Human immunodeficiency virus envelope (gp120) binding to DC-SIGN and primary dendritic cells is carbohydrate dependent but does not involve 2G12 or cyanovirin binding sites: Implications for structural analyses of gp120-DC-SIGN binding

Journal of Virology

Volumn 76, Issue 24, 2002, Pages 12855-12865

  Hong, Patrick W P ^a   Flummerfelt, Karen B ^a   De Parseval, Aymeric ^b   Gurney, Kevin ^a   Elder, John H ^b   Lee, Benhur ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CALCIUM ION; CARBOHYDRATE; CD209 ANTIGEN; CD4 ANTIGEN; CYANOVIRIN N; ENDO BETA N GLUCOSAMINIDASE H; EPITOPE; GLUCOSAMINIDASE; GLYCOPROTEIN GP 120; LECTIN; MANNAN; MANNOSE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2G12; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL LINE; CELL SURFACE; CONTROLLED STUDY; DENDRITIC CELL; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; LECTIN BINDING; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIMIAN IMMUNODEFICIENCY VIRUS; STRUCTURE ANALYSIS; T LYMPHOCYTE; VIRUS ENVELOPE; VIRUS MUTATION; WILD TYPE;

ANTIBODIES, MONOCLONAL; BACTERIAL PROTEINS; BINDING SITES; BINDING, COMPETITIVE; CARRIER PROTEINS; CELL ADHESION MOLECULES; CELL LINE; DENDRITIC CELLS; GLYCOSYLATION; HIV ENVELOPE PROTEIN GP120; HUMANS; LECTINS, C-TYPE; MANNOSE; RECEPTORS, CELL SURFACE;

EID: 0036892624     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.76.24.12855-12865.2002     Document Type: Article

References (48)

