Mechanisms of human immunodeficiency virus type 1 (HIV-1) neutralization: Irreversible inactivation of infectivity by anti-HIV-1 antibody

Journal of Virology

Volumn 70, Issue 8, 1996, Pages 5236-5245

  Mcdougal, J Steven ^a,b   Kennedy, M Susan ^b   Orloff, Sherry L ^b   Nicholson, Janet K A ^b   Spira, Thomas J ^b  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G ANTIBODY; MAGNESIUM ION; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY;

ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; SERUM; VIRION; VIRUS INACTIVATION; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION;

EID: 0029900653     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.8.5236-5245.1996     Document Type: Article

References (69)

1. Albert, J., B. Abrahamsson, K. Nagy, E. Aurelius, H. Gaines, G. Nystrom, and E. M. Fenyo. 1990. Rapid development of isolate-specific neutralizing antibodies after primary HIV-1 infection and consequent emergence of virus variants which resist neutralization by autologous sera. AIDS 4:107-112.
2. Arendrup, M., C. Nielsen, J. E. S. Hansen, C. Pedersen, L. Mathiesen, and J. O. Nielsen. 1992. Autologous HIV-1 neutralizing antibodies: emergence of neutralization-resistant escape virus and subsequent development of escape virus neutralizing antibodies. J. Acquired Immune Defic. Syndr. 5:303-307.
3. Barbas, C. F., III, E. Bjorling, F. Chiodi, N. Dunlop, D. Cababa, T. M. Jones, S. L. Zebedee, M. A. A. Persson, P. L. Nara, E. Norrby, and D. R. Burton. 1992. Recombinant human Fab fragments neutralize human type 1 immunodeficiency virus in vitro. Proc. Natl. Acad. Sci. USA 89:9339-9343.
4. Brioen, P., B. Rombaut, and A. Boeye. 1985. Hit-and-run neutralization of poliovirus. J. Gen. Virol. 66:2495-2499.
5. Cavacini, L. A, C. L. Emes, J. Power, M. Duval, and M. Posner. 1994. Effect of antibody valency on interaction with cell-surface expressed HIV-1 and viral neutralization. J. Immunol. 152:2538-2545.
6. Cheng-Mayer, C., M. Quiroga, J. W. Tung, D. Dina, and J. A. Levy. 1990. Viral determinants of human immunodeficiency virus type 1 T-cell or macrophage tropism, cytopathogenicity, and CD4 antigen modulation. J. Virol. 64:4390-4398.
7. Daar, E. S., X. L. Li, T. Moudgil, and D. D. Ho. 1990. High concentrations of recombinant soluble CD4 are required to neutralize primary human immunodeficiency virus type 1 isolates. Proc. Natl. Acad. Sci. USA 87:6574-6578.
8. Delwart, E. L., E. G. Shpaer, J. Louwagie, F. E. McCutchan, M. Grez, H. Rubsamen-Waigmann, and J. I. Mullins. 1993. Genetic relationships determined by a DNA heteroduplex mobility assay: analysis of HIV-1 env genes. Science 262:1257-1261.
9. Denisova, G., J. Zwickel, and J. M. Gershoni. 1995. Binding of HIV-1 gp120 to an anti-V3 loop antibody reveals novel antigen-induced epitopes. FASEB J. 9:127-132.
10. di Marzo Veronese, F., M. S. Reitz, G. Gupta, M. Robert-Guroff, C. Boyer-Thompson, A. Louie, R. C. Gallo, and P. Lusso. 1993. Loss of a neutralizing epitope by a spontaneous point mutation in the V3 loop of HIV-1 isolated from an infected laboratory worker. J. Biol. Chem. 268:25894-25901.
11. Dimmock, N. J. 1987. Multiple mechanisms of neutralization of animal viruses. Trends Biochem. Sci. 12:70-75.
12. D'Souza, M. P., G. Milman, J. A. Bradac, D. McPhee, C. V. Hanson, R. M. Hendry, and Collaborating Investigators. 1995. Neutralization of primary HIV-1 isolates by anti-envelope monoclonal antibodies. AIDS 9:867-874.
