Cyanovirin-N inhibits mannose-dependent Mycobacterium-C-type lectin interactions but does not protect against murine tuberculosis

Journal of Immunology

Volumn 189, Issue 7, 2012, Pages 3585-3592

  Driessen, Nicole N ^a,d   Boshoff, Helena I M ^b   Maaskant, Janneke J ^a   Gilissen, Sebastiaan A C ^a   Vink, Simone ^a   Van Der Sar, Astrid M ^a   Vandenbroucke Grauls, Christina M J E ^a   Bewley, Carole A ^c   Appelmelk, Ben J ^a   Geurtsen, Jeroen ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD209 ANTIGEN; CYANOVIRIN N; LECTIN; LIPOARABINOMANNAN; MANNOSE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; IN VIVO STUDY; LIGAND BINDING; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; TUBERCULOSIS;

ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; CELL LINE; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; LECTINS, C-TYPE; MACROPHAGES; MANNOSE; MICE; MICE, INBRED C57BL; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; TREATMENT OUTCOME; TUBERCULOSIS;

EID: 84866526429     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102408     Document Type: Article

References (43)

1. World Health Organization. 2010. Global tuberculosis control. World Health Organization report 2010. World Health Organization Press, Geneva, Switzerland. Report No.: WHO/HTM/TB/2010.7.
2. Fine, P. E. 1995. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 346: 1339-1345.
3. Torrelles, J. B., and L. S. Schlesinger. 2010. Diversity in Mycobacterium tuberculosis mannosylated cell wall determinants impacts adaptation to the host. Tuberculosis (Edinb.) 90: 84-93.
4. Schlesinger, L. S. 1993. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J. Immunol. 150: 2920-2930. (Pubitemid 23127541)
5. Tailleux, L., O. Schwartz, J. L. Herrmann, E. Pivert, M. Jackson, A. Amara, L. Legres, D. Dreher, L. P. Nicod, J. C. Gluckman, et al. 2003. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 197: 121-127. (Pubitemid 36110263)
6. Driessen, N. N., R. Ummels, J. J. Maaskant, S. S. Gurcha, G. S. Besra, G. D. Ainge, D. S. Larsen, G. F. Painter, C. M. Vandenbroucke-Grauls, J. Geurtsen, and B. J. Appelmelk. 2009. Role of phosphatidylinositol mannosides in the interaction between mycobacteria and DC-SIGN. Infect. Immun. 77: 4538-4547.
7. Geijtenbeek, T. B., S. J. Van Vliet, E. A. Koppel, M. Sanchez-Hernandez, C. M. Vandenbroucke-Grauls, B. Appelmelk, and Y. Van Kooyk. 2003. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197: 7-17. (Pubitemid 36110253)
8. Pitarque, S., J. L. Herrmann, J. L. Duteyrat, M. Jackson, G. R. Stewart, F. Lecointe, B. Payre, O. Schwartz, D. B. Young, G. Marchal, et al. 2005. Deciphering the molecular bases of Mycobacterium tuberculosis binding to the lectin DC-SIGN reveals an underestimated complexity. Biochem. J. 392: 615-624. (Pubitemid 43022742)
9. Torrelles, J. B., A. K. Azad, and L. S. Schlesinger. 2006. Fine discrimination in the recognition of individual species of phosphatidyl-myo- inositol mannosides from Mycobacterium tuberculosis by C-type lectin pattern recognition receptors. J. Immunol. 177: 1805-1816. (Pubitemid 44092518)
10. Ehlers, S. 2010. DC-SIGN and mannosylated surface structures of Mycobacterium tuberculosis: a deceptive liaison. Eur. J. Cell Biol. 89: 95-101.
11. Neyrolles, O., B. Gicquel, and L. Quintana-Murci. 2006. Towards a crucial role for DC-SIGN in tuberculosis and beyond. Trends Microbiol. 14: 383-387. (Pubitemid 44233297)
12. Boyd, M. R., K. R. Gustafson, J. B. McMahon, R. H. Shoemaker, B. R. O'Keefe, T. Mori, R. J. Gulakowski, L. Wu, M. I. Rivera, C. M. Laurencot, et al. 1997. Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development. Antimicrob. Agents Chemother. 41: 1521-1530. (Pubitemid 27289680)
