchor and the mannooligosaccharide caps
play a critical role in DC-SIGN-ManLAM interaction. Finally, we report
that DC-SIGN binds poorly to the PILAM and uncapped AraLAM-containing
species Mycobacterium fortuitum and Mycobacterium
chelonae, respectively. Interestingly, smooth colony-forming
Mycobacterium avium, in which ManLAM is capped with single
mannose residues, was also poorly recognized by the lectin.
Altogether, our results provide molecular insight into the
mechanisms of mycobacteria-DC-SIGN interaction, and suggest that
DC-SIGN may act as a pattern recognition receptor and discriminate
between Mycobacterium species through selective recognition
of the mannose caps on LAM molecules.
The interaction between Mycobacterium tuberculosis and
host dendritic cells (DCs)1
is thought to be critical for mounting a protective anti-mycobacterial immune response and for determining the outcome of infection (1-4). However, the molecular bases of DC infection by mycobacteria remain poorly understood. We have recently shown that M. tuberculosis, as well as the vaccine strain Mycobacterium
bovis bacillus Calmette-Guérin (BCG), use the DC-specific
intercellular adhesion molecule-3 (ICAM-3)-grabbing nonintegrin
(DC-SIGN) to bind to and enter human DCs (5), a feature that may allow
the bacillus to persist within a unique immature compartment of the
cells (6). DC-SIGN/CD209 is a calcium-dependent (C-type)
transmembrane lectin that contains a single carbohydrate recognition
domain at its extracellular C-terminal end. It is expressed on DCs as
well as on some macrophage (M The DC-SIGN carbohydrate recognition domain binds to mannose-rich
glycoconjugates (15), a feature that is consistent with our finding
that M. tuberculosis lipoarabinomannan (termed ManLAM; see
below), a highly mannosylated surface lipoglycan, might be a key
mycobacterial ligand for DC-SIGN (5). Indeed, purified M. tuberculosis-derived ManLAM was found to inhibit the binding of
M. tuberculosis to human monocyte-derived DCs, as well as to recombinant HeLa-derived cells expressing DC-SIGN. LAM is a major component of the mycobacterial cell wall. It contains a carbohydrate backbone composed of D-mannan and
D-arabinan (Fig.
1). The mannan core is attached to an
acylated mannosylphosphatidylinositol (MPI) anchor at its reducing end;
the arabinan domain is capped with either mannose residues in so-called
ManLAMs or with phosphoinositide motifs in so-called PILAMs (16, 17),
or uncapped in so-called AraLAM (40). The caps of ManLAMs consist of
mono-,
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS AND DISCUSSION
REFERENCES
) subsets, including alveolar M
s (7,
8). DC-SIGN has been described initially as a receptor for ICAM-3 and
ICAM-2, as well as for human and simian immunodeficiency viruses,
enabling the trans infection of susceptible CD4+
T lymphocytes by these viruses (9-12). Thereafter, it was shown to
bind to other microbes, namely Ebola virus and Leishmania
pifanoi (13, 14).
(1
2)-di-, and
(1
2)-tri-mannopyranosides, with
dimannopyranosides being the most abundant motif (18-20). So
far, ManLAMs have been detected in slow growing mycobacteria
only. These include various strains of M. tuberculosis,
M. bovis BCG, the leprosy agent
Mycobacterium leprae, and the opportunistic
species Mycobacterium avium (16, 17, 21, 22). By contrast,
PILAM or AraLAM expression seems to be fairly limited to fast growing
mycobacteria, including nonpathogenic Mycobacterium
smegmatis (16, 17, 21, 23), Mycobacterium chelonae
(40), and Mycobacterium
fortuitum.2 In addition to their structural role in
organizing of the cell wall, LAMs are known to be potent inducers of
various cytokines when in contact with mammalian phagocytic cells
(24).
View larger version (13K):
[in a new window]
Fig. 1.
Structural organization of ManLAM
versus PILAM. Manp,
mannopyranose; Ins, myo-inositol; P,
phosphate; R1-R4,
acyl chains.