13. Durda, P. J., B. Leece, A. Jenoski, H. Rabin, A. Fisher, and F. Wong-Staal. 1988. Characterization of murine monoclonal antibodies to HIV-1 induced by synthetic peptides. AIDS Res. Hum. Retroviruses 4:331-342.
14. Emini, E. A., P. L. Nara, W. A. Schleif, J. A. Lewis, J. P. Davide, D. R. Lee, J. Kessler, S. Conley, S. Matsushita, S. D. Putney, R. J. Gerety, and J. W. Eichberg. 1990. Antibody-mediated in vitro neutralization of human immunodeficiency virus type 1 abolishes infectivity for chimpanzees. J. Virol. 64:3674-3678.
15. Emini, E. A., W. A. Schleif, J. H. Nunberg, A. J. Conley, Y. Eda, S. Tokiyoshi, S. D. Putney, S. Matsushita, K. E. Cobb, C. M. Jett, J. W. Eichberg, and K. K. Murthy. 1992. Prevention of HIV-1 infection in chimpanzees by gp120 V3 domain-specific monoclonal antibody. Nature (London) 355:728-730.
16. Fahey, J. L., and E. W. Terry. 1978. Ion exchange chromatography and gel filtration, p. 8.1-8.16. In D. M. Weir (ed.). Handbook of experimental immunology, volume 1. Immunochemistry. Blackwell, Oxford.
17. Franklin, E. C. 1960. Structural units of human 7S gamma globulin. J. Clin. Invest. 39:1933-1941.
18. Gollins, S. W., and J. S. Porterfield. 1986. A new mechanism for the neutralization of enveloped viruses by antiviral antibody. Nature (London) 321: 244-249.
19. Gomatos, P. J., N. M. Stamatos, H. E. Gendelman, A. Fowler, D. L Hoover, C. Kalter, D. S. Burke, E. C. Tramont, and M. S. Meltzer. 1990. Relative inefficiency of soluble recombinant CD4 for inhibition of infection by monocyte-tropic HIV in monocytes and T cells. J. Immunol. 144:4183-4188.
20. Ho, D. D., J. A. McKeating, X. L. Li, T. Moudgil, E. S. Daar, N.-C. Sun, and J. E. Robinson. 1991. Conformational epitope on gp120 important in CD4 binding and human immunodeficiency virus type 1 neutralization identified by a human monoclonal antibody. J. Virol. 65:489-493.
21. Ho, D. D., A. U. Neumann, A. S. Perelson, W. Chen, J. M. Leonard, and M. Markowitz. 1995. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature (London) 373:123-126.
22. Kida, H., S. Yoden, M. Kuwabara, and R. Yanagawa. 1985. Interference with a conformational change in the haemagglutinin molecule of infiuencza virus by antibodies as a possible neutralization mechanism. Vaccine 3:219-222.
23. Kinney-Thomas, E., J. N. Weber, J. McClure, P. R Clapham, M. C. Singhal, M. K. Shriver, and R. A. Weiss. 1988. Neutralizing monoclonal antibodies to the AIDS virus. AIDS 2:25-29.
24. Kozal, M. J., R. W. Shafer, M. A. Winters, D. A. Katzenstein, and T. C. Merigan. 1993. A mutation in human immunodeficiency virus reverse transcriptase and decline in CD4 lymphocyte numbers in long-term zidovudine recipients. J. Infect. Dis. 167:526-532.
25. Layne, S. P., M. J. Merges, M. Dembo, J. L. Spouge, and P. L. Nara. 1990. HJV requires multiple gp120 molecules for CD4-mediated infection. Nature (London) 346:277-279.
26. Levy, J. A. 1993. Pathogenesis of human immunodeficiency virus infection. Microbiol. Rev. 57:183-289.
27. Mascola, J. R., and D. S. Burke. 1993. Antigen detection in neutralization assays: high levels of interfering anti-p24 antibodies in some plasma. AIDS Res. Hum. Retroviruses 9:1173-1174.
