Cryptic nature of a conserved, CD4-inducible V3 loop neutralization epitope in the native envelope glycoprotein oligomer of CCR5-restricted, but not CXCR4-using, primary human immunodeficiency virus type 1 strains

Journal of Virology

Volumn 79, Issue 11, 2005, Pages 6957-6968

  Lusso, Paolo ^a,b   Earl, Patricia L ^d   Sironi, Francesca ^a   Santoro, Fabio ^a   Ripamonti, Chiara ^a   Scarlatti, Gabriella ^a   Longhi, Renato ^c   Berger, Edward A ^d   Burastero, Samuele E ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF CAGLIARI   (Italy)

^c CNR   (Italy)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; D19 ANTIBODY; ENVELOPE PROTEIN; EPITOPE; GLYCOPROTEIN; GLYCOPROTEIN GP 120; MONOCLONAL ANTIBODY; MONOMER; OLIGOMER; UNCLASSIFIED DRUG;

ARTICLE; GENETIC VARIABILITY; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; VIRAL GENETICS; VIRUS ISOLATION; VIRUS NEUTRALIZATION; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD4; CELL LINE; CONSERVED SEQUENCE; EPITOPE MAPPING; EPITOPES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PEPTIDE FRAGMENTS; PHENOTYPE; RECEPTORS, CCR5; RECEPTORS, CXCR4; SEQUENCE HOMOLOGY, AMINO ACID;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MURINAE;

EID: 18744368767     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.11.6957-6968.2005     Document Type: Article

References (68)

