Balancing reversion of cytotoxic T-lymphocyte and neutralizing antibody escape mutations within human immunodeficiency virus type 1 Env upon transmission

Journal of Virology

Volumn 83, Issue 17, 2009, Pages 8986-8992

  Peut, Viv ^a   Campbell, Shahan ^a   Gaeguta, Adriana ^a   Center, Rob J ^a   Wilson, Kim ^b   Alcantara, Sheilajen ^a   Fernandez, Caroline S ^a   Purcell, Damian F J ^a   Kent, Stephen J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ANIMAL CELL; ARTICLE; CD8+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; GENE LOSS; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MACACA; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; VIRUS MUTANT; VIRUS MUTATION; VIRUS TRANSMISSION; WILD TYPE; ADAPTATION; ANIMAL; DISEASE TRANSMISSION; GENETICS; GLYCOSYLATION; HUMAN; IMMUNOLOGY; MISSENSE MUTATION; MONKEY DISEASE; SERODIAGNOSIS; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA;

ADAPTATION, BIOLOGICAL; ANIMALS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GLYCOSYLATION; HIV ANTIBODIES; HIV-1; HUMANS; MACACA; MUTATION, MISSENSE; NEUTRALIZATION TESTS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 69249205653     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00599-09     Document Type: Article

References (32)