We have shown that the slow growing mycobacteria M. tuberculosis and M. bovis BCG, which express
ManLAM, interact with human DCs through DC-SIGN and that purified
M. tuberculosis-derived ManLAM inhibits
M. tuberculosis binding to recombinant HeLa-derived cells
expressing DC-SIGN and to monocyte-derived DCs. The goal of the present
report was to obtain a better understanding of the molecular
determinants of the LAM molecule involved in binding to DC-SIGN. Using
a DC-SIGN-expressing recombinant cell line as a readout, we first
report that DC-SIGN binds poorly to the fast growing species M. smegmatis and that M. smegmatis-derived PILAM, which
lacks mannose caps, exhibits a very limited ability to inhibit M. tuberculosis binding to the lectin. Using various chemically or
enzymatically generated variants of the ManLAM molecule, we further
demonstrate that both the acyl chains on the MPI anchor and the
mannose-capping residues play a key role in the ManLAM-DC-SIGN ligation
process. Moreover, we show that DC-SIGN does not bind to the PILAM- and
AraLAM-containing species M. fortuitum and M. chelonae, respectively. Altogether, our findings provide evidences that DC-SIGN may discriminate between ManLAM-containing slow growers, such as M. tuberculosis, and nonpathogenic
PILAM-containing fast growers, such as M. smegmatis, through
a high affinity for mannose-capping residues on ManLAM.
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EXPERIMENTAL PROCEDURES |
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Cells and Bacteria--
DC-SIGN+ HeLa (HeLa-DC)
cells were obtained by transducing HeLa cells with the retroviral
vector TRIP-U3 encoding for human DC-SIGN (25). HeLa and HeLa-DC
cells were propagated in RPMI 1640 (Invitrogen) supplemented
with 10% fetal calf serum (Dutscher, Brumath, France).
M. tuberculosis H37Rv, M. smegmatis
mc2155, and clinical isolates of M. fortuitum,
M. chelonae, and M. avium
(smooth colony-forming) were propagated in 7H9 medium containing 10%
albumin-dextrose-catalase supplement.
Mycobacterial Glycoconjugate Purification and Chemical
Degradation--
ManLAM from M. bovis BCG Pasteur and PILAM
from M. smegmatis were purified as described previously (19,
23, 26). M. tuberculosis H37Rv-purified ManLAM was a kind
gift from the Colorado State University. dManLAM was prepared by
incubating ManLAM (200 µg) in 200 µl of NaOH 0.1 M for
2 h at 37 °C. After neutralization with 200 µl of HCl, 0.1 M, the reaction products were dialyzed against water and
freeze-dried. ManLAM was prepared by incubating ManLAM (200 µg)
for 6 h at 37 °C in 30 µl of a jack beans
-mannosidase (Sigma) solution (2 mg/ml, 0.1 M sodium acetate buffer, pH
4.5, 1 mM ZnSO4). After a second addition of 50 µl of enzyme solution, the reaction was continued overnight. The
reaction products were then dialyzed against 50 mM
NH4CO3, pH 7.6. Elimination of
-mannosidase was achieved by denaturation (2 min at 110 °C) followed by overnight tryptic digestion (37 °C, 3.2 µg of trypsin).
ManLAM was
recovered after dialysis against water, freeze-dried, and analyzed for
cap contents by CE-LIF as previously described (27). Briefly, ManLAM or
ManLAM (1 µg) was submitted to mild acidic hydrolysis (15 µl of
HCl, 0.1 M, for 20 min at 110 °C) in the presence of
mannoheptose (100 pmol) as the internal standard. The reaction products
were then submitted to 1-aminopyrene-3,6,8-trisulfonate (APTS) tagging and subjected to CE-LIF analysis. Separations were performed using an
uncoated, fused silica capillary column (50 µm internal diameter; 40 cm effective length; 47 cm total length; Sigma), and analyses were
carried out at a temperature of 25 °C with an applied voltage of 20 kV using acetic acid 1% (w/v), triethylamine 30 mM in
water, pH 3.5, as a running electrolyte. The amount of
each cap motif was determined relative to the internal standard.
