Evolutionary dynamics of the glycan shield of the human immunodeficiency virus envelope during natural infection and implications for exposure of the 2G12 epitope

Journal of Virology

Volumn 78, Issue 22, 2004, Pages 12625-12637

  Bacheux, Laurent ^a   Moreau, Alain ^a   Ataman Önal, Yasemin ^b   Biron, François ^c   Verrier, Bernard ^b   Barin, Francis ^a,d  

^a UNIVERSITÉ DE TOURS   (France)

^b BIOMÉRIEUX   (France)

^c CROIX ROUSSE HOSPITAL   (France)

^d CHU BRETONNEAU   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLYCAN; GLYCOPROTEIN; HUMAN MONOCLONAL ANTIBODY;

AMINO ACID SEQUENCE; ANTIGENICITY; ARTICLE; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; KINETICS; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VIRUS ENVELOPE;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIGENS, CD4; EPITOPES; EVOLUTION, MOLECULAR; GENE PRODUCTS, ENV; GLYCOSYLATION; HIV ANTIBODIES; HIV-1; HUMANS; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYSACCHARIDES;

EID: 7644239787     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.22.12625-12637.2004     Document Type: Article

References (54)

1. Ataman-Onal, Y., C. Coiffier, A. Giraud, A. Babic-Erceg, F. Biron, and B. Verrier. 1999. Comparison of complete env gene sequences from individuals with symptomatic primary HIV type 1 infection. AIDS Res. Hum. Retrovir. 15:1035-1039.
2. Baba, T. W., V. Liska, R. Hofmann-Lehmann, J. Vlasak, W. Xu, S. Ayehunie, L. A. Cavacini, M. R. Posner, H. Katinger, G. Stiegler, B. J. Bernacky, T. A. Rizvi, R. Schmidt, L. R. Hill, M. E. Keeling, Y. Lu, J. E. Wright, T. C. Chou, and R. M. Ruprecht. 2000. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat. Med. 6:200-206.
3. Barin, F., S. Brunet, D. Brand, C. Moog, R. Peyre, F. Damond, P. Charneau, and F. Barré-Sinoussi. 2004. Interclade neutralization and enhancement of human immunodeficiency virus type 1 identified by an assay using HeLa cells expressing both CD4 receptor and CXCR4/CCR5 coreceptors. J. Infect. Dis. 189:322-327.
4. Binley, J. M., R. Wyatt, E. Desjardins, P. D. Kwong, W. Hendrickson, J. P. Moore, and J. Sodroski. 1998. Analysis of the interaction of antibodies with a conserved enzymatically deglycosylated core of the HIV type 1 envelope glycoprotein 120. AIDS Res. Hum. Retrovir. 14:191-198.
5. Brand, D., F. Lemiale, G. Thibault, B. Verrier, S. Lebigot, P. Roingeard, L. Buzelay, S. Brunet, and F. Barin. 2000. Antigenic properties of recombinant envelope glycoproteins derived from T-cell-line-adapted isolates or primary human immunodeficiency virus isolates and their relationship to immunogenicity. Virology 271:350-362.
6. Burton, D. R. 1997. A vaccine for HIV type 1: the antibody perspective. Proc. Natl. Acad. Sci. USA 94:10018-10023.
7. Burton, D. R., and D. C. Montefiori. 1997. The antibody response in HIV-1 infection. AIDS 11(Suppl. A):S87-S98.
8. Burton, D. R., J. Pyati, R. Koduri, S. J. Sharp, G. B. Thornton, P. W. Parren, L. S. Sawyer, R. M. Hendry, N. Dunlop, P. L. Nara, et al. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024-1027.
9. Burton, D. R., R. C. Desrosiers, R. W. Doms, M. B. Feinberg, R. C. Gallo, B. Hahn, J. A. Hoxie, E. Hunter, B. Korber, A. Landay, M. M. Lederman, J. Lieberman, J. M. McCune, J. P. Moore, N. Nathanson, L. Picker, D. Richman, C. Rinaldo, M. Stevenson, D. I. Watkins, S. M. Wolinsky, and J. A. Zack. 2004. A sound rationale needed for phase III HIV-1 vaccine trials. Science 303:316.
10. Calarese, D. A., C. N. Scanlan, M. B. Zwick, S. Deechongkit, Y. Mimura, R. Kunert, P. Zhu, M. R. Wormald, R. L. Stanfield, K. H. Roux, J. W. Kelly, P. M. Rudd, R. A. Dwek, H. Katinger, D. R. Burton, and I. A. Wilson. 2003. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300:2065-2071.
11. Cao, Y., L. Qin, L. Zhang, J. Safrit, and D. D. Ho. 1995. Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N. Engl. J. Med. 332:201-208.
12. Conley, A. J., J. A. Kessler II, L. J. Boots, J. S. Tung, B. A. Arnold, P. M. Keller, A. R. Shaw, and E. A. Emini. 1994. Neutralization of divergent human immunodeficiency virus type 1 variants and primary isolates by IAM-41-2F5, an anti-gp41 human monoclonal antibody. Proc. Natl. Acad. Sci. USA 91:3348-3352.
