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

Journal of Virology

Volumn 71, Issue 4, 1997, Pages 2779-2785

  Fouts, Timothy R ^a   Binley, James M ^a   Trkola, Alexandra ^a   Robinson, James E ^b   Moore, John P ^a,c  

^a ROCKEFELLER UNIVERSITY   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AARON DIAMOND AIDS RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 120; MONOCLONAL ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CHO CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; KIDNEY CELL; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; VIRUS NEUTRALIZATION;

EID: 0030897825     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.4.2779-2785.1997     Document Type: Article

References (77)

1. Alkhatib, G., C. Combadiere, C. C. Broder, Y. Feng, P. E. Kennedy, P. M. Murphy, and E. A. Berger. 1996. CC CKR5: a RANTES, MIP-1α, MIP-1β receptor is a fusion cofactor for macrophage-tropic HIV-1. Science 272: 1955-1958.
2. Allaway, G. P., K. L. Davis-Bruno, G. A. Beaudry, E. B. Garcia, E. L. Wong, A. M. Ryder, K. W. Hasel, M.-C. Gauduin, R. A. Koup, J. S. McDougal, and P. J. Maddon. 1995. Expression and characterization of CD4IgG2, a novel heterotetramer which neutralizes primary HIV-1 isolates. AIDS Res. Hum. Retroviruses 11:513-540.
3. Baldinotti, F., D. Matteucci, P. Mazzetti, C. Giannelli, P. Bandecchi, F. Tozzini, and M. Bendinelli. 1994. Serum neutralization of feline immunodeficiency virus is markedly dependent on passage history of the virus and host system. J. Virol. 68:4572-4579.
4. Binley, J. M., T. Fouts, J. Sodroski, and J. P. Moore. Unpublished results.
5. Bou-Habib, K. C., G. Roderiquez, T. Oravecz, P. W. Berman, P. Lusso, and M. A. Norcross. 1994. Cryptic nature of envelope V3 region epitopes protects primary monocytotropic human immunodeficiency virus type 1 from antibody neutralization. J. Virol. 68:6006-6013.
6. Brighty, D. W., M. Rosenberg, I. S. Y. Chen, and M. Ivey-Hoyle. 1991. Envelope proteins from clinical isolates of human immunodeficiency virus type 1 that are refractory to neutralization by soluble CD4 possess high affinity for CD4 receptor. Proc. Natl. Acad. Sci. USA 88:7802-7805.
7. Burton, D. R., J. Pyati, R. Koduri, S. J. Sharp, G. B. Thornton, P. W. H. I. Parren, L. S. W. Sawyer, R. M. Hendry, N. Dunlop, P. L. Nara, M. Lamacchia, E. Garratty, E. R. Stiehm, Y. J. Bryson, Y. Cao, J. P. Moore, D. D. Ho, and C. F. Barbas III. 1994. Efficient neutralization of primary isolates of HIV-1 by recombinant human monoclonal antibody. Science 266:1024-1027.
8. Cammarota, G., D. Matteucci, M. Kistello, E. Nicoletti, S. Giannecehini, and M. Bendinelli. 1988. Reduced sensitivity to strain-specific neutralization of laboratory-adapted feline immunodeficiency virus after one passage in vivo: association with amino acid substitutions in the V4 region of the surface glycoprotein. AIDS Res. Hum. Retroviruses 4:331-342.
9. Choc, H., M. Farzan, Y. Sun, N. Sullivan, B. Rollins, P. D. Ponath, L. Wu, C. R. Mackay, G. LaRosa, W. Newman, N. Gerard, C. Gerard, and J. Sodroski. 1996. The β-chemokine receptors CCR3 and CCR5 facilitate infection by primary isolates. Cell 85:1135-1148.
10. Connor, R. I., B. K. Chen, S. Choe, and N. R. Landau. 1995. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206:935-944.
11. Cook, R. F., S. L. Berger, K. E. Rushlow, J. M. McManus, S. J. Cook, S. Harrold, M. L. Raabe, R. C. Montelaro, and C. J. Issel. 1995. Enhanced sensitivity to neutralizing antibodies in a variant of equine infectious anemia virus is linked to amino acid substitutions in the surface unit envelope glycoprotein. J. Virol. 69:1493-1499.