Binding and Inhibition Assay--
Cells were infected at a
multiplicity of infection of 1 bacterium/cell for 4 h at 4 °C
in RPMI 1640, washed extensively in RPMI 1640, and analyzed by scoring
colony-forming units after plating on agar and incubation at 37 °C.
In binding inhibition experiments, cells were preincubated for 1 h
at 4 °C with 10 µg/ml of the indicated components. These
components were left in the culture medium during the infection process.
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RESULTS AND DISCUSSION |
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Mycobacterial species can be divided into slow and fast growers.
To gain a better understanding of the molecular basis of their ligation
to DC-SIGN, we first compared the relative ability of the slow growing
pathogenic species M. tuberculosis versus the fast growing
saprophytic species M. smegmatis to bind to the lectin. A
binding assay was performed on HeLa-derived cells expressing or not
DC-SIGN (HeLa-DC and HeLa, respectively). As we reported previously,
M. tuberculosis was found to bind to HeLa-DC ~15 times more than to HeLa cells (Fig.
2A), and in a multiplicity of
infection-dependent manner (data not shown). Conversely,
M. smegmatis binding to HeLa-DC was found to be only ~2
times more than to HeLa cells (Fig. 2A). Our previous
finding that M. tuberculosis ManLAM can inhibit M. tuberculosis binding to DC-SIGN suggests that the reduced ability of M. smegmatis to bind to HeLa-DC cells may be due to the
inability of M. smegmatis PILAM to bind to the lectin. To
test this hypothesis, we performed a M. tuberculosis binding
assay on HeLa-DC cells that had been preincubated or not with LAM
molecules from various mycobacterial species. As reported previously,
yeast mannan and M. tuberculosis- as well as M. bovis BCG-derived ManLAMs were found to inhibit mycobacterial
binding to HeLa-DC cells by as much as ~90% (Fig. 2B). By
contrast, M. smegmatis-derived PILAM was found to inhibit
poorly (~25% inhibition) the binding of M. tuberculosis
to HeLa-DC cells. Interestingly, PILAM was found able to fully inhibit
M. smegmatis binding to HeLa-DC cells (data not shown).
The fact that BCG-derived ManLAM inhibits M. tuberculosis binding to DC-SIGN as well as M. tuberculosis-derived ManLAM does is consistent with our previous
result showing that M. bovis BCG binds to DC-SIGN to the
same extent as M. tuberculosis and with the known
structural similarity between ManLAMs from M. bovis BCG and
M. tuberculosis (18).
|
Because DC-SIGN is a mannose-binding lectin and because PILAMs are
devoid of mannose caps (Fig. 1), we next reasoned that the results
described above might indicate that ManLAM capping residues may be the
ManLAM subdomains preferentially recognized by the lectin. To test this
hypothesis, we treated M. bovis BCG-derived ManLAM with
-exomannosidase to obtain ManLAM devoid of mannose caps (
ManLAM).
The reaction was assessed by CE-LIF analysis as previously described
(18, 27). A typical electropherogram obtained for
ManLAM is
presented in Fig. 3A. Peaks
corresponding to mannooligosaccharide caps, i.e.
mono-,
(1
2)-di-, and
(1
2)-tri-mannopyranosides, were almost
undetectable. Quantification indicated that more than 95% of cap
demannosylation was achieved. The ability of
ManLAM to inhibit
M. tuberculosis binding to DC-SIGN was evaluated
in binding experiments. In contrast to native ManLAM,
ManLAM failed to inhibit mycobacterial binding to the lectin (~10% binding
inhibition, Fig. 3B). Similar results were obtained when
cells were treated with M. tuberculosis-derived
ManLAM
prior to the binding assay (data not shown). These results indicate
that mannooligosaccharide caps are critical structural features for
ManLAM-mediated inhibition of M. tuberculosis binding
to DC-SIGN.