13. D'Souza, M. P., D. Livnat, J. A. Bradac, S. H. Bridges, et al. 1997. Evaluation of monoclonal antibodies to human immunodeficiency virus type 1 primary isolates by neutralization assays: performance criteria for selecting candidate antibodies for clinical trials. J. Infect. Dis. 175:1056-1062.
14. Fouts, T. R., J. M. Binley, A. Trkola, J. E. Robinson, and J. P. Moore. 1997. Neutralization of the human immunodeficiency virus type 1 primary isolate JR-FL by human monoclonal antibodies correlates with antibody binding to the oligomeric form of the envelope glycoprotein complex. J. Virol. 71:2779-2785.
15. Gauduin, M. C., P. W. Parren, R. Weir, C. F. Barbas, D. R. Burton, and R. A. Koup. 1997. Passive immunization with a human monoclonal antibody protects hu-PBL-SCID mice against challenge by primary isolates of HIV-1. Nat. Med. 3:1389-1393.
16. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
17. Hofmann-Lebmann, R., R. A. Rasmussen, J. Vlasak, B. A. Smith, T. W. Baba, V. Liska, D. C. Montefiori, H. M. McClure, D. C. Anderson, B. J. Bernacky, T. A. Rizvi, R. Schmidt, L. R. Hill, M. E. Keeling, H. Katinger, G. Stiegler, M. R. Posner, L. A. Cavacini, T. C. Chou, and R. M. Ruprecht. 2001. Passive immunization against oral AIDS virus transmission: an approach to prevent mother-to-infant HIV-1 transmission? J. Med. Primatol. 30:190-196.
18. Korber, B., B. T. Foley, C. Kuiken, S. K. Pillai, and J. G. Sodroski. 1998. Numbering positions in HIV relative to HXB2CG, p. III-102-III-111. In B. Korber, C. L. Kuiken, B. Foley, F. Hahn, F. McCutchan, J. W. Mellors, and J. Sodroski (ed.), Human retroviruses and AIDS 1998. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, N. Mex.
19. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244-1245.
20. 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.
21. Kwong, P. D., R. Wyatt, S. Majeed, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 2000. Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure Fold Des. 8:1329-1339.
22. 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.
23. Mascola, J. R., M. G. Lewis, G. Stiegler, D. Harris, T. C. VanCott, D. Hayes, M. K. Louder, C. R. Brown, C. V. Sapan, S. S. Frankel, Y. Lu, M. L. Robb, H. Katinger, and D. L. Birx. 1999. Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J. Virol. 73:4009-4018.
24. Mascola, J. R., G. Stiegler, T. C. VanCott, H. Katinger, C. B. Carpenter, C. E. Hanson, H. Beary, D. Hayes, S. S. Frankel, D. L. Birx, and M. G. Lewis. 2000. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6:207-210.
25. Mo, H., L. Stamalatos, J. E. Ip, C. F. Barbas, P. W. Parren, D. R. Burton, J. P. Moore, and D. D. Ho. 1997. Human immunodeficiency virus type 1 mutants that escape neutralization by human monoclonal antibody IgG1b12. J. Virol. 71:6869-6874.
26. Moog, C., H. J. Fleury, I. Pellegrin, A. Kim, and A. M. Aubertin. 1997. Autologous and heterologous neutralizing antibody responses following initial seroconversion in human immunodeficiency virus type 1-infected individuals. J. Virol. 71:3734-3741.
27. Moore, J. P., Y. Cao, D. D. Ho, and R. A. Koup. 1994. Development of the anti-gp120 antibody response during seroconversion to human immunodeficiency virus type 1. J. Virol. 68:5142-5155.
28. Moore, J. P., F. E. McCutchan, S. W. Poon, J. Mascola, J. Liu, Y. Cao, and D. D. Ho. 1994. Exploration of antigenic variation in gp120 from clades A through F of human immunodeficiency virus type 1 by using monoclonal antibodies. J. Virol. 68:8350-8364.
29. Moulard, M., S. K. Phogat, Y. Shu, A. F. Labrijn, X. Xiao, J. M. Binley, M. Y. Zhang, I. A. Sidorov, C. C. Broder, J. Robinson, P. W. Parren, D. R. Burton, and D. S. Dimitrov. 2002. Broadly cross-reactive HIV-1-neutralizing human monoclonal Fab selected for binding to gp120-CD4-CCR5 complexes. Proc. Natl. Acad. Sci. USA 99:6913-6918.
30. Muster, T., F. Steindl, M. Purtscher, A. Trkola, A. Klima, G. Himmler, F. Ruker, and H. Katinger. 1993. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 67:6642-6647.
31. Ohagen, A., A. Devitt, K. J. Kunstman, P. R. Gorry, P. P. Rose, B. Korber, J. Taylor, R. Levy, R. L. Murphy, S. M. Wolinsky, and D. Gabuzda. 2003. Genetic and functional analysis of full-length human immunodeficiency virus type 1 env genes derived from brain and blood of patients with AIDS. J. Virol. 77:12336-12345.
