Susceptibility of recently transmitted subtype B human immunodeficiency virus type 1 variants to broadly neutralizing antibodies

Journal of Virology

Volumn 81, Issue 16, 2007, Pages 8533-8542

  Quakkelaar, Esther D ^a   Van Alphen, Floris P J ^a   Boeser Nunnink, Brigitte D M ^a   Van Nuenen, Ad C ^a   Pantophlet, Ralph ^b   Schuitemaker, Hanneke ^a,c  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c SANQUIN RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY;

ARTICLE; CONTROLLED STUDY; HOMOSEXUALITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; PRIORITY JOURNAL; SEROCONVERSION; SEXUAL TRANSMISSION; VIRUS GENE; VIRUS NEUTRALIZATION; VIRUS TRANSMISSION;

AIDS VACCINES; AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIGENS, VIRAL; EPITOPES; GENE PRODUCTS, ENV; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HOMOSEXUALITY, MALE; HUMANS; MALE; NEUTRALIZATION TESTS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 34547735938     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02816-06     Document Type: Article

References (55)

1. 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.
2. Beaumont, T., A. van Nuenen, S. Broersen, W. A. Blattner, V. V. Lukashov, and H. Schuitemaker. 2001. Reversal of HIV-1 IIIB toward a neutralization resistant phenotype in an accidentally infected laboratory worker with a progressive clinical course. J. Virol. 75:2246-2252.
3. Binley, J. M., T. Wrin, B. Korber, M. B. Zwick, M. Wang, C. Chappey, G. Stiegler, R. Kunert, S. Zolla-Pazner, H. Katinger, C. J. Petropoulos, and D. R. Burton. 2004. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78:13232-13252.
4. Boom, R., C. J. A. Sol, M. M. M. Salimans, C. L. Jansen, P. M. E. Wertheim-van Dillen, and J. Van der Noordaa. 1991. A rapid and simple method for purification of nucleic acids. J. Clin. Microbiol. 28:495-503.
5. Brown, B. K., J. M. Darden, S. Tovanabutra, T. Oblander, J. Frost, E. Sanders-Buell, M.S. de Souza, D. L. Birx, F. E. McCutchan, and V. R. Polonis. 2005. Biologic and genetic characterization of a panel of 60 human immunodeficiency virus type 1 isolates, representing clades A, B, C, D, CRF01_AE, and CRF02_AG, for the development and assessment of candidate vaccines. J. Virol. 79:6089-6101.
6. Burton, D. R., R. C. Desrosiers, R. W. Doms, W. C. Koff, P. D. Kwong, J. P. Moore, G. J. Nabel, J. Sodroski, I. A. Wilson, and R. T. Wyatt. 2004. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5:233-236.
7. Burton, D. R., J. Pyati, R. Koduri, S. J. Sharp, G. B. Thornton, P. W. H. Parren, L. S. W. Sawyer, R. M. Hendry, N. Dunlop, P. L. Nara, M. Lamacchia, E. M. 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 a recombinant human monoclonal antibody. Science 266:1024-1027.
8. 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.
9. Choudhry, V., M. Y. Zhang, I. Harris, I. A. Sidorov, B. Vu, A. S. Dimitrov, T. Fouts, and D. S. Dimitrov. 2006. Increased efficacy of HIV-1 neutralization by antibodies at low CCR5 surface concentration. Biochem. Biophys. Res. Commun. 348:1107-1115.
10. Conley, A. J., M. K. Gorny, J. A. Kessler, 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.
11. Dacheux, L., A. Moreau, Y. Ataman-Onal, F. Biron, B. Verrier, and F. Barin. 2004. Evolutionary dynamics of the glycan shield of the human immunodeficiency virus envelope during natural infection and implications for exposure of the 2G12 epitope. J. Virol. 78:12625-12637.
12. Derdeyn, C. A., J. M. Decker, F. Bibollet-Ruche, J. L. Mokili, M. Muldoon, S. A. Denham, M. L. Heil, F. Kasolo, R. Musonda, B. H. Hahn, G. M. Shaw, B. T. Korber, S. Allen, and E. Hunter. 2004. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303:2019-2022.
13. De Roda Husman, A. M., M. Koot, M. Cornelissen, M. Brouwer, S. M. Broersen, M. Bakker, M. Th.L. Roos, M. Prins, F. De Wolf, R. A. Coutinho, F. Miedema, J. Goudsmit, and H. Schuitemaker. 1997. Association between CCR5 genotype and the clinical course of HIV-1 infection. Ann. Intern. Med. 127:882-890.
14. Frost, S. D., Y. Liu, S. L. Pond, C. Chappey, T. Wrin, C. J. Petropoulos, S. J. Little, and D. D. Richman. 2005. Characterization of human immunodeficiency virus type 1 (HIV-1) envelope variation and neutralizing antibody responses during transmission of HIV-1 subtype B. J. Virol. 79:6523-6527.