12. 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.
13. Deng, H.-K., R. Lui, W. Ellmeier, S. Choe, D. Unutmaz, M. Burkhart, P. Di Marzio, S. Marmon, R. E. Sutton, C. M. Hill, C. B. Davis, S. C. Peiper, T. J. Schall, D. R. Littman, and N. R. Landau. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661-666.
14. Doranz, B. J., J. Rucker, Y. Yi, R. J. Smyth, M. Samson, S. C. Peiper, M. Parmentier, R. G. Collman, and R. W. Doms. 1996. A dual-tropic primary HIV-1 isolate that uses fusin and the β-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85:1149-1158.
15. Dragic, T., V. Litwin, G. P. Allaway, S. R. Martin, Y. Huang, K. A. Nagashima, C. Cayanan, P. J. Maddon, R. A. Koup, J. P. Moore, and W. A. Paxton. 1996. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667-673.
16. Fujita, K., P. Silver, and K. Peden. 1992. Changes in both gp120 and gp41 can account for increased growth potential and expanded host range of human immunodeficiency virus type 1. J. Virol. 66:4445-4451.
17. Gorny, M. K., A. J. Conley, S. Karwowska, A. Buchbinder, J.-Y. Xu, E. A. Emini, S. Koenig, and S. Zolla-Pazner. 1992. Neutralization of diverse human immunodeficiency virus type 1 variants by an anti-V3 human monoclonal antibody. J. Virol. 66:7538-7542.
18. Gorny, M. K., J. P. Moore, A. J. Conley, S. Karwowska, J. Sodroski, C. Williams, S. Burda, L. J. Boots, and S. Zolla-Pazner. 1994. Human anti-V2 monoclonal antibody that neutralizes primary but not laboratory isolates of human immunodeficiency virus type 1. J. Virol. 68:8312-8320.
19. Gorny, M. K., J.-Y. Xu, V. Gianakakos, S. Karwowska, C. Williams, H. W. Sheppard, C. V. Hanson, and S. Zolla-Pazner. 1991. Production of site-selected neutralizing human monoclonal antibodies against the third variable domain of the human immunodeficiency type 1 envelope glycoprotein. Proc. Natl. Acad. Sci. USA 88:3238-3242.
20. Graham, B. S., and P. Wright. 1996. Candidate AIDS vaccines. N. Engl. J. Med. 333:1331-1339.
21. Grunow. R., S. Jahn, T. Porstmann, S. S. Kiessig, H. Steinkellner, F. Steindl, D. Mattanovich, L. Gutter, F. Deinhardt, H. Katinger, and R. von Baehr. 1988. The high-efficiency, human B-cell line immortalizing heteromyeloma CD-F7. Production of human monoclonal antibodies to human immunodeficiency virus. J. Immunol. Methods 106:257-265.
22. Haigwood, N. L., P. L. Nara, E. Brooks, G. A. van Nest, G. Ott, K. W. Higgins, N. Dunlop, C. J. Scandella, J. W. Eichberg, and K. S. Steimer. 1992. Native but not denatured recombinant human immunodeficiency virus type 1 gp120 generates broad-spectrum neutralizing antibodies in baboons. J. Virol. 66:172-182.
23. Haynes, B. F., G. Pantaleo, and A. S. Fauci. 1996. Toward an understanding of the correlates of protective immunity to HIV infection. Science 271:324-328.
24. Ho, P. D., M. S. Fung, Y. Z. Cao, X. L. Li, C. Sun, T. W. Chang, and N. C. Sun. 1991. Another discontinuous epitope on glycoprotein gp120 that is important in human immunodeficiency virus type 1 neutralization is identified by a monoclonal antibody. Proc. Natl. Acad. Sci. USA 88:8949-8952.
25. 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 that is important in human immunodeficiency virus type 1 neutralization is identified by a monoclonal antibody. Proc. Natl. Acad. Sci. USA 65:489-493.
