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Infect Immun. Oct 2005; 73(10): 7064–7068.
PMCID: PMC1230978

Mycobacterial Lipomannan Induces Matrix Metalloproteinase-9 Expression in Human Macrophagic Cells through a Toll-Like Receptor 1 (TLR1)/TLR2- and CD14-Dependent Mechanism

Abstract

Lipomannans (LM) from various mycobacterial species were found to induce expression and secretion of the matrix metalloproteinase 9 (MMP-9) both in human macrophage-like differentiated THP-1 cells and in primary human macrophages. Inhibition studies using antireceptor-neutralizing antibodies are indicative of a Toll-like receptor 1 (TLR1)/TLR2- and CD14-dependent signaling mechanism. Moreover, LM was shown to down-regulate transcription of the metalloproteinase inhibitor TIMP-1, a major endogenous MMP-9 regulator.

Matrix metalloproteinases (MMPs) form a family of Zn2+- and Ca2+-dependent endopeptidases, which are involved in various physiological and pathological processes, through their capacity for degrading components of the extracellular matrix (11, 32, 36, 37). MMP-9, known as the 92-kDa gelatinase B, is the predominant MMP secreted by monocytes/macrophages during bacterial diseases (7-9, 25, 27, 30, 31, 38). This enzyme is secreted as a proenzyme latent form, which undergoes extracellular proteolytic cleavage to provide the active form. Once secreted and activated, the activities of MMPs are regulated by specific tissue inhibitors (TIMPs) produced by a variety of cells, TIMP-1 being a major MMP-9 inhibitor (1). Although MMP-9 is a critical factor in host defense mechanisms by facilitating leukocyte extravasation into infected sites, excessive production of MMP-9 may contribute to host tissue injury and exacerbation of the inflammation response, as reported in Mycobacterium tuberculosis infection (3, 9, 28, 30, 31).

Lipomannan (LM) and lipoarabinomannan (LAM) are major complex lipoglycans ubiquitously found in the mycobacterial cell wall. LM, considered as a direct biosynthetic precursor of LAM, is composed of a phosphatidyl-myo-inositol anchor linked to a d-mannan core. In LAM, the mannan domain is followed of a d-arabinan domain which can be capped by mannosyl or phosphoinositol residues (2, 16, 24). LM and LAM exhibit a wide array of biological activities which enhance antimycobacterial immune defenses or facilitate mycobacterial survival through inhibition of the immune response. The interaction of these lipoglycans with Toll-like receptor 2 (TLR2), CD14, mannose receptor or dendritic cell-specific intracellular adhesion molecule 3 is dependent on structural features of LM and LAM (4, 10, 19, 21-23, 29, 31, 35, 39). LAM from M. tuberculosis was reported to up-regulate MMP-9 expression in the monocytic THP-1 cell line and in macrophages through binding to the mannose receptor (3, 30, 31). However, although recent studies have emphasized the role of LM as a strong immunomodulator (2), no information is available regarding to its potential contribution in MMP-9 secretion.

In this study, we investigated the ability of LM from various mycobacteria, including pathogenic species, to stimulate MMP-9 gene expression and MMP-9 secretion from human macrophage-like THP-1 cells and human primary macrophages. We also addressed the possible involvement of TLR1, TLR2, and CD14 in MMP-9 production in response to LM stimulation.

Induction of MMP-9 from human macrophages in response to mycobacterial LM.