1. Allen, T. M., M. Altfeld, X. G. Yu, K. M. O'Sullivan, M. Lichterfeld, S. Le Gall, M. John, B. R. Mothe, P. K. Lee, E. T. Kalife, D. E. Cohen, K. A. Freedberg, D. A. Strick, M. N. Johnston, A. Sette, E. S. Rosenberg, S. A. Mallal, P. J. Goulder, C. Brander, and B. D. Walker. 2004. Selection, transmission, and reversion of an antigen-processing cytotoxic T-lymphocyte escape mutation in human immunodeficiency virus type 1 infection. J. Virol. 78:7069-7078. (Pubitemid 38781545)
2. Barouch, D. H., J. Kunstman, M. J. Kuroda, J. E. Schmitz, S. Santra, F. W. Peyerl, G. R. Krivulka, K. Beaudry, M. A. Lifton, D. A. Gorgone, D. C. Montefiori, M. G. Lewis, S. M. Wolinsky, and N. L. Letvin. 2002. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415:335-339.
3. Blay, W. M., S. Gnanakaran, B. Foley, N. A. Doria-Rose, B. T. Korber, and N. L. Haigwood. 2006. Consistent patterns of change during the divergence of human immunodeficiency virus type 1 envelope from that of the inoculated virus in simian/human immunodeficiency virus-infected macaques. J. Virol. 80:999-1014.
4. Blay, W. M., T. Kasprzyk, L. Misher, B. A. Richardson, and N. L. Haigwood. 2007. Mutations in envelope gp120 can impact proteolytic processing of the gp160 precursor and thereby affect neutralization sensitivity of human immunodeficiency virus type 1 pseudoviruses. J. Virol. 81:13037-13049.
5. Borrow, P., H. Lewicki, X. Wei, M. S. Horwitz, N. Peffer, H. Meyers, J. A. Nelson, J. E. Gairin, B. H. Hahn, M. B. A. Oldstone, and G. M. Shaw. 1997. Antiviral pressure exerted by HIV-1-specific CTLs during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3:205-211.
6. Brockman, M. A., A. Schneidewind, M. Lahaie, A. Schmidt, T. Miura, I. Desouza, F. Ryvkin, C. A. Derdeyn, S. Allen, E. Hunter, J. Mulenga, P. A. Goepfert, B. D. Walker, and T. M. Allen. 2007. Escape and compensation from early HLA-B57-mediated cytotoxic T-lymphocyte pressure on human immunodeficiency virus type 1 Gag alter capsid interactions with cyclophilin A. J. Virol. 81:12608-12618.
7. Brumme, Z. L., C. J. Brumme, J. Carlson, H. Streeck, M. John, Q. Eichbaum, B. L. Block, B. Baker, C. Kadie, M. Markowitz, H. Jessen, A. D. Kelleher, E. Rosenberg, J. Kaldor, Y. Yuki, M. Carrington, T. M. Allen, S. Mallal, M. Altfeld, D. Heckerman, and B. D. Walker. 2008. Marked epitopeand allele-specific differences in rates of mutation in human immunodefi- ciency type 1 (HIV-1) Gag, Pol, and Nef cytotoxic T-lymphocyte epitopes in acute/early HIV-1 infection. J. Virol. 82:9216-9227.
8. Bunnik, E. M., L. Pisas, A. C. van Nuenen, and H. Schuitemaker. 2008. Autologous neutralizing humoral immunity and evolution of the viral envelope in the course of subtype B human immunodeficiency virus type 1 infection. J. Virol. 82:7932-7941.
9. Chen, H., A. Piechocka-Trocha, T. Miura, M. Brockman, B. Julg, B. Baker, A. Rothchild, B. Block, A. Schneidewind, T. Koibuchi, F. Pereyra, T. Allen, and B. Walker. 2009. Differential neutralization of human immunodeficiency virus (HIV) replication in autologous CD4 T cells by HIV-specific cytotoxic T lymphocytes. J. Virol. 83:3138-3149.
10. Fernandez, C. S., M. Z. Smith, C. J. Batten, R. De Rose, J. C. Reece, E. Rollman, V. Venturi, M. P. Davenport, and S. J. Kent. 2007. Vaccineinduced T cells control reversion of AIDS virus immune escape mutants. J. Virol. 81:4137-4144.
11. Fernandez, C. S., I. Stratov, R. De Rose, K. Walsh, C. J. Dale, M. Z. Smith, M. B. Agy, S. L. Hu, K. Krebs, D. I. Watkins, D. H. O'Connor, M. P. Davenport, and S. J. Kent. 2005. Rapid viral escape at an immunodominant simian-human immunodeficiency virus cytotoxic T-lymphocyte epitope exacts a dramatic fitness cost. J. Virol. 79:5721-5731.
12. Friedrich, T. C., E. J. Dodds, L. J. Yant, L. Vojnov, R. Rudersdorf, C. Cullen, D. T. Evans, R. C. Desrosiers, B. R. Mothe, J. Sidney, A. Sette, K. Kunstman, S. Wolinsky, M. Piatak, J. Lifson, A. L. Hughes, N. Wilson, D. H. O'Connor, and D. I. Watkins. 2004. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat. Med. 10:275-281.
13. Frost, S. D., T. Wrin, D. M. Smith, S. L. Kosakovsky Pond, Y. Liu, E. Paxinos, C. Chappey, J. Galovich, J. Beauchaine, C. J. Petropoulos, S. J. Little, and D. D. Richman. 2005. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc. Natl. Acad. Sci. USA 102:18514-18519.