13. Tsai, C. C., P. Emau, Y. Jiang, M. B. Agy, R. J. Shattock, A. Schmidt, W. R. Morton, K. R. Gustafson, and M. R. Boyd. 2004. Cyanovirin-N inhibits AIDS virus infections in vaginal transmission models. AIDS Res. Hum. Retroviruses 20: 11-18. (Pubitemid 38147172)
14. Xiong, S., J. Fan, and K. Kitazato. 2010. The antiviral protein cyanovirin-N: the current state of its production and applications. Appl. Microbiol. Biotechnol. 86: 805-812.
15. Balzarini, J., Y. Van Herrewege, K. Vermeire, G. Vanham, and D. Schols. 2007. Carbohydrate-binding agents efficiently prevent dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin (DC-SIGN)-directed HIV-1 transmission to T lymphocytes. Mol. Pharmacol. 71: 3-11. (Pubitemid 46020972)
16. Barrientos, L. G., F. Lasala, J. R. Otero, A. Sanchez, and R. Delgado. 2004. In vitro evaluation of cyanovirin-N antiviral activity, by use of lentiviral vectors pseudotyped with filovirus envelope glycoproteins. J. Infect. Dis. 189: 1440-1443. (Pubitemid 38543593)
17. Helle, F., C. Wychowski, N. Vu-Dac, K. R. Gustafson, C. Voisset, and J. Dubuisson. 2006. Cyanovirin-N inhibits hepatitis C virus entry by binding to envelope protein glycans. J. Biol. Chem. 281: 25177-25183. (Pubitemid 44401904)
18. Sambandamurthy, V. K., S. C. Derrick, K. V. Jalapathy, B. Chen, R. G. Russell, S. L. Morris, and W. R. Jacobs, Jr. 2005. Long-term protection against tuberculosis following vaccination with a severely attenuated double lysine and pantothenate auxotroph of Mycobacterium tuberculosis. Infect. Immun. 73: 1196-1203. (Pubitemid 40165781)
19. Behr, M. A., and P. M. Small. 1999. A historical and molecular phylogeny of BCG strains. Vaccine 17: 915-922. (Pubitemid 29074746)
20. Puttinaowarat, S., K. Thompson, J. Lilley, and A. Adams. 1999. Characterization of Mycobacterium spp. isolated from fish by pyrolysis mass spectrometry (PyMS) analysis. Inland Aquat. Anim. Health Res. Institute Newslett. 8: 4-8.
21. Bewley, C. A. 2001. Solution structure of a cyanovirin-N:Man α 1-2Man αcomplex: structural basis for high-affinity carbohydrate-mediated binding to gp120. Structure 9: 931-940. (Pubitemid 32972159)
22. 8) D1D3 and Man(9) with nanomolar affinity: implications for binding to the HIV envelope protein gp120. J. Am. Chem. Soc. 123: 3892-3902.
23. Wilson, M. B., and P. P. Nakane. 1978. Recent developments in the periodate method of conjugating horse radish peroxidase (HRPO) to antibodies. In Immunofluorescence and Related Staining Techniques. W. Knapp, K. Holubar, and G. Wick, eds. Elsevier/North Holland Biomedical, Amsterdam, pp. 215-224.
24. Wisdom, G. B. 1996. Horseradish peroxidase labeling of antibody using periodate oxidation. In The Protein Handbook, 2nd Ed., J. M. Walker, ed. Humana Press Inc., Totowa, NJ, pp. 273-274.
25. Appelmelk, B. J., J. den Dunnen, N. N. Driessen, R. Ummels, M. Pak, J. Nigou, G. Larrouy-Maumus, S. S. Gurcha, F. Movahedzadeh, J. Geurtsen, et al. 2008. The mannose cap of mycobacterial lipoarabinomannan does not dominate the Mycobacterium-host interaction. Cell. Microbiol. 10: 930-944. (Pubitemid 351386948)
26. Kolk, A. H., M. L. Ho, P. R. Klatser, T. A. Eggelte, S. Kuijper, S. de Jonge, and J. van Leeuwen. 1984. Production and characterization of monoclonal antibodies to Mycobacterium tuberculosis, M. bovis (BCG) and M. leprae. Clin. Exp. Immunol. 58: 511-521. (Pubitemid 15189978)
27. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
28. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76: 4350-4354. (Pubitemid 9256559)
