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Mycobacteria Target DC-SIGN to Suppress Dendritic Cell Function

Teunis B.H. Geijtenbeek¹, Sandra J. van Vliet¹, Estella A. Koppel¹, Marta Sanchez-Hernandez¹, Christine M.J.E. Vandenbroucke-Grauls², Ben Appelmelk² and Yvette van Kooyk¹

¹ Department of Molecular Cell Biology, Vrije Universiteit Medical Center Amsterdam, 1081 BT Amsterdam, Netherlands
² Department of Medical Microbiology, Vrije Universiteit Medical Center Amsterdam, 1081 BT Amsterdam, Netherlands

Address correspondence to T. Geijtenbeek, Department of Molecular Cell Biology, Free University Medical Center Amsterdam, v.d. Boechorststraat 7, 1081 BT Amsterdam, Netherlands. Phone: 31-20-4448080; Fax: 31-20-4448081; E-mail: T.Geijtenbeek.Cell{at}med.vu.nl

Mycobacterium tuberculosis represents a world-wide health risk and immunosuppression is a particular problem in M. tuberculosis infections. Although macrophages are primarily infected, dendritic cells (DCs) are important in inducing cellular immune responses against M. tuberculosis. We hypothesized that DCs represent a target for M. tuberculosis and that the observed immuno-suppression results from modulation of DC functions. We demonstrate that the DC-specific C-type lectin DC-SIGN is an important receptor on DCs that captures and internalizes intact Mycobacterium bovis bacillus Calmette-Guérin (BCG) through the mycobacterial cell wall component ManLAM. Antibodies against DC-SIGN block M. bovis BCG infection of DCs. ManLAM is also secreted by M. tuberculosis–infected macrophages and has been implicated as a virulence factor. Strikingly, ManLAM binding to DC-SIGN prevents mycobacteria- or LPS-induced DC maturation. Both mycobacteria and LPS induce DC maturation through Toll-like receptor (TLR) signaling, suggesting that DC-SIGN, upon binding of ManLAM, interferes with TLR-mediated signals. Blocking antibodies against DC-SIGN reverse the ManLAM-mediated immunosuppressive effects. Our results suggest that M. tuberculosis targets DC-SIGN both to infect DCs and to down-regulate DC-mediated immune responses. Moreover, we demonstrate that DC-SIGN has a broader pathogen recognition profile than previously shown, suggesting that DC-SIGN may represent a molecular target for clinical intervention in infections other than HIV-1.

Key Words: DC-SIGN • Toll-like receptors • Mycobacterium tuberculosis • ManLAM • immunosuppression