26. Javaherian, K., A. J. Langlois, C. McDanal, K. L. Ross, L. I. Eckler, C. L. Jellis, A. T. Profy, J. R. Rusche, D. P. Bolognesi, S. D. Putney, and T. J. Matthews. 1989. Principal neutralizing domain of the human immunodeficiency virus type 1 envelope protein. Proc. Natl. Acad. Sci. USA 86:6768-6772.
27. Kang, C.-Y., P. Nara, S. Chamat, V. Caralli, T. Ryskamp, N. Haigwood, R. Newman, and H. Kohler. 1991. Evidence for non-V3-specific neutralizing antibodies that interfere with gp120/CD4 binding in human immunodeficiency virus 1-infected humans. Proc. Natl. Acad. Sci. USA 88:6171-6175.
28. Karlsson, G. B., F. Gao, J. Robinson, B. Hahn, and J. Sodroski. 1996. Increased envelope spike density and stability are not required for the neutralization resistance of primary human immunodeficiency viruses. J. Virol. 70:6136-6142.
29. Kent, K. A., and J. Robinson. 1996. Antigenic determinants on HIV-1 envelope glycoproteins: a Dickens of a time with an Oligomer Twist. AIDS 10(Suppl. A):S107-S114.
30. Klasse, P. J., and J. P. Moore. 1996. Quantitative model of antibody-and soluble CD4-mediated neutralization of primary isolates and T-cell line-adapted strains of human immunodeficiency virus type 1. J. Virol. 70:3668-3677.
31. Kliks, S. C., T. Shioda, N. L. Haigwood, and J. A. Levy. 1993. V3 variability can influence the ability of an antibody to neutralize or enhance infection by diverse strains of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 90:11518-11522.
32. Koyanagi, Y., S. Miles, R. T. Mitsuyasu, J. E. Merrill, H. V. Vinters, and I. S. Y. Chen. 1989. Dual infection of the central nervous system by AIDS viruses with distinct cellular tropism. Science 236:819-822.
33. Lu, M., S. C. Blacklow, and P. S. Kim. 1995. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat. Struct. Biol. 2:1075-1082.
34. McDougal, J. S., M. S. Kennedy, S. L. Orloff, J. K. A. Nicholson, and T. J. Spira. 1996. Mechanisms of human immunodeficiency virus type 1 (HIV-1) neutralization: irreversible inactivation of infectivity by anti-HIV-1 antibody. J. Virol. 70:5236-5245.
35. McKeating, J. A., Y.-J. Zhang, C. Arnold, R. Frederiksson, E.-M. Fenyo, and P. Balfe. 1996. Chimeric viruses expressing primary envelope glycoproteins of human immunodeficiency virus type 1 show increased sensitivity to neutralization by human sera. Virology 220:450-460.
36. Moore, J. P. 1995. Back to primary school. Nature 376:115.
37. Moore, J. P. 1990. Simple methods for monitoring HIV-1 and HIV-2 gp120 binding to soluble CD4 by enzyme-linked immunosorbent assay: HIV-2 has a 25-fold lower affinity than HV-1 for soluble CD4. AIDS 4:297-305.
38. Moore, J. P., L. C. Burkly, R. I. Connor, Y. Cao, R. Tizard, D. D. Ho, and R. A. Fisher. 1993. Adaptation of two primary human immunodeficiency virus type 1 isolates to growth in transformed T-cell lines correlates with alterations in the responses of their envelope glycoproteins to soluble CD4. AIDS Res. Hum. Retroviruses 9:539-539.
39. Moore, J. P., Y. Cao, L. Qing, Q. J. Sattentau, J. Pyati, R. Koduri, J. Robinson, C. F. Barbas III, D. R. 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.
40. 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.
41. Moore, J. P., and D. D. Ho. 1995. HIV-1 neutralization: the consequences of viral adaptation to growth on transformed T cells. AIDS 9(Suppl. A):S117-S136.
42. Moore, J. P., J. A. McKeating, Y. Huang, A. Ashkenazi, and D. D. Ho. 1992. Virions of primary human immunodeficiency virus type 1 isolates resistant to soluble CD4 (sCD4) neutralization differ in sCD4 binding and glycoprotein gp120 retention from sCD4-sensitive isolates. J. Virol. 66:235-243.