28. Matsushita, S., M. Robert-Guroff, J. Rusche, A. Koito, T. Hattori, H. Hoshino, K. Javaherian, K. Takatsuki, and S. Putney. 1988. Characterization of a human immunodeficiency virus neutralizing monoclonal antibody and mapping of the neutralizing epitope. J. Virol. 62:2107-2114.
29. Matthews, T. J. 1994. Dilemma of neutralization resistance of human immunodeficiency virus type 1 field isolates and vaccine development. J. Virol. 10:631-632.
30. McDougal, J. S., S. P. Cort, M. S. Kennedy, C. D. Cabridilla, P. M. Feorino, D. P. Francis, D. Hicks, V. S. Kalyanaraman, and L. S. Martin. 1985. Immunoassay for the detection and quantitation of infectious human retrovirus, lymphadenopathy-associated virus (LAV). J. Immunol. Methods 76:171-183.
31. McDougal, J. S., M. S. Kennedy, J. K. A. Nicholson, T. J. Spira, H. W. Jaffe, J. E. Kaplan, D. B. Fishbein, P. O'Malley, C. Aloisio, C. M. Black, M. Hubbard, and C. B. Reimer. 1987. Antibody response to human immunodeficiency virus in homosexual men. Relation of antibody specificity, titer, and isotype to clinical status, severity of immunodeficiency and disease progression. J. Clin. Invest. 80:316-324.
32. MeDougal, J. S., A. Mawle, S. P. Cort, J. K. A. Nicholson, G. D. Cross, J. A. Scheppler-Campbell, D. Hicks, and J. Sligh. 1985. Cellular tropism of the human retrovirus HTLV-III/LAV. Role of T cell activation and expression of the T4 antigen. J. Immunol. 135:3151-3162.
33. McKeating, J. A., A. McNight, and J. P. Moore. 1991. Differential loss of envelope glycoprotein gp120 from virions of human immunodeficiency virus type 1 isolates: effects on infectivity and neutralization. J. Virol. 65:852-860.
34. Meyerhans, A., R Cheynier, J. Albert, M. Seth, S. Kwok, J. Sninsky, L. Morfeldt-Manson, B. Asjo, and S. Wain-Hobson. 1989. Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell 58:901-910.
35. Montefiori, D. C., J. Zhou, B. Barnes, D. Lake, E. M. Hersh, Y. Masuho, and L. B. Lefkowitz, Jr. 1991. Homotypic antibody responses to fresh clinical isolates of human immunodeficiency virus. Virology 182:635-643.
36. 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.
37. Moore, J. P., Y. Cao, L. Qing, Q. J. Sattentau, J. Pyati, R. Koduri, J. Robinson, C. F. Barbas, D. Burton, and D. D. Ho. 1995. Primary isolates of human immunodeficiency virus type 1 are relatively resistant to neutralization by monoclonal antibodies to gp120, and their neutralization is not predicted by studies with monomeric gp120. J. Virol. 69:101-109.
38. Moore, J. P., and D. D. Ho. 1993. Antibodies to discontinuous or conformationally sensitive epitopes on the gp120 glycoprotein of human immunodeficiency virus type 1 are highly prevalent in sera of infected humans. J. Virol. 67:863-875.
39. Moore, J. P., J. A. McKeating, W. A. Norton, and Q. J. Sattentau. 1991. Direct measurement of soluble CD4 binding to human immunodeficiency virus type 1 virions: gp120 dissociation and its implications for virus-cell binding and fusion reactions and their neutralization by soluble CD4. J. Virol. 65:1133-1140.
40. Moore, J. P., J. A. McKeating, R. A. Weiss, and Q. J. Sattentau. 1990. Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science 250:1139-1142.
41. Moore, J. P., Q. J. Sattentau, R. Wyatt, and J. Sodroski. 1994. Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies. J. Virol. 68:469-484.
42. Nara, P. L., R. R. Garrity, and J. Goudsmit. 1991. Neutralization of HIV-1: a paradox of humoral proportions. FASEB J. 5:2437-2455.