1. Baribaud, F., S. Pohlmann, T. Sparwasser, M. T. Kimata, Y. K. Choi, B. S. Haggarty, N. Ahmad, T. Macfarlan, T. G. Edwards, G. J. Leslie, J. Arnason, T. A. Reinhart, J. T. Kimata, D. R. Littman, J. A. Hoxie, and R. W. Doms. 2001. Functional and antigenic characterization of human, rhesus macaque, pigtailed macaque, and murine DC-sign. J. Virol. 75:10281-10289.
2. Bewley, C. A. 2001. Solution structure of a cyanovirin-N:Man α1-2Manα complex: Structural basis for high-affinity carbohydrate-mediated binding to gp120. Structure 9:931-940.
3. Bolmstedt, A. J., B. R. O'Keefe, S. R. Shenoy, J. B. McMahon, and M. R. Boyd. 2001. Cyanovirin-N defines a new class of antiviral agent targeting N-linked, high-mannose glycans in an oligosaccharide-specific manner. Mol. Pharmacol 59:949-954.
4. Choe, H., K. A. Martin, M. Farzan, J. Sodroski, N. P. Gerard, and C. Gerard. 1998. Structural interactions between chemokine receptors, gp120 Env and CD4. Semin. Immunol. 10:249-257.
5. Curtis, B. M., S. Scharnowske, and A. J. Watson. 1992. Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc. Natl. Acad. Sci. USA 89:8356-8360.
6. de Parseval, A., and J. H. Elder. 2001. Binding of recombinant feline immunodeficiency virus surface glycoprotein to feline cells: Role of CXCR4, cell-surface heparans, and an unidentified non-CXCR4 receptor. J. Virol. 75:4528-4539.
7. Dey, B., D. L. Lerner, P. Lusso, M. R. Boyd, J. H. Elder, and E. A. Berger. 2000. Multiple antiviral activities of cyanovirin-N: Blocking of human immunodeficiency virus type 1 gp120 interaction with CD4 and coreceptor and inhibition of diverse enveloped viruses. J. Virol. 74:4562-4569.
8. Doms, R. W., and D. Trono. 2000. The plasma membrane as a combat zone in the HIV battlefield. Genes Dev. 14:2677-2688.
9. Esser, M. T., T. Mori, I. Mondor, Q. J. Sattentau, B. Dey, E. A. Berger, M. R. Boyd, and J. D. Lifson. 1999. Cyanovirin-N binds to gp120 to interfere with CD4-dependent human immunodeficiency virus type 1 virion binding, fusion, and infectivity but does not affect the CD4 binding site on gp120 or soluble CD4-induced conformational changes in gp120. J. Virol. 73:4360-4371.
10. Feinberg, H., D. A. Mitchell, K. Drickamer, and W. I. Weis. 2001. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294:2163-2166.
11. Figdor, C. G., Y. van Kooyk, and G. J. Adema. 2002. C-type lectin receptors on dendritic cells and Langerhans cells. Nat. Rev. Immunol. 2:77-84.
12. Geijtenbeek, T. B., D. S. Kwon, R. Torensma, S. J. van Vliet, G. C. van Duljnhoven, J. Middel, I. L. Cornelissen, H. S. Nottet, V. N. KewalRamani, D. R. Littman, C. G. Figdor, and Y. van Kooyk. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587-597.
13. 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.
14. Gordon, C. J., M. A. Muesing, A. E. Proudfoot, C. A. Power, J. P. Moore, and A. Trkola. 1999. Enhancement of human immunodeficiency virus type 1 infection by the CC-chemokine RANTES is independent of the mechanism of virus-cell fusion. J. Virol. 73:684-694.
15. Hester, G., H. Kaku, I. J. Goldstein, and C. S. Wright. 1995. Structure of mannose-specific snowdrop (Galanthus nivalis) lectin is representative of a new plant lectin family. Nat. Struct. Biol. 2:472-479.
16. Hoffman, T. L., and R. W. Doms. 1999. HIV-1 envelope determinants for cell tropism and chemokine receptor use. Mol. Membr. Biol. 16:57-65.
17. Kunert, R., F. Ruker, and H. Katinger. 1998. Molecular characterization of five neutralizing anti-HIV type 1 antibodies: Identification of nonconventional D segments in the human monoclonal antibodies 2G12 and 2F5. AIDS Res. Hum. Retrovir. 14:1115-1128.
18. Kwon, D. S., G. Gregorio, N. Bitton, W. A. Hendrickson, and D. R. Littman. 2002. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T-cell infection. Immunity 16:135-144.
19. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
20. Lee, B., G. Leslie, E. Soilleux, U. O'Doherty, S. Baik, E. Levroney, K. Flummerfelt, W. Swiggard, N. Coleman, M. Malim, and R. W. Doms. 2001. cis Expression of DC-SIGN allows for more efficient entry of human and simian immunodeficiency viruses via CD4 and a coreceptor. J. Virol. 75:12028-12038.
21. Lee, R. T., Y. Ichikawa, T. Kawasaki, K. Drickamer, and Y. C. Lee. 1992. Multivalent ligand binding by serum mannose-binding protein. Arch. Biochem. Biophys. 299:129-136.
22. Lee, Y. C., R. T. Lee, K. Rice, Y. Ichikawa, and T.-C. Wong. 1991. Topography of binding sites of animal lectins: Ligands' view. Pure Appl. Chem. 63:499-506.
23. Maley, F., R. B. Trimble, A. L. Tarentino, and T. H. Plummer, Jr. 1989. Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal. Biochem. 180:195-204.
24. Means, R. E., and R. C. Desrosiers. 2000. Resistance of native, oligomeric envelope on simian immunodeficiency virus to digestion by glycosidases. J. Virol. 74:11181-11190.