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Because MPI anchor has been shown previously to be involved in some of the biological activities of ManLAM, particularly their binding to C-type lectins (28, 29), we then evaluated the role of the acyl part of the MPI anchor in ManLAM-DC-SIGN interaction. To this end, M. bovis BCG-derived dManLAM was prepared by alkali treatment. As shown on Fig. 3B, dManLAM failed to inhibit M. tuberculosis binding to HeLa-DC cells, revealing that a native acylated MPI anchor is required for ManLAM-mediated inhibition of mycobacterial binding to DC-SIGN.
Finally, we wished to know whether our finding was still valid in other Mycobacterium species for which the LAM structure was known. In agreement with what we reported above, the PILAM- and AraLAM-containing species M. fortuitum and M. chelonae were poorly recognized by DC-SIGN. Indeed, in a representative binding assay done in triplicate, M. fortuitum and M. chelonae bound to HeLa-DC cells 2.3 and 1.5 times more than to HeLa cells, respectively (data not shown). Interestingly, the ManLAM-containing slow grower M. avium was also found to bind poorly to DC-SIGN-expressing HeLa cells (~1.7 times more than to HeLa cells; data not shown). This is not surprising because ManLAM from smooth colony-forming M. avium, which is the one used in our assay, has been reported to be capped mainly with single mannose residues instead of the di- and tri-mannopyranoside motifs found in M. tuberculosis- and M. bovis BCG-derived ManLAM (22). Because DC-SIGN does not bind to single mannose molecules but to more complex mannosylated structures (15), it is likely that such mono-mannosylated ManLAM is not recognized by the lectin. These results raise the possibility, currently under investigation, that DC-SIGN may recognize mycobacteria from the tuberculosis complex only.
Altogether, our results demonstrate that the DC-SIGN-ManLAM interaction involves both the MPI anchor acyl chains and the mannose residues from caps of the ManLAM molecule. As established recently for the binding of ManLAM to the human surfactant pulmonary protein A C-type lectin (29, 30), the MPI fatty acids are most likely involved in the supermolecular organization of the ManLAM molecules in aggregates, allowing macromolecular clustering in aqueous solution. Micelle formation probably results in a huge increase in ManLAM valence and increases ManLAM avidity to DC-SIGN. This is likely to explain the poor ability of dManLAM to inhibit M. tuberculosis binding to HeLa-DC cells but does not indicate whether LAM acyl chains, which are likely to be buried within the bacterial cell wall, can interact with the lectin in vivo. However, the latter definitely should be investigated, as our result is reminiscent of the involvement of the acyl chains of the M. tuberculosis 19-kDa lipoprotein antigen in binding to toll-like receptor-2 (TLR2) on phagocytic cells (31).
Selective recognition of the ManLAM mannose-capping residues by DC-SIGN
on the surface of DCs is likely to have important consequences for both
the pathogenesis and immunology of tuberculosis and other mycobacterial
diseases. LAMs have various effects on phagocytic cells, including
Ms and DCs (24). PILAMs induce the secretion of proinflammatory
cytokines, such as tumor necrosis factor-
, interleukin-1 (IL-1),
IL-12, and IL-6, and the production of microbicidal radicals, such as
NO
activation effect
of interferon-
produced by effector T lymphocytes. PILAMs are thus
now considered as proinflammatory molecules, whereas ManLAMs are viewed
rather as anti-inflammatory components (17, 24), which is consistent with the known ability of ManLAM-containing slow growing mycobacteria to resist immune defense mechanisms of their susceptible host (32). In
particular, our recent results demonstrate that ManLAM inhibits the
secretion of IL-12 by human DCs, a process that, like DC-SIGN ligation,
requires both the MPI anchor acyl chains and the mannose caps (27). In
this previous study (27), based on experiments using monoclonal
antibodies, we suggested that ManLAM was acting through ligation of the
mannose receptor (MR). Although MR is also involved in LAM mannose caps
recognition (33), one cannot rule out the possibility that ManLAM could
act also through the ligation of DC-SIGN, which is currently under
investigation. Indeed, DC-SIGN ligation by ManLAM, either attached to
the bacilli or released in the milieu through exocytosis (34), is
likely to induce major signaling events, possibly including cell
deactivation and/or secretion of anti-inflammatory cytokines such as
transforming growth factor-
or IL-10 (35). Interestingly,
PILAMs but not ManLAMs can activate cells in a
TLR2-dependent manner (36). It will be of interest to study
the cross-talk between phagocytic cell surface lectins, such as MR and
DC-SIGN, and TLRs in response to mycobacterial ligands, including LAMs
from various mycobacterial species.