1. Berger, E. A., P. M. Murphy, and J. M. Farber. 1999. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu. Rev. Immunol. 17:657-700.
2. Bou-Habib, D. C., G. Roderiquez, T. Oravecz, P. W. Berman, P. Lusso, and M. A. Norcross. 1994. Cryptic nature of envelope V3 region epitopes protects primary human immunodeficiency virus type 1 from antibody neutralization. J. Virol. 68:6006-6013.
3. Cao, J., N. Sullivan, E. Desjardins, C. Parolin, J. Robinson, R. Wyatt, and J. Sodroski. 1997. Replication and neutralization of human immunodeficiency virus type 1 lacking the V1/V2 variable loops of the gp120 envelope glycoprotein. J. Virol. 71:9808-9812.
4. Cavacini, L. A., M. Duval, J. Robinson, and M. R. Posner. 2002. Interactions of human antibodies, epitope exposure, antibody binding and neutralization of primary isolate HIV-1 virions. AIDS 16:2409-2417.
5. Cavacini, L. A., M. Duval, L. Song, R. Sangster, S.-H. Xiang, J. Sodroski, and M. Posner. 2003. Conformational changes in Env oligomer induced by an antibody dependent on the V3 loop base. AIDS 17:685-689.
6. Cecilia, D., V. N. Kewal Ramani, J. O'Leary, B. Volsky, P. Nyambi, S. Burda, S. Xu, D. R. Littman, and S. Zolla-Pazner. 1998. Neutralization profiles of primary human immunodeficiency virus type 1 isolates in the context of coreceptor usage. J. Virol. 72:6988-6996.
7. Choe, 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 beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135-1148.
8. Cocchi, F., A. DeVico, A. Garzino-Demo, A. Cara, R. C. Gallo, and P. Lusso. 1996. The V3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection. Nat. Med. 2:1244-1247.
9. Conley, A. J., M. K. Gorny, J. A. Kessler, II, L. J. Boots, M. Ossorio-Castro, S. Koenig, D. W. Lineberger, E. A. Emini, C. Williams, and S. Zolla-Pazner. 1994. Neutralization of primary human immunodeficiency virus type 1 isolates by the broadly reactive anti-V3 monoclonal antibody, 447-52D. J. Virol. 68:6994-7000.
10. Connor, R. I., K. E. Sheridan, D. Ceradini, S. Choe, and N. R. Landau. 1997. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J. Exp. Med. 185:621-628.
11. Cornelissen, M., M. Mulder-Kampinga, J. Veenstra, F. Zorgdrager, C. Kuiken,S. Hartman, J. Dekker, L. van der Hoek, C. Sol, and R. Coutinho. 1995. Syncytium-inducing (SI) phenotype suppression at seroconversion after intramuscular inoculation of a non-syncytium-inducing/SI phenotypically mixed human immunodeficiency virus population. J. Virol. 69:1810-1818.
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. Di Marzo Veronese, F., M. S. Reitz, Jr., 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.
14. Earl, P. L., C. C. Broder, D. Long, S. A. Lee, J. Peterson, S. Chakrabarti, R. W. Doms, and B. Moss. 1994. Native oligomeric forms of human immunodeficiency virus type 1 envelope glycoprotein elicit a diverse array of monoclonal antibody reactivities. J. Virol. 68:3015-3026.
15. 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.
16. Gallo, R. C., and L. Montagnier. 2003. Retrospective: the discovery of HIV as the cause of AIDS. N. Engl. J. Med. 349:2283-2285.
17. 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.
18. Gorny, M. K., K. Revesz, C. Williams, B. Volsky, M. K. Louder, C. A. Anyangwe, C. Krachmarov, S. C. Kayman, A. Pinter, A. Nadas, P. N. Nyambi, J. R. Mascola, and S. Zolla-Pazner. 2004. The V3 loop is accessible on the surface of most human immunodeficiency virus type 1 primary isolates and serves as a neutralization epitope. J. Virol. 78:2394-2404.
19. Gorny, M. K., C. Williams, B. Volsky, K. Revesz, S. Cohen, V. R. Polonis, W. J. Honnen, S. C. Kayman, C. Krachmarov, A. Pinter, and S. Zolla-Pazner. 2002. Human monoclonal antibodies specific for conformation-sensitive epitopes of V3 neutralize human immunodeficiency virus type 1 primary isolates from various clades. J. Virol. 76:9035-9045.
20. Grivel, J. C., and L. B. Margolis. 1999. CCR5- and CXCR4-tropic HIV-1 are equally cytopathic for their T-cell targets in human lymphoid tissue. Nat. Med. 5:344-346.
21. Ida, S., H. Gatanaga, T. Shioda, Y. Nagai, N. Kobayashi, S. Shimada, S. Kimura, A. Iwamoto, and S. Oka 1997. HIV type 1 V3 variation dynamics in vivo: long-term persistence of non-syncytium-inducing genotypes and transient presence of syncytium-inducing genotypes during the course of progressive AIDS. AIDS Res. Hum. Retrovir. 13:1597-1609.
22. Jensen, M. A., L. Fu-Sheng, A. B. van't Wout, D. C. Nickle, D. Shriner, H.-X. He, S. McLaughlin, R. Shankarappa, J. B. Margolick, and J. I. Mullins. 2003. Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences. J. Virol. 77:13376-13388.
23. Karlsson, I., L. Antonsson, Y. Shi, A. Karlssond, J. Albert, T. Leitner, B. Olde, C. Owman, and E. M. Fenyo. 2003. HIV biological variability unveiled: frequent isolations and chimeric receptors reveal unprecedented variation of coreceptor use. AIDS 17:2561-2569.