43. Moore, J. P., J. A. McKeating, I. M. Jones, P. E. Stephens, G. Clements, S. Thomson, and R. A. Weiss. 1990. Characterization of recombinant gp120 and gp160 from HIV-1: binding to monoclonal antibodies and soluble CD4. AIDS 4:307-315.
44. 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.
45. Moore, J. P., Q. J. Sattentau, H. Yoshiyama, M. Thali, M. Charles, N. Sullivan, S.-W. Poon, M. S. Fung, F. Traincard, M. Pinkus, G. Robey, J. E. Robinson, D. D. Ho, and J. Sodroski. 1993. Probing the structure of the V2 domain of human immunodeficiency virus type 1 surface glycoprotein gp120 with a panel of eight monoclonal antibodies: human immune response to the V1 and V2 domains. J. Virol. 67:6136-6151.
46. Moore, J. P., and J. Sodroski. 1996. A model of the human immunodeficiency virus type 1 gp120 exterior envelope glycoprotein surface derived from antibody cross-competition analysis. J. Virol. 70:1863-1872.
47. Moore, J. P., A. Trkola, B. Korber, L. J. Boots, J. A. Kessler II, F. E. McCutchan, J. Mascola, D. D. Ho, J. Robinson, and A. J. Conley. 1995. A human monoclonal antibody to a complex epitope in the V3 region of gp120 of human immunodeficiency virus type 1 has broad reactivity within and outside clade B. J. Virol. 69:122-130.
48. O'Brien, W. A., Y. Koyanagi, A. Namazie, J. Q. Zhao, A. Diagne, K. Idler, J. A. Zack, and I. S. Y. Chen. 1990. HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature 348:69-73.
49. O'Brien, W. A., S.-H. Mao, Y. Cao, and J. P. Moore. 1994. Macrophage-tropic 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.
50. Orloff, S. L., C. I. Bandea, M. S. Kennedy, G. P. Allaway, P. J. Maddon, and J. S. McDougal. 1995. Increase in sensitivity to soluble CD4 by primary HIV type 1 isolates after passage through C8166 cells: association with sequence changes in the first constant region of glycoprotein 120. AIDS Res. Hum. Retroviruses 11:335-342.
51. Poignard, P., T. Fouts, D. Naniche, J. P. Moore, and Q. J. Sattentau. 1996. Neutralizing antibodies to human immunodeficiency virus type 1 gp120 induce envelope glycoprotein subunit dissociation. J. Exp. Med. 183:473-484.
52. Rich, E. A., I. S. Y. Chen, J. A. Zack, M. L. Lenard, and W. O'Brien. 1991. Increased susceptibility of differentiated mononuclear phagocytes to productive infection with HIV-1. J. Clin. Invest. 89:123-132.
53. 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.
54. Sattentau, Q. J. Personal communication.
55. 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.
56. Sawyer, L. S. W., M. T. Wrin, L. Crawford-Miksza, B. Potts, Y. Wu, P. A. Weber, R. D. Alfonso, and C. V. Hanson. 1994. Neutralization sensitivity of human immunodeficiency virus type 1 is determined in part by the cell in which the virus is propagated. J. Virol. 67:1342-1349.
57. Schutten, M., A. C. Andeweg, M. L. Bosch, and A. D. M. E. Osterhaus. 1995. Enhancement of infectivity of a non-syncytium inducing HIV-1 by sCD4 and human antibodies that neutralize syncytium inducing HIV-1. Scand. J. Immunol. 41:18-22.
58. Scott, C. F., Jr., S. Silver, A. T. Profy, S. D. Putney, S. Langlois, K. Weinhold, and J. E. Robinson. 1990. Human monoclonal antibody that recognizes the V3 region of human immunodeficiency virus gp120 and neutralizes the human T-lymphotropic virus type IIIMN strain. Proc. Natl. Acad. Sci. USA 87:8597-8601.
59. Stamatatos, L., and C. Cheng-Mayer. 1995. Structural modulations of the envelope gp120 glycoprotein of HIV-1 upon oligomerization and differential V3 loop-epitope exposure of isolates displaying distinct tropism upon virion-soluble receptor binding. J. Virol. 69:6191-6198.