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. Gray, E. S., T. Meyers, G. Gray, D. C. Montefiori, and L. Morris. 2006. Insensitivity of paediatric HIV-1 subtype C viruses to broadly neutralizing monoclonal antibodies raised against subtype B. PLoS Med. 3:e255.
17. Haigwood, N. L., D. C. Montefiori, W. F. Sutton, J. McClure, A. J. Watson, G. Voss, V. M. Hirsch, B. A. Richardson, N. L. Letvin, S. L. Hu, and P. R. Johnson. 2004. Passive immunotherapy in simian immunodeficiency virus-infected macaques accelerates the development of neutralizing antibodies. J. Virol. 78:5983-5995.
18. 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.
19. Lange, J. M. A., C. A. B. Boucher, C. E. M. Hollak, E. H. H. Wiltink, P. Reiss, E. A. Van Royen, M. Th. L. Roos, S. A. Danner, and J. Goudsmit. 1990. Failure of zidovudine prophylaxis after accidental exposure to HIV-1. N. Engl. J. Med. 322:1375-1377.
20. Letvin, N. L., D. H. Barouch, and D. C. Montefiori. 2002. Prospects for vaccine protection against HIV-1 infection and AIDS. Annu. Rev. Immunol. 20:73-99.
21. Li, B., J. M. Decker, R. W. Johnson, F. Bibollet-Ruche, X. Wei, J. Mulenga, S. Allen, E. Hunter, B. H. Hahn, G. M. Shaw, J. L. Blackwell, and C. A. Derdeyn. 2006. Evidence for potent autologous neutralizing antibody titers and compact envelopes in early infection with subtype C human immunodeficiency virus type 1. J. Virol. 80:5211-5218.
22. Li, M., F. Gao, J. R. Mascola, L. Stamatatos, V. R. Polonis, M. Koutsoukos, G. Voss, P. Goepfert, P. Gilbert, K. M. Greene, M. Bilska, D. L. Kothe, J. F. Salazar-Gonzalez, X. Wei, J. M. Decker, B. H. Hahn, and D. C. Montefiori. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125.
23. Li, M., J. F. Salazar-Gonzalez, C. A. Derdeyn, L. Morris, C. Williamson, J. E. Robinson, J. M. Decker, Y. Li, M. G. Salazar, V. R. Polonis, K. Mlisana, S. A. Karim, K. Hong, K. M. Greene, M. Bilska, J. Zhou, S. Allen, E. Chomba, J. Mulenga, C. Vwalika, F. Gao, M. Zhang, B. T. Korber, E. Hunter, B. H. Hahn, and D. C. Montefiori. 2006. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J. Virol. 80:11776-11790.
24. Louder, M. K., A. Sambor, E. Chertova, T. Hunte, S. Barrett, F. Ojong, E. Sanders-Buell, S. Zolla-Pazner, F. E. McCutchan, J. D. Roser, D. Gabuzda, J. D. Lifson, and J. R. Mascola. 2005. HIV-1 envelope pseudotyped viral vectors and infectious molecular clones expressing the same envelope glycoprotein have a similar neutralization phenotype, but culture in peripheral blood mononuclear cells is associated with decreased neutralization sensitivity. Virology 339:226-238.
25. 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.
26. 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.
27. McInerney, T. L., L. McLain, S. J. Armstrong, and N. J. Dimmock. 1997. A human IgG1 (b12) specific for the CD4 binding site of HIV-1 neutralizes by inhibiting the virus fusion entry process, but b12 Fab neutralizes by inhibiting a postfusion event. Virology 233:313-326.
28. McMichael, A. J., and T. Hanke. 2003. HIV vaccines 1983-2003. Nat. Med. 9:874-880.
29. Miller, M. D., R. Geleziunas, E. Bianchi, S. Lennard, R. Hrin, H. Zhang, M. Lu, Z. An, P. Ingallinella, M. Finotto, M. Mattu, A. C. Finnefrock, D. Bramhill, J. Cook, D. M. Eckert, R. Hampton, M. Patel, S. Jarantow, J. Joyce, G. Ciliberto, R. Cortese, P. Lu, W. Strohl, W. Schleif, M. McElhaugh, S. Lane, C. Lloyd, D. Lowe, J. Osbourn, T. Vaughan, E. Emini, G. Barbato, P. S. Kim, D. J. Hazuda, J. W. Shiver, and A. Pessi. 2005. A human monoclonal antibody neutralizes diverse HIV-1 isolates by binding a critical gp41 epitope. Proc. Natl. Acad. Sci. USA 102:14759-14764.
30. Montefiori, D. C., T. S. Hill, H. T. Vo, B. D. Walker, and E. S. Rosenberg. 2001. Neutralizing antibodies associated with viremia control in a subset of individuals after treatment of acute human immunodeficiency virus type 1 infection. J. Virol. 75:10200-10207.
31. 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.
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.
33. Nakowitsch, S., H. Quendler, H. Fekete, R. Kunert, H. Katinger, and G. Stiegler. 2005. HIV-1 mutants escaping neutralization by the human antibodies 2F5, 2G12, and 4E10: in vitro experiments versus clinical studies. AIDS 19:1957-1966.