24. Kayman, S. C., Z. Wu, K. Revesz, H. Chen, R. Kopelman, and A. Pinter. 1994. Presentation of native epitopes in the V1/V2 and V3 regions of human immunodeficiency virus type 1 gp120 by fusion glycoproteins containing isolated gp120 domains. J. Virol. 68:400-410.
25. Koot, M., I. Keet, A. Vos, R. deGoede, M. Roos, R. Coutinho, F. Miedema, P. Schellekens, and M. Tersmette. 1993. Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD44+ cell depletion and progression to AIDS. Ann. Intern. Med. 118:681-688.
26. Kwong, P. D., M. L. Doyle, D. J. Casper, C. Cicala, S. A. Leavitt, S. Majeed, and J. Arthos. 2002. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420:678-682.
27. Kwong, P. D., R. Wyatt, J. Robinson, R. Sweet, J. Sodroski, and W. Hendrickson. 1998. Structure of an HIV-1 gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing antibody. Nature 393:648-659.
28. LaCasse, R. A., K. E. Follis, T. Moudgil, M. Trahey, J. M. Binley, V. Planelles, S. Zolla-Pazner, and J. H. Nunberg. 1998. Coreceptor utilization by human immunodeficiency virus type 1 is not a primary determinant of neutralization sensitivity. J. Virol. 72:2491-2495.
29. Lathey, J. L., R. D. Pratt, and S. A. Specter 1997. Appearance of autologous neutralizing antibody correlates with reduction in virus load and phenotype switch during primary infection with human immunodeficiency virus type. J. Infect. Dis. 175:231-232.
30. + T-cell clone (PM1): failure to downregulate CD4 and to interfere with cell-line-tropic HIV-1. J. Virol. 69:3712-3720.
31. Lusso, P., and R. C. Gallo. 1997. Chemokines and HIV infection. Curr. Opin. Infect. Dis. 10:12-17.
32. Maddon, P. J., A. G. Dalgleish, J. S. Mcdougal, P. R. Clapham, R. A. Weiss, and R. Axel. 1986. The T4 gene encodes the AIDS virus receptor and is expressed in the immune-system and the brain. Cell 47:333-348.
33. Mascola, J. R., S. W. Snyder, O. S. Weislow, S. M. Belay, R. B. Belshe, D. H. Schwartz, M. L. Clements, R. Dolin, B. S. Graham, G. J. Gorse, M. C. Keefer, M. J. McElrath, M. C. Walker, K. F. Wagner, J. G. McNeil, F. E. McCutchan, D. S. Burke, et al. 1996. Immunization with envelope subunit vaccine products elicits neutralizing antibodies against laboratory-adapted but not primary isolates of human immunodeficiency virus type 1. J. Infect. Dis. 173:340-348.
34. Mbah, H. A., S. Burda, M. K. Gorny, C. Williams, K. Revesz, S. Zolla-Pazner, and P. N. Nyambi. 2001. Effect of soluble CD4 on exposure of epitopes on primary, intact, native human immunodeficiency virus type 1 virions of different genetic clades. J. Virol. 75:7785-7788.
35. McKeating, J. A., J. Gow, J. Goudsmit, L. H. Pearl, C. Mulder, and R. A. Weiss. 1989. Characterization of HIV-1 neutralization escape mutants. AIDS 3:777-784.
36. Montefiori, D. C., R. G. Collman, T. R. Fouts, J. Y. Zhou, M. Bilska, J. A. Hoxie, J. P. Moore, and D. P. Bolognesi. 1998. Evidence that antibody-mediated neutralization of human immunodeficiency virus type 1 by sera from infected individuals is independent of coreceptor usage. J. Virol. 72:1886-1893.
37. Moore, J. P., Y. Cao, L. Qing, Q. J. Sattentau, J. Pyati, R. Koduri, 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.
38. Moore, J. P., P. W. Parren, and D. R. Burton. 2001. Genetic subtypes, humoral immunity, and human immunodeficiency virus type 1 vaccine development J. Virol. 75:5721-5729.
39. Moore, J. P., A. Trkola, B. Korber, L. J. Boots, J. A. Kessler 2nd, 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.
40. Nara, P. L., L. Smit, N. Dunlop, W. Hatch, M. D. Waters, J. Kelliher, R. C. Gallo, P. J. Fischinger, and J. Goudsmit. 1990. Emergence of viruses resistant to neutralization by V3-specific antibodies in experimental human immunodeficiency virus type 1 (IIIB) infection of chimpanzees. J. Virol. 64: 3779-3791.
41. Nussbaum, O., C. C. Broder, and E. A. Berger. 1994. Fusogenic mechanisms of enveloped-virus glycoproteins analyzed by a novel recombinant vaccinia virus-based assay quantitating cell fusion-dependent reporter gene activation. J. Virol. 68:5411-5422.
42. Parren, P. W., L. Mondor, D. Naniche, H. J. Ditzel, P. J. Klasse, D. R. Burton, and Q. J. Sattentau. 1998. Neutralization of human immunodeficiency virus type 1 by antibody to gp120 is determined primarily by occupancy of sites on the virion irrespective of epitope specificity. J. Virol. 72:3512-3519.
43. Philpott, S., B. Weiser, K. Anastos, C. M. Kitchen, E. Robison, and W. A. Meyer III. 2001. Preferential suppression of CXCR4-specific strains of HIV-1 by antiviral therapy. J. Clin. Investig. 107:431-438.
44. Rizzuto, C., R. Wyatt, N. Hernandez-Ramos, Y. Sun, P. D. Kwong, W. A. Hendrickson, and J. Sodroski. 1998. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280:1949-1953.
45. Salzwedel, K., E. D. Smith, B. Dey, and E. A. Berger. 2000. Sequential CD4-coreceptor interactions in human immunodeficiency virus type 1 Env function: soluble CD4 activates Env for coreceptor-dependent fusion and reveals blocking activities of antibodies against cryptic conserved epitopes on gp120. J. Virol. 74:326-333.