43. Nicholson, J. K. A., T. J. Spira, C. H. Aloisio, B. M. Jones, M. S. Kennedy, R. C. Holman, and J. S. McDougal. 1989. Serial determinations of HIV-1 titers in HIV-infected homosexual men: association of rising titers with CD4 T cell depletion and progression to AIDS. AIDS Res. Hum. Retroviruses 5:205-215.
44. Nisinoff, A. 1962. Conceptual advances in immunology and oncology, p. 1-373. Hoeber & Harper, New York.
45. O'Brien, W. A., S.-H. Mao, Y. Cao, and J. P. Moore. 1994. Macrophagetropic and T-cell line-adapted chimeric strains of human immunodeficiency virus type 1 differ in their susceptibilities to neutralization by soluble CD4 at different temperatures, J. Virol. 68:5264-5269.
46. Orloff, G. M., S. L. Orloff, M. S. Kennedy, P. J. Maddon, and J. S. McDougal. 1991. Penetration of CD4 T cells by HIV-1. The CD4 receptor does not internalize with HIV, and CD4-related signal transduction events are not required for entry. J. Immunol. 146:2578-2587.
47. Orloff, S. L., M. S. Kennedy, A. A. Belperron, P.J. Maddon, and J. S. McDougal. 1993. Two mechanisms of soluble CD4 (sCD4)-mediated inhibition of human immunodeficiency virus type 1 (HIV-1) infectivity and their relation to primary HIV-1 isolates with reduced sensitivity to sCD4. J. Virol. 67:1461-1471.
48. Page, K. A., S. M. Stearns, and D. R. Littman. 1992. Analysis of mutations in the V3 domain of gp160 that affect fusion and infectivity. J. Virol. 66:524-533.
49. Pinter, A., W. J. Honnen, S. A. Tilley, C. Bona, H. Zaghouani, M. K. Gorny, and S. Zolla-Pazner. 1989. Oligomeric structure of gp41, the transmembrane protein of human immunodeficiency virus type 1. J. Virol. 63:2674-2679.
50. Posner, M. R., T. Hideshima, T. Cannon, M. Mukherjee, K. H. Mayer. and R. A. Byrn. 1991. An IgG human monoclonal antibody that reacts with HIV-1/gp120, inhibits virus binding to cells, and neutralizes infection. J. Immunol. 146:4325-4332.
51. Prince, A. M., H. Reesink, D. Pascual, B. Horowitz, I. Hewlett, K. K. Murthy, K. E. Cobb, and J. W. Eichberg. 1991. Prevention of HIV infection by passive immunization with HIV immunoglobulin. AIDS Res. Hum. Retroviruses 7:971-973.
52. Putney, S. D., T. J. Matthews, W. G. Robey, D. L. Lynn, M. Robert-Guroff, W. T. Mueller, A. J. Langlois, J. Ghrayeb, S. R. Petteway, Jr., K. J. Weinhold, P. J. Fischinger, F. Wong-Staal, R. C. Galllo, and D. P. Bolognesi. 1986. HTLV-III/LAV-neutralizing antibodies to an E, coli-produced fragment of the virus envelope. Science 234:1392-1395.
53. Roben, P., J. P. Moore, M. Thali, J. Sodroski, C. F. Barbas, 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.
54. Rusche, J. R., K. Javaherian, C. McDanal, J. Petro, D. L. Lynn, R. Grimaila, A. Langlois, R. C. Gallo, L. O. Arthur, P. J. Fischinger, D. P. Bolognesi, S. D. Putney, and T. J. Matthews. 1988. Antibodies that inhibit fusion of human immunodeficiency virus-infected cells bind a 24-amino acid sequence of the viral envelope. Proc. Natl. Acad. Sci. USA 85:3198-3202.
55. Sabino, E., L.-Z, Pan, C. Cheng-Mayer, and A. Mayer. 1994. Comparison of in vivo plasma and peripheral blood mononuclear cell HIV-1 quasispecies to short-term tissue culture isolates: an analysis of tat and C2-V3 env regions. AIDS 8:901-909.
