Neutralization efficiency is greatly enhanced by bivalent binding of an antibody to epitopes in the V4 region and the membrane-proximal external region within one trimer of human immunodeficiency virus type 1 glycoproteins

Journal of Virology

Volumn 84, Issue 14, 2010, Pages 7114-7123

  Wang, Pengcheng ^a,b   Yang, Xinzhen ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MEDICAL COLLEGE OF JINAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; IMMUNOGLOBULIN G; PROTEIN MPER; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; GENE INSERTION; GENETIC ENGINEERING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; BINDING SITES, ANTIBODY; CELL LINE; EPITOPES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; VIRION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77953786430     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00545-10     Document Type: Article

References (68)

1. Amano, H., and Y. Hosaka. 1992. Morphological estimation of total number of influenza A type virion spikes. J. Electron Microsc. (Tokyo) 41:104-106.
2. Andersson, A., V. Vetter, L. Kreutzer, and G. Bauer. 1994. Avidities of IgG directed against viral capsid antigen or early antigen: useful markers for significant Epstein-Barr virus serology. J. Med. Virol. 43:238-244.
3. Barbato, G., E. Bianchi, P. Ingallinella, W. H. Hurni, M. D. Miller, G. Ciliberto, R. Cortese, R. Bazzo, J. W. Shiver, and A. Pessi. 2003. Structural analysis of the epitope of the anti-HIV antibody 2F5 sheds light into its mechanism of neutralization and HIV fusion. J. Mol. Biol. 330:1101-1115.
4. Bennett, A., J. Liu, D. Van Ryk, D. Bliss, J. Arthos, R. M. Henderson, and S. Subramaniam. 2007. Cryoelectron tomographic analysis of an HIV-neutralizing protein and its complex with native viral gp120. J. Biol. Chem. 282:27754-27759.
5. 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.
6. Burton, D. R., E. O. Saphire, and P. W. Parren. 2001. A model for neutralization of viruses based on antibody coating of the virion surface. Curr. Top. Microbiol. Immunol. 260:109-143.
7. Burton, D. R., R. A. Williamson, and P. W. Parren. 2000. Antibody and virus: binding and neutralization. Virology 270:1-3.
8. Cantin, R., J. F. Fortin, G. Lamontagne, and M. Tremblay. 1997. The presence of host-derived HLA-DR1 on human immunodeficiency virus type 1 increases viral infectivity. J. Virol. 71:1922-1930. (Pubitemid 27078570)
9. Chan, D. C., D. Fass, J. M. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-273.
10. Chen, B., E. M. Vogan, H. Gong, J. J. Skehel, D. C. Wiley, and S. C. Harrison. 2005. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433:834-841. (Pubitemid 40314887)
11. Chiu, W., and F. J. Rixon. 2002. High resolution structural studies of complex icosahedral viruses: a brief overview. Virus Res. 82:9-17. (Pubitemid 34273705)
12. Dimmock, N. J., and S. A. Hardy. 2004. Valency of antibody binding to virions and its determination by surface plasmon resonance. Rev. Med. Virol. 14:123-135.
13. Farzan, M., H. Choe, E. Desjardins, Y. Sun, J. Kuhn, J. Cao, D. Archambault, P. Kolchinsky, M. Koch, R. Wyatt, and J. Sodroski. 1998. Stabilization of human immunodeficiency virus type 1 envelope glycoprotein trimers by disulfide bonds introduced into the gp41 glycoprotein ectodomain. J. Virol. 72:7620-7625. (Pubitemid 28377899)
14. Fortin, J. F., R. Cantin, G. Lamontagne, and M. Tremblay. 1997. Host-derived ICAM-1 glycoproteins incorporated on human immunodeficiency virus type 1 are biologically active and enhance viral infectivity. J. Virol. 71:3588-3596.
15. Freed, E. O., and M. A. Martin. 1996. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol. 70:341-351.
16. Greenspan, N. S. 2001. Affinity, complementarity, cooperativity, and specificity in antibody recognition. Curr. Top. Microbiol. Immunol. 260:65-85.