46. 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.
47. 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.
48. Scarlatti, G., T. Leitner, E. Halapi, J. Wahlberg, P. Marchisio, M. A. Clerici-Schoeller, H. Wigzell, E. M. Fenyo, J. Albert, and M. Uhlen. 1993. Comparison of variable region 3 sequences of human immunodeficiency virus type 1 from infected children with the RNA and DNA sequences of the virus populations of their mothers. Proc. Natl. Acad. Sci. USA 90:1721-1725.
49. Scarlatti, G., E. Tresoldi, A. Björndal, R. Fredriksson, C. Colognesi, H. K. Deng, M. S. Malnati, A. Plebani, A. G. Siccardi, D. R. Littman, E. M. Fenyö, and P. Lusso. 1997. In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat. Med. 3:1259-1265.
50. Shankarappa, R., J. B. Margolik, S. Gange, A. G. Rodrigo, D. Upchurch, H. Farzadegan, P. Gupta, C. R. Rinaldo, G. H. Learn, He, X., and J. I. Mullins 1999. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 73:10489-10502.
51. Sharon, M., N. Kessler, R. Levy, S. Zolla-Pazner, M. Gorlach, and J. Anglister. 2003. Alternative conformations of the V3 loop of HIV-1: structures that mimic β-hairpins in MIP-1α/RANTES and SDF-1 suggest a mechanism for co-receptor selectivity. Structure 11:225-236.
52. Spenlehauer, C., S. Saragosti, H. Fleury, A. Kirn, A. Aubertin, and C. Moog. 1998. Study of the V3 loop as a target epitope for antibodies involved in the neutralization of primary isolates versus T-cell line-adapted strains of human immunodeficiency virus type 1. J. Virol. 72:9855-9864.
53. Stamatatos, L., and C. Cheng-Mayer. 1995. Structural modulations of the envelope gp120 glycoprotein of human immunodeficiency virus type 1 upon oligomerization and differential V3 loop epitope exposure of isolates displaying distinct tropism upon virion-soluble receptor binding. J. Virol. 69:6191-6198.
54. Stanfield, R. L., M. K. Gorny, C. Williams, S. Zolla-Pazner, and I. A. Wilson. 2004. Structural rationale for the broad neutralization of HIV-1 by human monoclonal antibody 447-52D. Structure 12:193-204.
55. Sullivan, N., Y. Sun, Q. Sattentau, M. Thali, D. Wu, G. Denisova, J. Gershoni, J. Robinson, J. Moore, and J. Sodroski. 1998. CD4-induced conformational changes in the human immunodeficiency virus type 1 gp120 glycoprotein: consequences for virus entry and neutralization. J. Virol. 72:4694-4703.
56. 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.
57. 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.
58. Trkola, A., T. Ketas, V. N. Kewalramani, F. Endorf, J. M. Binley, H. Katinger, J. Robinson, D. R. Littman, and J. P. Moore. 1998. Neutralization sensitivity of human immunodeficiency virus type 1 primary isolates to antibodies and CD4-based reagents is independent of coreceptor usage. J. Virol. 72:1876-1885.
59. VanCott, T. C., V. R. Polonis, L. D. Loomis, N. L. Michael, P. L. Nara, and D. L. Birx. 1995. Differential role of V3-specific antibodies in neutralization assays involving primary and laboratory-adapted isolates of HIV type 1. AIDS Res. Hum. Retrovir. 11:1379-1391.
60. van 't Wout, A. B., N. A. Kootstra, G. A. Mulder-Kampinga, N. Albrecht-van Lent, H. J. Scherpbier, J. Veenstra, K. Boer, R. A. Coutinho, F. Miedema, and H. Schuitemaker. 1994. Macrophage-tropic variants initiate HIV-1 infection after sexual, parenteral, and vertical transmission. J. Clin. Investig. 94:2060-2067.
61. Wolinsky, S. M., R. S. Veazey, K. J. Kunstman, P. J. Klasse, J. Dufour, A. J. Marozsan, M. S. Springer, and J. P. Moore. 2004. Effect of a CCR5 inhibitor on viral loads in macaques dual-infected with R5 and X4 primate immunodeficiency viruses. Virology 328:19-29.
62. Wrin, T., T. P. Loh, J. C. 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.
63. Wu, L., N. P. Gerard, R. Wyatt, H. Choe, C. Parolin, N. Ruffing, A. Borsetti, A. Cardoso, E. Desjardins, 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.
64. Wyatt, R., P. D. Kwong, E. Desjardins, R. W. Sweet, J. Robinson, W. A. Hendrickson, and J. Sodroski. 1998. The antigenic structure of the human immunodeficiency virus gp120 envelope glycoprotein. Nature 393:705-710.
65. Wyatt, R., J. Moore, M. Accola, E. Desjardins, 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.
66. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888.
67. Xiang, S. H., N. Doka, R. K. Choudhary, J. Sodroski, and J. E. Robinson. 2002. Characterization of CD4-induced epitopes on the HIV type 1 gp120 envelope glycoprotein recognized by neutralizing human monoclonal antibodies. AIDS Res. Hum. Retrovir. 18:1207-1217.
68. Zhang, Y., R. Fredriksson, J. McKeating, and E. M. Fenyo. 1997. Passage of HIV-1 molecular clones into different cells lines confers differential sensitivity to neutralization. Virology 238:254-264.