Mycobacterium kansasii and Mycobacterium chelonae are two opportunistic pathogens that are particularly virulent in immunocompromised patients and are frequently associated with skin lesions and serious pulmonary diseases (14, 15, 18, 26). The capacities of various LM isolated from M. kansasii (LMMk), M. chelonae (LMMc), and Mycobacterium bovis BCG (LMBCG; sharing the same structure of LM from M. tuberculosis [24]) for triggering the MMP-9 gene expression was first investigated by reverse transcription (RT)-PCR analysis on differentiated THP-1 cells in serum-free medium. LM from M. chelonae (ATCC 19538), M. kansasii (PHR1 901, a clinical isolate), and M. bovis BCG (Pasteur strain 1173P2) were purified as described previously (12, 13). The endotoxin content of each preparation was <20 pg lipopolysaccharide (LPS)/10 μg as determined by the chromogenic Limulus lysate assay (QCL1000; BioWhittaker, Walkersville, MD). Human promonocytic leukemia THP-1 cells (European Collection of Cell Cultures no. 88081201) were differentiated with 50 nM 1,25-dihydroxy-vitamin D3 (Calbiochem, Darmstadt, Germany) for 72 h (34). To determine the effects of LM on the expression levels of the MMP-9 and TIMP-1 genes, 5 × 106 differentiated THP-1 cells were incubated in 12-well plates in RPMI-glutamine serum-free medium with either increasing LM concentrations or 100 ng/ml of LPS from Escherichia coli 055B5 (Sigma) used as a positive control of MMP-9 induction. Following 24-h incubation at 37°C, total RNA was purified from activated cells by using the Nucleospin RNA II kit (Macherey-Nagel, Düren, Germany), according to the manufacturer's instructions. Reverse transcription was performed with 5 μg of total RNA, in presence of M1MLVRT reverse transcriptase (Promega, Madison, WI), oligo(dT) primers, deoxynucleotide triphosphate, and RNasin. PCR amplification was performed by using primer pairs (Eurogentec) designed for the specific detection of human MMP-9, TIMP-1, and GAPDH genes, according to the method of Devy et al. (6). The first-strand sequence amplification was performed with GoTaq polymerase (Promega). Each amplification reaction consisted of an initial denaturation at 94°C and multiple cycles (23, 23, and 17 cycles at 68°C, 65°C, and 69°C for MMP-9, TIMP-1, and GAPDH genes, respectively) and a primer extension step at 72°C. PCR products (208, 627, and 256 bp for MMP-9, TIMP-1, and GAPDH genes, respectively) were separated by electrophoresis on a 2% agarose gel, visualized by ethidium bromide staining, and then analyzed with the Bio-Rad GelDoc analysis system (Bio-Rad, Italy).

As illustrated in Fig. Fig.1A,1A, each LM type was found to up-regulate MMP-9 mRNA synthesis in a dose-dependent manner, whereas in unstimulated cells, no specific product was detected. The induction of MMP-9 mRNA was maximal with 10 μg/ml of LM. LMMk, LMMc, and LMBCG displayed similar MMP-9-inducing activities. Expression levels of GAPDH mRNA, a housekeeping gene product included as an internal control, remained unchanged, regardless of the concentration of LM used.

FIG. 1.
(A) MMP-9 gene (MMP-9) expression in differentiated THP-1 cells in response to LM. Differentiated human promonocytic THP-1 cells were incubated for 24 h with 0.1 to 20 μg/ml of LM purified from M. kansasii (KanLM), M. chelonae (CheLM), or M. bovis ...

Tumor necrosis factor alpha (TNF-α) was previously shown to stimulate secretion of MMP-9 in monocytes/macrophages (20). Although LM is a poor TNF-α-inducing factor in the absence of serum (35), we examined the contribution of low levels of TNF-α released in culture supernatants to induced MMP-9 induction. Hence, differentiated THP-1 cells were stimulated for 24 h at 37°C with 1 or 10 μg/ml of LMMc and LMMk, in fetal calf serum-free RPMI medium, and in the absence or presence of 5 μg/ml of TNF-α-neutralizing goat polyclonal antibodies (R&D Systems, Minneapolis, MN). Neutralization of TNF-α reduced only weakly the secretion of MMP-9 with at most 22% inhibition (Fig. (Fig.1B).1B). These results suggest that the vast majority of MMP-9 induced by LM in absence of serum is secreted through a TNF-α-independent mechanism.

The MMP-9-inducing capacity of LM was next examined on human blood monocyte-derived macrophages. Human peripheral blood mononuclear cells were isolated by density gradient centrifugation on Lymphoprep separation medium (Nycomed, Oslo, Norway), and adherent monocytes were collected after lymphocyte depletion. Purity of the population was evaluated by flow cytometry analysis (FACScalibur cytometer; Becton Dickinson). Macrophages were derived from monocytes in the presence of 100 ng/ml macrophagic colony-stimulating factor for 48 h in RPMI-glutamine supplemented with 10% heat-inactivated fetal calf serum. Macrophages were then stimulated with 10 μg/ml of LM for 24 h and processed for RT-PCR analysis, as described above. Figure Figure1C1C shows that all LM subtypes were potent MMP-9-inducing factors in primary human macrophages. Although LMBCG, LMMc, and LMMk display subtle structural differences pertaining mainly to the nature of fatty acids bound to anchor and the linkage and the degree of substitution in the mannopyranosyl side chains of the mannan core (2, 24), they behave similarly in up-regulating MMP-9 synthesis, suggesting that the MMP-9-inducing activity is a common feature to all mycobacterial LMs.