56. Sattentau, Q. J., and J. P. Moore. 1991. Conformational changes induced in the human immunodeficiency virus envelope glycoprotein by soluble CD4 binding. J. Exp. Med. 174:407-415.
57. Sattentau, Q. J., and J. P. Moore. 1995. Human immunodeficiency virus type 1 neutralization is determined by epitope exposure on the gp120 oligomer. J. Exp. Med. 182:185-196.
58. Seiller-Moiseiwitsch, F., B. H. Margolin, and R. Swanstrom. 1994. Genetic variability of the human immunodeficiency virus: statistical and biological issues. Annu. Rev. Genet. 28:559-596.
59. Simmonds, P., L. Q. Zhang, F. J. F. McOmish, P. Balfe, C. A. Ludlam, and A. J. Brown. 1991. Discontinuous sequence change of human immunodeficiency virus (HIV) type 1 env sequences in plasma viral and lymphocyteassociated proviral populations in vivo: implications for models of HIV pathogenesis. J. Virol. 65:6266-6276.
60. Skinner, M. A., A. J. Langlois, C. B. McDanal, J. S. McDougal, D. J. Bolognesi, and T. J. Matthews. 1988. Neutralizing antibodies to an immunodominant envelope sequence do not prevent gp120 binding to CD4. J. Virol. 62:4195-4200.
61. Spear, G. T., B. L. Sullivan, A. L. Landay, and T. F. Lint. 1990. Neutralization of human immunodeficiency virus type 1 by complement occurs by viral lysis. J. Virol. 64:5869-5873.
62. Tremblay, M., and M. A. Wainberg. 1990. Neutralization of multiple HIV-1 isolates from a single subject by autologous sequential sera. J. Infect. Dis. 162:735-737.
63. VanCott, T. C., F. R. Bethke, V. R. Polonis, M. K. Gorny, S. Zolla-Pazner, R. R. Redfield, and D. L. Birx. 1994. Dissociation rate of antibody-gp120 binding interactions is predictive of V3-mediated neutralization of HIV-1. J. Immunol. 153:449-459.
64. Wei, X., S. K. Ghosh, M. E. Taylor, V. A. Johnson, E. A. Emini, P. Deutsch, J. D. Lifson, S. Bonhoeffer, M. A. Nowak, B. H. Hahn, M. S. Saag, and G. M. Shaw. 1995. Viral dynamics in human immunodeficiency virus type 1 infection. Nature (London) 373:117-122.
65. WHO Global Programme on AIDS. 1990. Report of a WHO workshop on the measurement and significance of neutralizing antibody to HIV and SIV. AIDS 4:269-275.
66. Wolfs, T. F. W., J.-J. De Jong, H. van den Berg, J. M. G. H. Tijnagel, W. J. A. Krone, and J. Goudsmit. 1990. Evolution of sequences encoding the principal neutralization epitope of human immunodeficiency virus 1 is host dependent, rapid, and continuous. Proc. Natl. Acad. Sci. USA 87:9938-9942.
67. Wrin, T., T. P. Loh, J. Charron Vennari, H. Schuitemaker, and J. H. Nunberg. 1995. Adaptation to persistent growth in the H9 cell line renders a primary isolate of human immunodeficiency virus type 1 sensitive to neutralization by vaccine sera. J. Virol. 69:39-48.
68. Wyatt, R., M. Thali, S. Tilley, A. Pinter, M. Posner, D. Ho, J. Robinson, and J. Sodroski. 1992. Relationship of the human immunodeficiency virus type 1 gp120 third variable loop to a component of the CD4 binding site in the fourth conserved region. J. Virol. 66:6997-7004.
69. Zhou, Y.-J., J. W. Burns, Y. Morita, T. Tanaka, and M. K. Estes. 1994. Localization of rotavirus VP4 neutralization epitopes involved in antibody-induecd conformational changes of virus structure. J. Virol. 68:3955-3964.