17. Haynes, B. F., J. Fleming, E. W. St Clair, H. Katinger, G. Stiegler, R. Kunert, J. Robinson, R. M. Scearce, K. Plonk, H. F. Staats, T. L. Ortel, H. X. Liao, and S. M. Alam. 2005. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308:1906-1908.
18. Herrera, C., P. J. Klasse, C. W. Kibler, E. Michael, J. P. Moore, and S. Beddows. 2006. Dominant-negative effect of hetero-oligomerization on the function of the human immunodeficiency virus type 1 envelope glycoprotein complex. Virology 351:121-132. (Pubitemid 44037656)
19. Hewat, E. A., T. C. Marlovits, and D. Blaas. 1998. Structure of a neutralizing antibody bound monovalently to human rhinovirus 2. J. Virol. 72:4396-4402.
20. Hewat, E. A., N. Verdaguer, I. Fita, W. Blakemore, S. Brookes, A. King, J. Newman, E. Domingo, M. G. Mateu, and D. I. Stuart. 1997. Structure of the complex of an Fab fragment of a neutralizing antibody with foot-and-mouth disease virus: positioning of a highly mobile antigenic loop. EMBO J. 16:1492-1500.
21. Inouye, S., A. Hasegawa, S. Matsuno, and S. Katow. 1984. Changes in antibody avidity after virus infections: detection by an immunosorbent assay in which a mild protein-denaturing agent is employed. J. Clin. Microbiol. 20:525-529.
22. Klasse, P. J., and Q. J. Sattentau. 2001. Mechanisms of virus neutralization by antibody. Curr. Top. Microbiol. Immunol. 260:87-108.
23. Klasse, P. J., and Q. J. Sattentau. 2002. Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J. Gen. Virol. 83:2091-2108.
24. Kolchinsky, P., E. Kiprilov, and J. Sodroski. 2001. Increased neutralization sensitivity of CD4-independent human immunodeficiency virus variants. J. Virol. 75:2041-2050. (Pubitemid 32147543)
25. 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 8:1329-1339.
26. 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.
27. Kwong, P. D., R. Wyatt, Q. J. Sattentau, J. Sodroski, and W. A. Hendrickson. 2000. Oligomeric modeling and electrostatic analysis of the gp120 envelope glycoprotein of human immunodeficiency virus. J. Virol. 74:1961-1972.
28. Li, Y., H. Hui, C. J. Burgess, R. W. Price, P. M. Sharp, B. H. Hahn, and G. M. Shaw. 1992. Complete nucleotide sequence, genome organization, and biological properties of human immunodeficiency virus type 1 in vivo: evidence for limited defectiveness and complementation. J. Virol. 66:6587-6600.
29. Liu, F., S. Guttikonda, and M. R. Suresh. 2003. Bispecific monoclonal antibodies against a viral and an enzyme: utilities in ultrasensitive virus ELISA and phage display technology. J. Immunol. Methods 274:115-127. (Pubitemid 36263048)
30. Liu, J., A. Bartesaghi, M. J. Borgnia, G. Sapiro, and S. Subramaniam. 2008. Molecular architecture of native HIV-1 gp120 trimers. Nature 455:109-113.
31. + cells. J. Virol. 71:3341-3345.
32. 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. (Pubitemid 23309131)
33. Neurath, A. R., N. Strick, K. Lin, and S. Jiang. 1995. Multifaceted consequences of anti-gp41 monoclonal antibody 2F5 binding to HIV type 1 virions. AIDS Res. Hum. Retroviruses 11:687-696.
34. Ofek, G., M. Tang, A. Sambor, H. Katinger, J. R. Mascola, R. Wyatt, and P. D. Kwong. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737. (Pubitemid 39258398)
35. Ou, W., N. Lu, S. S. Yu, and J. Silver. 2006. Effect of epitope position on neutralization by anti-human immunodeficiency virus monoclonal antibody 2F5. J. Virol. 80:2539-2547. (Pubitemid 43271559)
36. Pullen, G. R., M. G. Fitzgerald, and C. S. Hosking. 1986. Antibody avidity determination by ELISA using thiocyanate elution. J. Immunol. Methods 86:83-87.