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• van Vliet, S. J., van Liempt, E., Saeland, E., Aarnoudse, C. A., Appelmelk, B., Irimura, T., Geijtenbeek, T. B. H., Blixt, O., Alvarez, R., van Die, I., van Kooyk, Y. (2005). Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int Immunol 17: 661-669 [Abstract] [Full Text]  
• van Gisbergen, K. P.J.M., Sanchez-Hernandez, M., Geijtenbeek, T. B.H., van Kooyk, Y. (2005). Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. JEM 201: 1281-1292 [Abstract] [Full Text]  
• Snyder, G. A., Ford, J., Torabi-Parizi, P., Arthos, J. A., Schuck, P., Colonna, M., Sun, P. D. (2005). Characterization of DC-SIGN/R Interaction with Human Immunodeficiency Virus Type 1 gp120 and ICAM Molecules Favors the Receptor's Role as an Antigen-Capturing Rather than an Adhesion Receptor. J. Virol. 79: 4589-4598 [Abstract] [Full Text]  
• Kleindienst, P., Wiethe, C., Lutz, M. B., Brocker, T. (2005). Simultaneous Induction of CD4 T Cell Tolerance and CD8 T Cell Immunity by Semimature Dendritic Cells. J. Immunol. 174: 3941-3947 [Abstract] [Full Text]  
• Buettner, M., Meinken, C., Bastian, M., Bhat, R., Stossel, E., Faller, G., Cianciolo, G., Ficker, J., Wagner, M., Rollinghoff, M., Stenger, S. (2005). Inverse Correlation of Maturity and Antibacterial Activity in Human Dendritic Cells. J. Immunol. 174: 4203-4209 [Abstract] [Full Text]  
• Klena, J., Zhang, P., Schwartz, O., Hull, S., Chen, T. (2005). The Core Lipopolysaccharide of Escherichia coli Is a Ligand for the Dendritic-Cell-Specific Intercellular Adhesion Molecule Nonintegrin CD209 Receptor. J. Bacteriol. 187: 1710-1715 [Abstract] [Full Text]  
• Pulendran, B. (2005). Variegation of the Immune Response with Dendritic Cells and Pathogen Recognition Receptors. J. Immunol. 174: 2457-2465 [Abstract] [Full Text]  
• McKenna, K., Beignon, A.-S., Bhardwaj, N. (2005). Plasmacytoid Dendritic Cells: Linking Innate and Adaptive Immunity. J. Virol. 79: 17-27 [Full Text]  
• Kissenpfennig, A., Ait-Yahia, S., Clair-Moninot, V., Stossel, H., Badell, E., Bordat, Y., Pooley, J. L., Lang, T., Prina, E., Coste, I., Gresser, O., Renno, T., Winter, N., Milon, G., Shortman, K., Romani, N., Lebecque, S., Malissen, B., Saeland, S., Douillard, P. (2005). Disruption of the langerin/CD207 Gene Abolishes Birbeck Granules without a Marked Loss of Langerhans Cell Function. Mol. Cell. Biol. 25: 88-99 [Abstract] [Full Text]  
• Kane, C. M., Cervi, L., Sun, J., McKee, A. S., Masek, K. S., Shapira, S., Hunter, C. A., Pearce, E. J. (2004). Helminth Antigens Modulate TLR-Initiated Dendritic Cell Activation. J. Immunol. 173: 7454-7461 [Abstract] [Full Text]  
• Lanoue, A., Clatworthy, M. R., Smith, P., Green, S., Townsend, M. J., Jolin, H. E., Smith, K. G.C., Fallon, P. G., McKenzie, A. N.J. (2004). SIGN-R1 Contributes to Protection against Lethal Pneumococcal Infection in Mice. JEM 200: 1383-1393 [Abstract] [Full Text]  
• Nicolle, D., Fremond, C., Pichon, X., Bouchot, A., Maillet, I., Ryffel, B., Quesniaux, V. J. F. (2004). Long-Term Control of Mycobacterium bovis BCG Infection in the Absence of Toll-Like Receptors (TLRs): Investigation of TLR2-, TLR6-, or TLR2-TLR4-Deficient Mice. Infect. Immun. 72: 6994-7004 [Abstract] [Full Text]  
• Arrighi, J.-F., Pion, M., Garcia, E., Escola, J.-M., van Kooyk, Y., Geijtenbeek, T. B., Piguet, V. (2004). DC-SIGN-mediated Infectious Synapse Formation Enhances X4 HIV-1 Transmission from Dendritic Cells to T Cells. JEM 200: 1279-1288 [Abstract] [Full Text]  
• Serrano-Gomez, D., Dominguez-Soto, A., Ancochea, J., Jimenez-Heffernan, J. A., Leal, J. A., Corbi, A. L. (2004). Dendritic Cell-Specific Intercellular Adhesion Molecule 3-Grabbing Nonintegrin Mediates Binding and Internalization of Aspergillus fumigatus Conidia by Dendritic Cells and Macrophages. J. Immunol. 173: 5635-5643 [Abstract] [Full Text]  