32. Pantophlet, R., E. Ollmann Saphire, P. Poignard, P. W. Parren, I. A. Wilson, and D. R. Burton. 2003. Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120. J. Virol. 77:642-658.
33. Parker, C. E., L. J. Deterding, C. Hager-Braun, J. M. Binley, N. Schulke, H. Katinger, J. P. Moore, and K. B. Tomer, 2001. Fine definition of the epitope on the gp41 glycoprotein of human immunodeficiency virus type 1 for the neutralizing monoclonal antibody 2F5. J. Virol. 75:10906-10911.
34. Parren, P. W., H. J. Ditzel, R. J. Gulizia, J. M. Binley, C. F. Barbas III, D. R. Burton, and D. E. Mosier. 1995. Protection against HIV-1 infection in hu-PBL-SCID mice by passive immunization with a neutralizing human monoclonal antibody against the gp120 CD4-binding site. AIDS 9:F1-F6.
35. Parren, P. W., P. A. Marx, A. J. Hessell, A. Luckay, J. Harouse, C. Cheng-Mayer, J. P. Moore, and D. R. Burton. 2001. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75:8340-8347.
36. Parren, P. W., J. P. Moore, D. R. Burton, and Q. J. Sattentau. 1999. The neutralizing antibody response to HIV-1: viral evasion and escape from humoral immunity. AIDS 13(Suppl. A):S137-S162.
37. Poignard, P., R. Sabbe, G. R. Picchio, M. Wang, R. J. Gulizia, H. Katinger, P. W. Parren, D. E. Mosier, and D. R. Burton. 1999. Neutralizing antibodies have limited effects on the control of established HIV-1 infection in vivo. Immunity 10:431-438.
38. Purtscher, M., A. Trkola, A. Grassauer, P. M. Schulz, A. Klima, S. Dopper, G. Gruber, A. Buchacher, T. Muster, and H. Katinger. 1996. Restricted antigenic variability of the epitope recognized by the neutralizing gp41 antibody 2F5. AIDS 10:587-593.
39. Richman, D. D., T. Wrin, S. J. Little, and C. J. Petropoulos. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA 100:4144-4149.
40. Roben, P., J. P. Moore, M. Thali, J. Sodroski, C. F. Barbas III, and D. R. Burton. 1994. Recognition properties of a panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1. J. Virol. 68:4821-4828.
41. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
42. 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.
43. Saphire, E. O., P. W. Parren, R. Pantophlet, M. B. Zwick, G. M. Morris, P. M. Rudd, R. A. Dwek, R. L. Stanfield, D. R. Burton, and I. A. Wilson. 2001. Crystal structure of a neutralizing human IgG against HIV-1: a template for vaccine design. Science 293:1155-1159.
44. Scanlan, C. N., R. Pantopblet, M. R. Wormald, E. Ollmann Saphire, R. Stanfield, I. A. Wilson, H. Katinger, R. A. Dwek, P. M. Rudd, and D. R. Burton. 2002. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of α1→2 mannose residues on the outer face of gp120. J. Virol. 76:7306-7321.
45. Stiegler, G., R. Kunert, M. Purtscher, S. Wolbank, R. Voglauer, F. Steindl, and H. Katinger. 2001. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 17:1757-1765.
46. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
47. Trkola, A., A. B. Pomales, H. Yuan, B. Korber, P. J. Maddon, G. P. Allaway, H. Katinger, C. F. Barbas III, D. R. Burton, D. D. Ho, and J. P. Moore. 1995. Cross-clade neutralization of primary isolates of human immunodeficiency vims type 1 by human monoclonal antibodies and tetrameric CD4-IgG. J. Virol. 69:6609-6617.
48. 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.
49. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
50. 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.
51. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888.
52. Zhang, Y. J., C. Fracasso, J. R. Fiore, A. Bjorndal, G. Angarano, A. Gringeri, and E. M. Fenyo. 1997. Augmented serum neutralizing activity against primary human immunodeficiency virus type 1 (HIV-1) isolates in two groups of HIV-1 infected long-term nonprogressors. J. Infect. Dis. 176:1180-1187.
53. Zwick, M. B., R. Kelleher, R. Jensen, A. F. Labrijn, M. Wang, G. V. Quinnan, Jr., P. W. Parren, and D. R. Burton. 2003. A novel human antibody against human immunodeficiency virus type 1 gp120 is V1, V2, and V3 loop dependent and helps delimit the epitope of the broadly neutralizing antibody immunoglobulin G1 b12. J. Virol. 77:6965-6978.
54. Zwick, M. B., A. F. Labrijn, M. Wang, C. Spenlehauer, E. O. Saphire, J. M. Binley, J. P. Moore, G. Stiegler, H. Katinger, D. R. Burton, and P. W. Parren. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75:10892-10905.