60. Steimer, K. S., C. J. Scandella, P. V. Skiles, and N. L. Haigwood. 1991. Neutralization of divergent HIV-1 isolates by conformation-dependent human antibodies to gp!20. Science 254:105-108.
61. Sullivan, N., Y. Sun, J. Li, W. Hofmann, and J. Sodroski. 1995. Replicative function and neutralization sensitivity of envelope glycoprotein from primary and T-cell line-passaged human immunodeficiency virus type isolates. J. Virol. 69:4413-4422.
62. Thali, M., C. Furman, D. D. Ho, J. Robinson, S. Tilley, A. Pinter, and J. Sodroski. 1992. Discontinuous, conserved neutralization epitopes overlapping the CD4-binding region of human immunodeficiency virus type 1 gp120 envelope glycoprotein. J. Virol. 66:5635-5641.
63. Thali, M., C. Furman, B. Wahren, M. Posner, D. D. Ho, J. Robinson, and J. Sodroski. 1992. Cooperativity of neutralizing antibodies directed against the V3 and CD4 binding regions of the human immunodeficiency virus gp120 envelope glycoprotein. J. Acquired Immune Defic. Syndr. 5:591-599.
64. Thali, M., J. P. Moore, C. Furman, M. Charles, D. D. Ho, J. Robinson, and J. Sodroski. 1993. Characterization of conserved human immunodeficiency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding. J. Virol. 67:3978-3988.
65. Thali, M., U. Olshevsky, C. Furman, D. Gabuzda, M. Posner, and J. Sodroski. 1991. Characterization of a discontinuous HIV-1 gp120 epitope recognised by a broadly reactive neutralizing human monoclonal antibody. J. Virol. 65:6788-6193.
66. Trkola A., T. Dragic, J. Arthos, J. M. Binley, W. C. Olson, G. P. Allaway, C. Cheng-Mayer, J. Robinson, P. J. Maddon, and J. P. Moore. 1996. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR5. Nature 384:184-186.
67. Trkola, A., A. P. 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 virus type 1 by human monoclonal antibodies and tetrameric CD4-IgG. J. Virol. 69:6609-6617.
68. 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.
69. Willey, R. L., M. A. Martin, and K. W. C. Peden. 1994. Increase in soluble CD4 binding to and CD4-induced dissociation of gp120 from virions correlates with infectivity of human immunodeficiency virus type 1. J. Virol. 68:1029-1039.
70. Wrin, T., T. P. Loh, J. C. Vennari, H. Schuitemaker, and J. H. Nunberg. 1995. Adaptation to 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.
71. Wu, L., N. P. Gerard, R. Wyatt, H. Choe, C. Parolin, N. Ruffing, A. Borsetti, A. A. Cardoso, E. Desjardin, W. Newman, C. Gerard, and J. Sodroski. 1996. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature 384:179-183.
72. Wyatt, R., J. P. Moore, M. Accola, E. Desjardin, J. Robinson, and J. Sodroski. 1995. Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J. Virol. 69:5723-5733.
73. Zhou, J. V., and D. C. Montefiori. 1997. Antibody-mediated neutralization of primary isolates of human immunodeficiency virus type 1 in peripheral blood mononuclear cells is not affected by the initial activation state of the cells. J. Virol. 71:2512-2517.
74. Zhuge, W., Q. Gao, Z. Q. Liu, O. Narayan, and E. B. Stephens. 1996. Neutralization of SIVmac239/17E in lymphocyte cultures involves virus strain-specific linear and conformational epitopes encoded by different regions of the env gene including the "V3" domain. Virology 222:184-192.
75. Zolla-Pazner, S., J. O'Leary, S. Burda, M. K. Gorny, M. Kim, J. Mascola, and F. McCutchan. 1995. Serotyping of primary human immunodeficiency virus type 1 isolates from diverse geographic locations by flow cytometry. J. Virol. 69:3807-3815.
76. Zolla-Pazner, S., and S. Sharpe. 1995. A resting cell assay for improved detection of antibody-mediated neutralization of HIV type 1 primary isolates. AIDS Res. Hum. Retroviruses 11:1449-1458.
77. Zhu, T., N. Wang, D. S. Nam, Y. Cao, R. A. Koup, and D. D. Ho. 1993. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261:1179-1181.