• Bergman, M. P., Engering, A., Smits, H. H., van Vliet, S. J., van Bodegraven, A. A., Wirth, H.-P., Kapsenberg, M. L., Vandenbroucke-Grauls, C. M.J.E., van Kooyk, Y., Appelmelk, B. J. (2004). Helicobacter pylori Modulates the T Helper Cell 1/T Helper Cell 2 Balance through Phase-variable Interaction between Lipopolysaccharide and DC-SIGN. JEM 200: 979-990 [Abstract] [Full Text]  
• Arrighi, J.-F., Pion, M., Wiznerowicz, M., Geijtenbeek, T. B., Garcia, E., Abraham, S., Leuba, F., Dutoit, V., Ducrey-Rundquist, O., van Kooyk, Y., Trono, D., Piguet, V. (2004). Lentivirus-Mediated RNA Interference of DC-SIGN Expression Inhibits Human Immunodeficiency Virus Transmission from Dendritic Cells to T Cells. J. Virol. 78: 10848-10855 [Abstract] [Full Text]  
• Niiya, H., Azuma, T., Jin, L., Uchida, N., Inoue, A., Hasegawa, H., Fujita, S., Tohyama, M., Hashimoto, K., Yasukawa, M. (2004). Transcriptional downregulation of DC-SIGN in human herpesvirus 6-infected dendritic cells. J. Gen. Virol. 85: 2639-2642 [Abstract] [Full Text]  
• Jang, S., Uematsu, S., Akira, S., Salgame, P. (2004). IL-6 and IL-10 Induction from Dendritic Cells in Response to Mycobacterium tuberculosis Is Predominantly Dependent on TLR2-Mediated Recognition. J. Immunol. 173: 3392-3397 [Abstract] [Full Text]  
• Van Liempt, E., Imberty, A., Bank, C. M. C., Van Vliet, S. J., Van Kooyk, Y., Geijtenbeek, T. B. H., Van Die, I. (2004). Molecular Basis of the Differences in Binding Properties of the Highly Related C-type Lectins DC-SIGN and L-SIGN to Lewis X Trisaccharide and Schistosoma mansoni Egg Antigens. J. Biol. Chem. 279: 33161-33167 [Abstract] [Full Text]  
• Mariotti, S., Teloni, R., Iona, E., Fattorini, L., Romagnoli, G., Gagliardi, M. C., Orefici, G., Nisini, R. (2004). Mycobacterium tuberculosis Diverts Alpha Interferon-Induced Monocyte Differentiation from Dendritic Cells into Immunoprivileged Macrophage-Like Host Cells. Infect. Immun. 72: 4385-4392 [Abstract] [Full Text]  
• Ludwig, I. S., Lekkerkerker, A. N., Depla, E., Bosman, F., Musters, R. J. P., Depraetere, S., van Kooyk, Y., Geijtenbeek, T. B. H. (2004). Hepatitis C Virus Targets DC-SIGN and L-SIGN To Escape Lysosomal Degradation. J. Virol. 78: 8322-8332 [Abstract] [Full Text]  
• Puig-Kroger, A., Serrano-Gomez, D., Caparros, E., Dominguez-Soto, A., Relloso, M., Colmenares, M., Martinez-Munoz, L., Longo, N., Sanchez-Sanchez, N., Rincon, M., Rivas, L., Sanchez-Mateos, P., Fernandez-Ruiz, E., Corbi, A. L. (2004). Regulated Expression of the Pathogen Receptor Dendritic Cell-specific Intercellular Adhesion Molecule 3 (ICAM-3)-grabbing Nonintegrin in THP-1 Human Leukemic Cells, Monocytes, and Macrophages. J. Biol. Chem. 279: 25680-25688 [Abstract] [Full Text]  
• Takahara, K., Yashima, Y., Omatsu, Y., Yoshida, H., Kimura, Y., Kang, Y.-S., Steinman, R. M., Park, C. G., Inaba, K. (2004). Functional comparison of the mouse DC-SIGN, SIGNR1, SIGNR3 and Langerin, C-type lectins. Int Immunol 16: 819-829 [Abstract] [Full Text]  
• Woltman, A. M., Schlagwein, N., van der Kooij, S. W., van Kooten, C. (2004). The Novel Cyclophilin-Binding Drug Sanglifehrin A Specifically Affects Antigen Uptake Receptor Expression and Endocytic Capacity of Human Dendritic Cells. J. Immunol. 172: 6482-6489 [Abstract] [Full Text]  
• Karlsson, H., Larsson, P., Wold, A. E., Rudin, A. (2004). Pattern of Cytokine Responses to Gram-Positive and Gram-Negative Commensal Bacteria Is Profoundly Changed when Monocytes Differentiate into Dendritic Cells. Infect. Immun. 72: 2671-2678 [Abstract] [Full Text]  

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