37. Ren, X., J. Sodroski, and X. Yang. 2005. An unrelated monoclonal antibody neutralizes human immunodeficiency virus type 1 by binding to an artificial epitope engineered in a functionally neutral region of the viral envelope glycoproteins. J. Virol. 79:5616-5624. (Pubitemid 40548230)
38. Rizzuto, C. D., and J. G. Sodroski. 1997. Contribution of virion ICAM-1 to human immunodeficiency virus infectivity and sensitivity to neutralization. J. Virol. 71:4847-4851. (Pubitemid 27204183)
39. Schlehuber, L. D., and J. K. Rose. 2004. Prediction and identification of a permissive epitope insertion site in the vesicular stomatitis virus glycoprotein. J. Virol. 78:5079-5087.
40. Schols, D., R. Pauwels, J. Desmyter, and E. De Clercq. 1992. Presence of class II histocompatibility DR proteins on the envelope of human immunodeficiency virus demonstrated by FACS analysis. Virology 189:374-376.
41. Schonning, K., O. Lund, O. S. Lund, and J. E. Hansen. 1999. Stoichiometry of monoclonal antibody neutralization of T-cell line-adapted human immunodeficiency virus type 1. J. Virol. 73:8364-8370. (Pubitemid 29441698)
42. Smith, T. J., N. H. Olson, R. H. Cheng, E. S. Chase, and T. S. Baker. 1993. Structure of a human rhinovirus-bivalently bound antibody complex: implications for viral neutralization and antibody flexibility. Proc. Natl. Acad. Sci. U. S. A. 90:7015-7018.
43. Smith, T. J., N. H. Olson, R. H. Cheng, H. Liu, E. S. Chase, W. M. Lee, D. M. Leippe, A. G. Mosser, R. R. Rueckert, and T. S. Baker. 1993. Structure of human rhinovirus complexed with Fab fragments from a neutralizing antibody. J. Virol. 67:1148-1158. (Pubitemid 23067616)
44. Starcich, B. R., B. H. Hahn, G. M. Shaw, P. D. McNeely, S. Modrow, H. Wolf, E. S. Parks, W. P. Parks, S. F. Josephs, R. C. Gallo, et al. 1986. Identification and characterization of conserved and variable regions in the envelope gene of HTLV-III/LAV, the retrovirus of AIDS. Cell 45:637-648.
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. Retroviruses 17:1757-1765.
46. Sullivan, N., Y. Sun, J. Binley, J. Lee, C. F. Barbas III, P. W. Parren, D. R. Burton, and J. Sodroski. 1998. Determinants of human immunodeficiency virus type 1 envelope glycoprotein activation by soluble CD4 and monoclonal antibodies. J. Virol. 72:6332-6338. (Pubitemid 28323943)
47. Tan, K., J. Liu, J. Wang, S. Shen, and M. Lu. 1997. Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. U. S. A. 94:12303-12308.
48. Thomas, D., W. W. Newcomb, J. C. Brown, J. S. Wall, J. F. Hainfeld, B. L. Trus, and A. C. Steven. 1985. Mass and molecular composition of vesicular stomatitis virus: a scanning transmission electron microscopy analysis. J. Virol. 54:598-607. (Pubitemid 15053149)
49. Tsai, P. K., C. J. Burke, J. W. Irwin, M. W. Bruner, J. S. Tung, G. F. Hollis, G. E. Mark, J. A. Kessler II, L. J. Boots, A. J. Conley, et al. 1995. Enhancing the avidity of a human recombinant anti-HIV-1 monoclonal antibody through oligomerization. J. Pharm. Sci. 84:866-870.
50. Verdaguer, N., G. Schoehn, W. F. Ochoa, I. Fita, S. Brookes, A. King, E. Domingo, M. G. Mateu, D. Stuart, and E. A. Hewat. 1999. Flexibility of the major antigenic loop of foot-and-mouth disease virus bound to a Fab fragment of a neutralising antibody: structure and neutralisation. Virology 255:260-268. (Pubitemid 29393337)
51. Wahlberg, J. M., W. A. Boere, and H. Garoff. 1989. The heterodimeric association between the membrane proteins of Semliki Forest virus changes its sensitivity to low pH during virus maturation. J. Virol. 63:4991-4997.
52. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387:426-430. (Pubitemid 27227210)
53. Wikoff, W. R., G. Wang, C. R. Parrish, R. H. Cheng, M. L. Strassheim, T. S. Baker, and M. G. Rossmann. 1994. The structure of a neutralized virus: canine parvovirus complexed with neutralizing antibody fragment. Structure 2:595-607. (Pubitemid 2110330)
54. Willey, R. L., R. A. Rutledge, S. Dias, T. Folks, T. Theodore, C. E. Buckler, and M. A. Martin. 1986. Identification of conserved and divergent domains within the envelope gene of the acquired immunodeficiency syndrome retrovirus. Proc. Natl. Acad. Sci. U. S. A. 83:5038-5042.
55. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888. (Pubitemid 28299385)
56. Wyma, D. J., A. Kotov, and C. Aiken. 2000. Evidence for a stable interaction of gp41 with Pr55(Gag) in immature human immunodeficiency virus type 1 particles. J. Virol. 74:9381-9387.
57. Yang, X., S. Kurteva, S. Lee, and J. Sodroski. 2005. Stoichiometry of antibody neutralization of human immunodeficiency virus type 1. J. Virol. 79:3500-3508. (Pubitemid 40327938)
58. Yang, X., S. Kurteva, X. Ren, S. Lee, and J. Sodroski. 2005. Stoichiometry of envelope glycoprotein trimers in the entry of human immunodeficiency virus type 1. J. Virol. 79:12132-12147. (Pubitemid 41348726)
59. Yang, X., S. Kurteva, X. Ren, S. Lee, and J. Sodroski. 2006. Subunit stoichiometry of human immunodeficiency virus type 1 envelope glycoprotein trimers during virus entry into host cells. J. Virol. 80:4388-4395.
60. Yang, X., I. Lipchina, S. Cocklin, I. Chaiken, and J. Sodroski. 2006. Antibody binding is a dominant determinant of the efficiency of human immunodeficiency virus type 1 neutralization. J. Virol. 80:11404-11408. (Pubitemid 44706582)
61. Yang, X., I. Lipchina, M. Lifton, L. Wang, and J. Sodroski. 2007. Antibody binding in proximity to the receptor/glycoprotein complex leads to a basal level of virus neutralization. J. Virol. 81:8809-8813. (Pubitemid 47242853)
62. Zanetti, G., J. A. Briggs, K. Grunewald, Q. J. Sattentau, and S. D. Fuller. 2006. Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLoS Pathog. 2:e83. (Pubitemid 44299887)
63. Zhou, T., L. Xu, B. Dey, A. J. Hessell, D. Van Ryk, S. H. Xiang, X. Yang, M. Y. Zhang, M. B. Zwick, J. Arthos, D. R. Burton, D. S. Dimitrov, J. Sodroski, R. Wyatt, G. J. Nabel, and P. D. Kwong. 2007. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445:732-737.
64. Zhu, P., E. Chertova, J. Bess, Jr., J. D. Lifson, L. O. Arthur, J. Liu, K. A. Taylor, and K. H. Roux. 2003. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. U. S. A. 100:15812-15817.
65. Zhu, P., J. Liu, J. Bess, Jr., E. Chertova, J. D. Lifson, H. Grise, G. A. Ofek, K. A. Taylor, and K. H. Roux. 2006. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441:847-852.
66. Zhu, P., H. Winkler, E. Chertova, K. A. Taylor, and K. H. Roux. 2008. Cryoelectron tomography of HIV-1 envelope spikes: further evidence for tripod-like legs. PLoS Pathog. 4:e1000203.
67. Zolla-Pazner, S. 1996. Mechanisms contributing to the neutralization of HIV-1. Immunol. Lett. 51:89-93.
68. Zwick, M. B., H. K. Komori, R. L. Stanfield, S. Church, M. Wang, P. W. Parren, R. Kunert, H. Katinger, I. A. Wilson, and D. R. Burton. 2004. The long third complementarity-determining region of the heavy chain is important in the activity of the broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2F5. J. Virol. 78:3155-3161.