The amount of MMP-9 protein released in culture supernatants of differentiated THP-1 cells (2 × 105 cells/well) was next quantified by enzyme-linked immunosorbent assay, after 48 h of cell incubation with either LMMk or LMMc in serum-free RPMI medium. Microtiter plates were coated overnight at 4°C with aliquots of cell supernatants, blocked with phosphate-buffered saline (PBS)-0.05% Tween 20-1% bovine serum albumin, and then incubated with biotin-conjugated anti-MMP-9 antibodies (1/500 dilution; Santa Cruz Biotechnology, CA), prior to the addition of extravidin-conjugated peroxidase (1/1,000 dilution) for 30 min. Detection was performed with o-phenylenediamine-dihydrochloride and by reading the absorbance at 490 nm. MMP-9 concentrations in culture supernatants were quantified according to a standard curve generated with human recombinant pro-MMP-9 (R&D Systems, Minneapolis, MN) at concentrations ranging from 2 to 30 ng/ml. LM induced the secretion of MMP-9 in a dose-dependent manner, and the levels of MMP-9 secreted from cells stimulated with LMMk and LMMc were approximately six and five times higher, respectively, than that from unstimulated cells (Fig. (Fig.2A2A).

FIG. 2.
Secretion of MMP-9 in the culture supernatant of differentiated THP-1 cells stimulated with LM. LMMk, KanLM; LMMc, CheLM. (A) Differentiated THP-1 cells were stimulated with increasing concentrations of LMMk or LMMc in RPMI-glutamine medium. Culture supernatants ...

MMP-9 is secreted from macrophages as a latent precursor form of 92-kDa pro-MMP-9, in which the propeptide can be cleaved by proteases, generating the mature 84-kDa MMP-9 form (11, 36). Both the pro-MMP-9 form and the mature form can be detected by gelatin zymography analysis. This technique was applied to determine the identity of the MMP-9 form released in response to LM stimulation. Therefore, the supernatants of differentiated THP-1 cells activated for 48 h with 10 μg/ml of either LMMk or LMMc were loaded on a 7.5% sodium dodecyl sulfate gel impregnated with 2 mg/ml gelatin and processed according the procedure described by Leber and Balkwill (17). Densitometric analysis of proteolytic bands was performed by using the Image1.61 analysis program. Figure Figure2B2B shows the gelatinolytic activity found in the supernatant of cells treated with LMMc or LMMk, characterized by intense bands comigrating with the recombinant 92-kDa pro-MMP-9, while the mature 84-kDa form remained undetectable. The presence of pro-MMP-9 was also confirmed by Western blot analysis (Fig. (Fig.2C).2C). For this aim, proteins present in the conditioned medium obtained after 48 h of culture with LM were precipitated with cold ethanol, lyophilized, and resuspended in sodium dodecyl sulfate-Laemmli loading buffer, as reported by Zhang et al. (40). Samples were then electrophoresed on a 10% polyacrylamide gel and transferred onto nitrocellulose membrane, which was subsequently blocked with PBS-0.1% Tween 20 buffer containing 5% nonfat dry milk, probed with primary mouse immunoglobulin G (IgG) antibodies of anti-MMP-9 recognizing both the pro-MMP-9 and the cleaved forms (1/250; Santa Cruz Biotechnology) in PBS-0.05% Tween 20-0.1% bovine serum albumin for 2 h, and incubated with horseradish peroxidase-conjugated anti-mouse IgG antibodies (1/4,000; Santa Cruz). Detection of MMP-9 was done using the enhanced chemiluminescence detection system (Amersham). Altogether, zymography and Western blot analysis indicate that LM stimulation induces only the release of the latent pro-MMP-9 form. Whether LM also regulates the activity of extracellular serine proteases secreted from immune cells at the inflammatory sites which convert the latent pro-MMP-9 to the mature MMP-9 remains an attractive hypothesis that remains to be elucidated.

Induction of MMP-9 gene by LM is mediated through a TLR1/TLR2- and CD14-dependent pathway.