From an evolutionary perspective, it is interesting that DC-SIGN can
discriminate between fast growing saprophytic and slow growing virulent
or potentially virulent mycobacteria. Until recently, it was proposed
that mannose capping of the LAM molecules was a unique feature of
virulent mycobacteria. This is unlikely to be the case because the
attenuated species M. bovis BCG also contains mannose-capped
LAM (21). Even if not virulent stricto sensu, M. bovis BCG can be pathogenic under certain conditions, especially in children and immunocompromised patients, in whom it may cause a
variety of effects ranging from local adenitis to disseminated disease
(37). Moreover, M. bovis BCG is derived from virulent M. bovis, which shares a common ancestor with M. tuberculosis (38). One cannot exclude that mannose capping of the
ManLAM molecule is a feature of virulent mycobacteria that has been
conserved during the recent evolution of M. bovis BCG from
M. bovis. In this context, DC-SIGN could be viewed as a
pattern recognition receptor (39) that has evolved to recognize
potentially harmful mycobacteria through their specific surface
glycosylated moieties. In parallel, mycobacteria could have evolved
mechanisms (LAM capping) to resist host immunity (deactivation of the
inflammatory response) in contrast with their fast growing,
soil-living, harmless ancestors.
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ACKNOWLEDGEMENTS |
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We thank L. Tailleux, V. Abadie, O. Schwartz (Institut Pasteur, Paris), and C. Petit (Institut Cochin,
Paris) for careful reading of the manuscript and helpful discussions.
We thank P. Charneau (Institut Pasteur, Paris) for providing
TRIP-U3. We acknowledge Colorado State University for the gift of
purified M. tuberculosis H37Rv-derived ManLAM.
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FOOTNOTES |
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* This work was supported by grants from the European Community "Cluster for Tuberculosis Vaccine Development," the Institut Pasteur, and the National Institutes of Health (NIAID Contract NO1 AI-75320, "Tuberculosis Research Materials and Vaccine Testing").The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
§ A JSPS overseas research fellow.
¶ These authors contributed equally to the work.
§§ To whom correspondence should be addressed. Tel.: 33-1-45-68-88-40; Fax: 33-1-45-68-88-43; E-mail: neyrolle@pasteur.fr.
Published, JBC Papers in Press, December 20, 2002, DOI 10.1074/jbc.C200586200
2 L. Bala, M. Gilleron, M. Rivière, and G. Puzo, unpublished data.
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ABBREVIATIONS |
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The abbreviations used are:
DC, dendritic cell;
DC-SIGN, DC-specific intercellular adhesion molecule-3-grabbing
nonintegrin;
BCG, bacillus Calmette-Guérin;
ICAM, intercellular adhesion molecule;
M, macrophage;
ManLAM, mannose-capped lipoarabinomannan;
ManLAM,
-exomannosidase-treated ManLAM;
dManLAM, deacylated ManLAM;
PILAM, phosphoinositide-capped lipoarabinomannan;
AraLAM, uncapped LAM;
MPI, mannosylphosphatidylinositol;
CE-LIF, capillary electrophoresis coupled
to laser-induced fluorescence;
APTS, 1-aminopyrene-3,6,8-trisulfonate;
IL, interleukin;
MR, mannose receptor;
TLR, toll-like receptor.
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