14. Goepfert, P. A., W. Lumm, P. Farmer, P. Matthews, A. Prendergast, J. M. Carlson, C. A. Derdeyn, J. Tang, R. A. Kaslow, A. Bansal, K. Yusim, D. Heckerman, J. Mulenga, S. Allen, P. J. Goulder, and E. Hunter. 2008. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. J. Exp. Med. 205:1009-1017.
15. Goulder, P., R. E. Phillips, R. Colbert, S. McAdam, G. Ogg, M. A. Nowak, P. Giangrande, G. Luzzi, B. Morgan, A. Edwards, A. J. McMichael, and S. Rowland-Jones. 1997. Late escape from an immunodominant cytotoxic Tlymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217.
16. Herbeck, J. T., D. C. Nickle, G. H. Learn, G. S. Gottlieb, M. E. Curlin, L. Heath, and J. I. Mullins. 2006. Human immunodeficiency virus type 1 env evolves toward ancestral states upon transmission to a new host. J. Virol. 80:1637-1644.
17. + T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
18. Koenig, S., A. J. Conley, Y. A. Brewah, G. M. Jones, S. Leath, L. J. Boots, V. Davey, G. Pantaleo, J. F. Demarest, C. Carter, et al. 1995. Transfer of HIV-1-specific cytotoxic T lymphocytes to an AIDS patient leads to selection for mutant HIV variants and subsequent disease progression. Nat. Med. 1:330-336.
19. Leslie, A. J., K. J. Pfafferott, P. Chetty, R. Draenert, M. M. Addo, M. Feeney, Y. Tang, E. C. Holmes, T. Allen, J. G. Prado, M. Altfeld, C. Brander, C. Dixon, D. Ramduth, P. Jeena, S. A. Thomas, A. St. John, T. A. Roach, B. Kupfer, G. Luzzi, A. Edwards, G. Taylor, H. Lyall, G. Tudor-Williams, V. Novelli, J. Martinez-Picado, P. Kiepiela, B. D. Walker, and P. J. Goulder. 2004. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10:282-289.
20. Liu, Y., J. McNevin, H. Zhao, D. M. Tebit, R. M. Troyer, M. McSweyn, A. K. Ghosh, D. Shriner, E. J. Arts, M. J. McElrath, and J. I. Mullins. 2007. Evolution of human immunodeficiency virus type 1 cytotoxic T-lymphocyte epitopes: fitness-balanced escape. J. Virol. 81:12179-12188. (Pubitemid 350085833)
21. Loh, L., C. J. Batten, J. Petravic, M. P. Davenport, and S. J. Kent. 2007. In vivo fitness costs of different Gag CD8 T-cell escape mutant simian-human immunodeficiency viruses in macaques. J. Virol. 81:5418-5422.
22. Loh, L., and S. J. Kent. 2008. Quantification of simian immunodeficiency virus cytotoxic T-lymphocyte escape mutant viruses. AIDS Res. Hum. Retrovir. 24:1067-1072.
23. Navis, M., D. E. Matas, A. Rachinger, F. A. Koning, P. van Swieten, N. A. Kootstra, and H. Schuitemaker. 2008. Molecular evolution of human immunodeficiency virus type 1 upon transmission between human leukocyte antigen disparate donor-recipient pairs. PLoS One 3:e2422.
24. Peut, V., and S. J. Kent. 2009. Substantial envelope-specific CD8 T-cell immunity fails to control SIV disease. Virology 384:21-27.
25. Peut, V., and S. J. Kent. 2007. Utility of human immunodeficiency virus type 1 envelope as a T-cell immunogen. J. Virol. 81:13125-13134. (Pubitemid 350156951)
26. Peyerl, F. W., H. S. Bazick, M. H. Newberg, D. H. Barouch, J. Sodroski, and N. L. Letvin. 2004. Fitness costs limit viral escape from cytotoxic T lymphocytes at a structurally constrained epitope. J. Virol. 78:13901-13910.
27. Phillips, R. E., S. Rowland-Jones, D. F. Nixon, F. M. Gotch, J. P. Edwards, A. O. Ogunlesi, J. G. Elvin, J. A. Rothbard, C. R. Bangham, C. R. Rizza, et al. 1991. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 354:453-459.
28. 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.
29. Sato, S., E. Yuste, W. A. Lauer, E. H. Chang, J. S. Morgan, J. G. Bixby, J. D. Lifson, R. C. Desrosiers, and W. E. Johnson. 2008. Potent antibody-mediated neutralization and evolution of antigenic escape variants of simian immunodeficiency virus strain SIVmac239 in vivo. J. Virol. 82:9739-9752.
30. Schneidewind, A., M. A. Brockman, R. Yang, R. I. Adam, B. Li, S. Le Gall, C. R. Rinaldo, S. L. Craggs, R. L. Allgaier, K. A. Power, T. Kuntzen, C. S. Tung, M. X. LaBute, S. M. Mueller, T. Harrer, A. J. McMichael, P. J. Goulder, C. Aiken, C. Brander, A. D. Kelleher, and T. M. Allen. 2007. Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J. Virol. 81:12382-12393. (Pubitemid 350085852)
31. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
32. 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. (Pubitemid 39585357)