29. Koppel, E. A., I. S. Ludwig, M. S. Hernandez, T. L. Lowary, R. R. Gadikota, A. B. Tuzikov, C. M. Vandenbroucke-Grauls, Y. van Kooyk, B. J. Appelmelk, and T. B. Geijtenbeek. 2004. Identification of the mycobacterial carbohydrate structure that binds the C-type lectins DC-SIGN, L-SIGN and SIGNR1. Immunobiology 209: 117-127. (Pubitemid 39255697)
30. Linehan, S. A., L. Martínez-Pomares, R. P. da Silva, and S. Gordon. 2001. Endogenous ligands of carbohydrate recognition domains of the mannose receptor in murine macrophages, endothelial cells and secretory cells; potential relevance to inflammation and immunity. Eur. J. Immunol. 31: 1857-1866. (Pubitemid 32547347)
31. Geijtenbeek, T. B., G. C. van Duijnhoven, S. J. van Vliet, E. Krieger, G. Vriend, C. G. Figdor, and Y. van Kooyk. 2002. Identification of different binding sites in the dendritic cell-specific receptor DC-SIGN for intercellular adhesion molecule 3 and HIV-1. J. Biol. Chem. 277: 11314-11320. (Pubitemid 34952896)
32. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179: 1109-1118.
33. Verreck, F. A., T. de Boer, D. M. Langenberg, M. A. Hoeve, M. Kramer, E. Vaisberg, R. Kastelein, A. Kolk, R. de Waal-Malefyt, and T. H. Ottenhoff. 2004. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc. Natl. Acad. Sci. USA 101: 4560-4565. (Pubitemid 38437450)
34. Tanne, A., B. Ma, F. Boudou, L. Tailleux, H. Botella, E. Badell, F. Levillain, M. E. Taylor, K. Drickamer, J. Nigou, et al. 2009. A murine DC-SIGN homologue contributes to early host defense against Mycobacterium tuberculosis. J. Exp. Med. 206: 2205-2220.
35. Boshoff, H. I., M. B. Reed, C. E. Barry, III, and V. Mizrahi. 2003. DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis. Cell 113: 183-193. (Pubitemid 36514970)
36. Schlesinger, L. S., S. R. Hull, and T. M. Kaufman. 1994. Binding of the terminal mannosyl units of lipoarabinomannan from a virulent strain of Mycobacterium tuberculosis to human macrophages. J. Immunol. 152: 4070-4079. (Pubitemid 24111079)
37. Mishra, A. K., N. N. Driessen, B. J. Appelmelk, and G. S. Besra. 2011. Lipoarabinomannan and related glycoconjugates: structure, biogenesis and role in Mycobacterium tuberculosis physiology and host-pathogen interaction. FEMS Microbiol. Rev. 35: 1126-1157.
38. Kang, P. B., A. K. Azad, J. B. Torrelles, T. M. Kaufman, A. Beharka, E. Tibesar, L. E. DesJardin, and L. S. Schlesinger. 2005. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J. Exp. Med. 202: 987-999. (Pubitemid 41396898)
39. Rajaram, M. V., M. N. Brooks, J. D. Morris, J. B. Torrelles, A. K. Azad, and L. S. Schlesinger. 2010. Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor gamma linking mannose receptor recognition to regulation of immune responses. J. Immunol. 185: 929-942.
40. Geurtsen, J., S. Chedammi, J. Mesters, M. Cot, N. N. Driessen, T. Sambou, R. Kakutani, R. Ummels, J. Maaskant, H. Takata, et al. 2009. Identification of mycobacterial a-glucan as a novel ligand for DC-SIGN: involvement of mycobacterial capsular polysaccharides in host immune modulation. J. Immunol. 183: 5221-5231.
41. Ernst, J. D. 1998. Macrophage receptors for Mycobacterium tuberculosis. Infect. Immun. 66: 1277-1281. (Pubitemid 128471479)
42. Tailleux, L., N. Pham-Thi, A. Bergeron-Lafaurie, J. L. Herrmann, P. Charles, O. Schwartz, P. Scheinmann, P. H. Lagrange, J. de Blic, A. Tazi, et al. 2005. DCSIGN induction in alveolar macrophages defines privileged target host cells for mycobacteria in patients with tuberculosis. PLoS Med. 2: e381.
43. Powlesland, A. S., E. M. Ward, S. K. Sadhu, Y. Guo, M. E. Taylor, and K. Drickamer. 2006. Widely divergent biochemical properties of the complete set of mouse DC-SIGN-related proteins. J. Biol. Chem. 281: 20440-20449. (Pubitemid 44065817)