25. Mitchell, D. A., A. J. Fadden, and K. Drickamer. 2001. A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR: Subunit organization and binding to multivalent ligands. J. Biol. Chem. 276:28939-28945.
26. O'Keefe, B. R., S. R. Shenoy, D. Xie, W. Zhang, J. M. Muschik, M. J. Currens, I. Chaiken, and M. R. Boyd. 2000. Analysis of the interaction between the HIV-inactivating protein cyanovirin-N and soluble forms of the envelope glycoproteins gp120 and gp41. Mol. Pharmacol. 58:982-992.
27. Pohlmann, S., F. Baribaud, and R. W. Doms. 2001. DC-SIGN and DC-SIGNR: Helping hands for HIV. Trends Immunol. 22:643-646.
28. Pohlmann, S., F. Baribaud, B. Lee, G. J. Leslie, M. D. Sanchez, K. Hiebenthal-Millow, J. Munch, F. Kirchhoff, and R. W. Doms. 2001. DC-SIGN interactions with human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus. J. Virol. 75:4664-4672.
29. Reitter, J. N., R. E. Means, and R. C. Desrosiers. 1998. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 4:679-684.
30. Sanders, R. W., M. Venturi, L. Schiffner, R. Kalyanaraman, H. Katinger, K. O. Lloyd, P. D. Kwong, and J. P. Moore. 2002. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76:7293-7305.
31. Sharron, M., S. Pohlmann, K. Price, E. Lolis, M. Tsang, F. Kirchhoff, R. W. Doms, and B. Lee. 2000. Expression and coreceptor activity of STRL33/Bonzo on primary peripheral blood lymphocytes. Blood 96:41-49.
32. Shenoy, S. R., B. R. O'Keefe, A. J. Bolmstedt, L. K. Cartner, and M. R. Boyd. 2001. Selective interactions of the human immunodeficiency virus-inactivating protein cyanovirin-N with high-mannose oligosaccharides on gp120 and other glycoproteins. J. Pharmacol. Exp. Ther. 297:704-710.
33. Sheriff, S., C. Y. Chang, and R. A. Ezekowitz. 1994. Human mannose-binding protein carbohydrate recognition domain trimerizes through a triple alphahelical coiled-coil. Nat. Struct. Biol. 1:789-794.
34. Soilleux, E. J., L. S. Morris, G. Leslie, J. Chehimi, Q. Luo, E. Levroney, J. Trowsdale, L. J. Montaner, R. W. Doms, D. Weissman, N. Coleman, and B. Lee. Constitutive and induced expression of DC-SIGN on dendritic cell and macrophage subpopulations in situ and in vitro. J. Leukoc. Biol. 71:445-457.
35. Steinman, R. M. 2000. DC-SIGN: A guide to some mysteries of dendritic cells. Cell 100:491-494.
36. Trkola, A., C. Gordon, J. Matthews, E. Maxwell, T. Ketas, L. Czaplewski, A. E. Proudfoot, and J. P. Moore. 1999. The CC-chemokine RANTES increases the attachment of human immunodeficiency virus type 1 to target cells via glycosaminoglycans and also activates a signal transduction pathway that enhances viral infectivity. J. Virol. 73:6370-6379.
37. Trkola, A., M. Purtscher, T. Muster, C. Ballaun, A. Buchacher, N. Sullivan, K. Srinivasan, J. Sodroski, J. P. Moore, and H. Katinger. 1996. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70:1100-1108.
38. Turville, S. G., J. Arthos, K. M. Donald, G. Lynch, H. Naif, G. Clark, D. Hart, and A. L. Cunningham. 2001. HIV gp120 receptors on human dendritic cells. Blood 98:2482-2488.
39. Ugolini, S., I. Mondor, and Q. J. Sattentau. 1999. HIV-1 attachment: Another look. Trends Microbiol. 7:144-149.
40. Weis, W. I., and K. Drickamer. 1996. Structural basis of lectin-carbohydrate recognition. Annu. Rev. Biochem. 65:441-473.
41. Weis, W. I., M. E. Taylor, and K. Drickamer. 1998. The C-type lectin superfamily in the immune system. Immunol. Rev. 163:19-34.
42. Wright, C. S., and G. Hester. 1996. The 2.0 Å structure of a cross-linked complex between snowdrop lectin and a branched mannopentaose: Evidence for two unique binding modes. Structure 4:1339-1352.
43. Wu, L., A. A. Bashirova, T. D. Martin, L. Villamide, E. Mehlhop, A. O. Chertov, D. Unutmaz, M. Pope, M. Carrington, and V. N. KewalRamani. 2002. Rhesus macaque dendritic cells efficiently transmit primate lentiviruses independently of DC-SIGN. Proc. Natl. Acad. Sci. USA 99:1568-1573.
44. Wu, L., T. D. Martin, R. Vazeux, D. Unutmaz, and V. N. KewalRamani. 2002. Functional evaluation of DC-SIGN monoclonal antibodies reveals DCSIGN interactions with ICAM-3 do not promote human immunodeficiency virus type 1 transmission. J. Virol. 76:5905-5914.
45. Wyatt, R., P. D. Kwong, E. Desjardins, R. W. Sweet, J. Robinson, W. A. Hendrickson, and J. G. Sodroski. 1998. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393:705-711.
46. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: Fusogens, antigens, and immunogens. Science 280:1884-1888.
47. Yamashita, K., K. Totani, T. Ohkura, S. Takasaki, I. J. Goldstein, and A. Kobata. 1987. Carbohydrate binding properties of complex-type oligosaccharides on immobilized Datura stramonium lectin. J. Biol. Chem. 262:1602-1607.
48. Zhu, X., C. Borchers, R. J. Bienstock, and K. B. Tomer. 2000. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry 39:11194-11204.