34. Pantophlet, R., E. Ollman Saphire, P. Poignard, P. W. H. I. Parren, I. A. Wilson, and D. R. Burton. 2002. 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.
35. Parren, P. W. H. I., 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. 75:8240-8347.
36. Purtscher, M., A. Trkola, G. Gruber, A. Buchacher, R. Predl, F. Steindl, C. Tauer, R. Berger, N. Barrett, and A. Jungbauer. 1994. A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 10:1651-1658.
37. Quakkelaar, E. D., E. M. Bunnik, F. P. van Alphen, B. D. Boeser-Nunnink, A. C. van Nuenen, and H. Schuitemaker. 2007. Escape of human immunodeficiency virus type 1 from broadly neutralizing antibodies is not associated with a reduction of viral replicative capacity in vitro. Virology 363:447-453.
38. 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.
39. Sagar, M., X. Wu, S. Lee, and J. Overbaugh. 2006. Human immunodeficiency virus type 1 V1-V2 envelope loop sequences expand and add glycosylation sites over the course of infection, and these modifications affect antibody neutralization sensitivity. J. Virol. 80:9586-9598.
40. 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.
41. Scanlan, C. N., R. Pantophlet, M. R. Wormald, E. Ollman 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 alfa1->2 mannose residues on the outer face of gp120. J. Virol. 76:7306-7321.
42. Schuitemaker, H., M. Koot, N. A. Kootstra, M. W. Dercksen, R. E. Y. De Goede, R. P. Van Steenwijk, J. M. A. Lange, J. K. M. Eeftink Schattenkerk, F. Miedema, and M. Tersmette. 1992. Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus populations. J. Virol. 66:1354-1360.
43. Shibata, R., T. Igarashi, N. Haigwood, A. Buckler-White, R. Ogert, W. Ross, R. Willey, M. W. Cho, and M. A. Martin. 1999. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infection of macaque monkeys. Nat. Med. 5:204-210.
44. Smith, D. M., D. D. Richman, and S. J. Little. 2005. HIV superinfection. J. Infect. Dis. 192:438-444.
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. Tersmette, M., I. N. Winkel, M. Groenink, R. A. Gruters, P. Spence, E. Saman, G. van der Groen, F. Miedema, and J. G. Huisman. 1989. Detection and subtyping of HIV-1 isolates with a panel of characterized monoclonal antibodies to HIV-p24 gag. Virology 171:149-155.
47. Trkola, A., H. Kuster, P. Rusert, B. Joos, M. Fischer, C. Leemann, A. Manrique, M. Huber, M. Rehr, A. Oxenius, R. Weber, G. Stiegler, B. Vcelar, H. Katinger, L. Aceto, and H. F. Gunthard. 2005. Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat. Med. 11:593-594.
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. 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 human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J. Clin. Investig. 94:2060-2067.
50. Veazey, R. S., R. J. Shattock, M. Pope, J. C. Kirijan, J. Jones, Q. Hu, T. Ketas, P. A. Marx, P. J. Klasse, D. R. Burton, and J. P. Moore. 2003. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat. Med. 9:343-346.
51. Veenstra, J., R. Schuurman, M. Cornelissen, A. B. Van't Wout, C. A. B. Boucher, H. Schuitemaker, J. Goudsmit, and R. A. Coutinho. 1995. Transmission of zidovudine-resistant human immunodeficiency virus type 1 variants following deliberate injection with blood of a patient with AIDS: characteristics and natural history of the virus. Clin. Infect. Dis. 21:556-560.
52. Wu, X., A. B. Parast, B. A. Richardson, R. Nduati, G. John-Stewart, D. Mbori-Ngacha, S. M. Rainwater, and J. Overbaugh. 2006. Neutralization escape variants of human immunodeficiency virus type 1 are transmitted from mother to infant. J. Virol. 80:835-844.
53. Xia, X., and Z. Xie. 2001. DAMBE: software package for data analysis in molecular biology and evolution. J. Hered. 92:371-373.
54. Zhang, M., B. Gaschen, W. Blay, B. Foley, N. Haigwood, C. Kuiken, and B. Korber. 2004. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14:1229-1246.
55. Zwick, M. B., R. Jensen, S. Church, M. Wang, G. Stiegler, R. Kunert, H. Katinger, and D. R. Burton. 2005. Anti-human immunodeficiency virus type 1 (HIV-1) antibodies 2F5 and 4E10 require surprisingly few crucial residues in the membrane-proximal external region of glycoprotein gp41 to neutralize HIV-1. J. Virol. 79:1252-1261.