In an attempt to identify receptors present on the surface of differentiated THP-1 cells that recognize LM and transmit a positive signal for MMP-9 expression, we evaluated the effects of various neutralizing antireceptor antibodies, known to inhibit biological activities of microbial products (21, 29, 31, 35), on MMP-9 synthesis. Differentiated cells were pretreated for 30 min at 37°C with 5 μg/ml of neutralizing antibodies (purchased from BD Biosciences, BD Pharmingen, San Diego, CA, or HBT, Uden, The Netherlands), and then 1 μg/ml of LMMk was added to the cells for 24 h to allow MMP-9 gene expression. The corresponding isotype controls were used as negative controls. As illustrated in Fig. Fig.3,3, pretreatment with anti-TLR2 (mouse IgG2a clone TL2-1), anti-TLR1 (mouse IgG1κ clone GD2.F4), and anti-CD14 (mouse IgG1 clone MEM-18) antibodies inhibited MMP-9 gene expression by 48%, 37%, and 66%, respectively. Surprisingly, the anti-mannose receptor antibody (mouse IgG1κ clone 19), previously shown to interfere with MMP-9 gene expression elicited by mannose lipoarabinomannan of M. tuberculosis (31), displayed only a residual inhibitory effect (8%). Antibodies raised against TLR4 (mouse IgG2aκ clone HTA 125), a potent LPS-responsive receptor, failed to inhibit MMP-9 gene expression. Incubation with the corresponding control isotype antibodies did not alter MMP-9 mRNA synthesis (data not shown). Altogether, these results suggest the participation of several pattern recognition receptors, in particular, TLR1/TLR2 and CD14, in the signaling pathway leading to MMP-9 induction. These results are consistent with previous studies demonstrating that macrophage activation by LMMk or LMMc is mediated by TLR2 and CD14 but is independent of TLR6 and TLR4 (2, 29, 35). Interestingly, the TLR1/TLR2 heterodimer triggers, through the adaptor protein MyD88, the activation of several signal transduction molecules, leading to the activation of NF-κB and mitogen-activated protein kinases in macrophages (33). Rivera-Marrero et al. (31) demonstrated that induction of MMP-9 by mannose lipoarabinomannan from M. tuberculosis required the transcriptional activation of AP-1 through mitogen-activated protein kinases. According to these authors, the addition of PD-98059, a MEK1 inhibitor, resulted in a total inhibition of MMP-9 induction (31). In preliminary experiments, we have tested the effect of PD-98059 and observed that, at 50 μM, this molecule strongly inhibited LM-induced MMP-9 expression in differentiated THP-1 cells (not shown), suggesting that MEK1 may participate in this transduction signal.

FIG. 3.
Inhibition of the MMP-9 expression by blocking pattern recognition receptors. Differentiated THP-1 cells were pretreated with 5 μg/ml of anti-CD14, anti-TLR1, anti-TLR2, anti-mannose receptor, or control isotype antibodies for 30 min at 37°C, ...

Modulation of TIMP-1 transcription by LM.

Alteration in the relative expression of TIMPs has been ascribed in many lung disorders characterized by inflammation, tissue fibrosis, and destruction (1, 5). TIMP-1 is an endogenous key regulating molecule, produced by macrophages, which forms a bimolecular complex with MMP-9 to inactivate the enzyme (1). TIMP-1 mRNA expression levels were examined in differentiated THP-1 cells stimulated with LM, following a procedure similar to that described for MMP-9 mRNA expression. In contrast to MMP-9 mRNA, TIMP-1 mRNA was constitutively expressed in unstimulated THP-1 cells (Fig. (Fig.4).4). However, transcription of the TIMP-1 gene was significantly inhibited after 24 h of exposure to 10 μg/ml of LM. Stimulation with either LMMc or LMMk resulted in a reproducible 40% or 33% decrease in TIMP-1 gene expression compared to unstimulated cells. Altogether, disruption of the MMP-9/TIMP-1 gene expression balance by increasing of pro-MMP-9 and inhibiting TIMP-1 expression results in a net activation of MMP-9.

FIG. 4.
TIMP-1 mRNA expression in differentiated THP-1 cells in response to LM. Differentiated THP-1 cells were incubated for 24 h with 10 μg/ml of either LMMk (KanLM) or LMMc (CheLM) in RPMI-glutamine serum-free medium. Expression levels of TIMP-1 and ...

The present study demonstrates for the first time that LM, which represent major cell wall lipoglycans, are potent pro-MMP-9-inducing factors from human macrophages. Overall, these results suggest that LM may play a major functional role in the mycobacterial immunopathology through the induction of MMP-9. This may be a critical step towards controlling pathogen growth and influencing the outcome of the infection as well as host tissue injury. Recent work suggests that MMP-9 participates directly in tissue destruction in tuberculosis patients (28). However, whether LM contributes to tissue remodeling and damage processes occurring during the course of mycobacterial infection requires further work. In vivo administration of LM in mice followed by immunohistochemical detection of MMP-9 and TIMP-1 will help to define the eventual participation of LM in tissue damage.

Acknowledgments

This work was supported by the Université des Sciences et Technologies de Lille, the Institut Fédératif de Recherche 118, the Centre National de la Recherche Scientifique (UMR no. 8576; director J.-C. Michalski). L. Kremer is supported by a grant from the Centre National de la Recherche Scientifique (Action Thématique et Incitative sur Programme Microbiologie Fondamentale).

Notes

Editor: J. L. Flynn

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