CD4+ target cell availability determines the dynamics of immune escape and reversion in vivo

Journal of Virology

Volumn 82, Issue 8, 2008, Pages 4091-4101

  Petravic, Janka ^a   Loh, Liyen ^b   Kent, Stephen J ^b   Davenport, Miles P ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EPITOPE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL KILLING; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; MACACA; NONHUMAN; PRIORITY JOURNAL; REVERTANT; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA; VIRUS MUTATION; VIRUS REPLICATION; ANIMAL; BIOLOGICAL MODEL; GENETIC SELECTION; GENETICS; IMMUNOLOGY; MUTATION; PHYSIOLOGY; VIROLOGY; VIRUS LOAD;

HUMAN IMMUNODEFICIENCY VIRUS; MACACA; SIMIAN IMMUNODEFICIENCY VIRUS; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; MACACA NEMESTRINA; MODELS, IMMUNOLOGICAL; MUTATION; SELECTION (GENETICS); SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIREMIA;

EID: 41949138131     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02552-07     Document Type: Article

References (39)

1. Allen, T. M., M. Altfeld, X. G. Vu, 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.
2. Allen, T. M., D. H. O'Connor, P. Jing, J. L. Dzuris, B. R. Mothe, T. U. Vogel, E. Dunphy, M. E. Liebl, C. Emerson, N. Wilson, K. J. Kunstman, X. Wang, D. B. Allison, A. L. Hughes, R. C. Desrosiers, J. D. Altman, S. M. Wolinsky, A. Sette, and D. I. Watkins. 2000. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 407:386-390.
3. Asquith, B., and A. R. McLean. 2007. In vivo CD8+ T cell control of immunodeficiency virus infection in humans and macaques. Proc. Natl. Acad. Sci. USA 104:6365-6370.
4. Bonhoeffer, S., A. D. Barbour, and R. J. De Boer. 2002. Procedures for reliable estimation of viral fitness from time-series data. Proc. R. Soc. Lond. B Biol. Sci. 269:1887-1893.
5. Brumme, Z. L., C. J. Brumme, D. Heckerman, B. T. Korber, M. Daniels, J. Carlson, C. Kadie, T. Bhattacharya, C. Chui, J. Szinger, T. Mo, R. S. Hogg, J. S. Montaner, N. Frahm, C. Brander, B. D. Walker, and P. R. Harrigan. 2007. Evidence of differential HLA class I-mediated viral evolution in functional and accessory/regulatory genes of HIV-1. PLoS Pathog. 3:e94.
6. Dale, C. J., R. De Rose, I. Stratov, S. Chea, D. C. Montefiori, S. Thomson, I. A. Ramshaw, B. E. Coupar, D. B. Boyle, M. Law, and S. J. Kent. 2004. Efficacy of DNA and fowlpox virus priming/boosting vaccines for simian/human immunodeficiency virus. J. Virol. 78:13819-13828.
7. Davenport, M. P., L. Zhang, J. W. Shiver, D. R. Casmiro, R. M. Ribeiro, and A. S. Perelson. 2006. Influence of peak viral load on the extent of CD4 + T-cell depletion in simian HIV infection. J. Acquir. Immune Defic. Syndr. 41:259-265.
8. De Rose, R., C. J. Batten, M. Z. Smith, C. S. Fernandez, V. Peut, S. Thomson, I. A. Ramshaw, B. E. Coupar, D. B. Boyle, V. Venturi, M. P. Davenport, and S. J. Kent. 2007. Comparative efficacy of subtype AE simian-human immunodeficiency virus priming and boosting vaccines in pigtail macaques. J. Virol. 81:292-300.
9. Evans, D. T., D. H. O'Connor, P. Jing, J. L. Dzuris, J. Sidney, J. da Silva, T. M. Allen, H. Horton, J. E. Venham, R. A. Rudersdorf, T. Vogel, C. D. Pauza, R. E. Bontrop, R. DeMars, A. Sette, A. L. Hughes, and D. I. Watkins. 1999. Virus-specific cytotoxic T-lymphocytc responses select for amino-acid variation in simian immunodeficiency virus Env and Nef. Nat. Med. 5:1270-1276.
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. Vaccine-induced 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, H. O'Connor, D. 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. Frater, A. J., H. Brown, A. Oxenius, H. F. Gunthard, B. Hirschel, N. Robinson, A. J. Leslie, R. Payne, H. Crawford, A. Prendergast, C. Brander, P. Kiepiela, B. D. Walker, P. J. Goulder, A. McLean, and R. E. Phillips. 2007. Effective T-cell responses select human immunodeficiency virus mutants and slow disease progression. J. Virol. 81:6742-6751.
13. Frater, A. J., C. T. Edwards, N. McCarthy, J. Fox, H. Brown, A. Milicic, N. Mackie, T. Pillay, J. W. Drijfhout, S. Dustan, J. R. Clarke, E. C. Holmes, H. T. Zhang, K. Pfafferott, P. J. Goulder, M. O. McClure, J. Weber, R. E. Phillips, and S. Fidler. 2006. Passive sexual transmission of human immunodeficiency virus type 1 variants and adaptation in new hosts. J. Virol. 80:7226-7234.
14. 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.
15. Friedrich, T. C., C. A. Frye, L. J. Yant, D. H. O'Connor, N. A. Kriewaldt, M. Benson, L. Vojnov, E. J. Dodds, C. Cullen, R. Rudersdorf, A. L. Hughes, N. Wilson, and D. I. Watkins. 2004. Extraepitopic compensatory substitutions partially restore fitness to simian immunodeficiency virus variants that escape from an immunodominant cytotoxic-T-lymphocyte response. J. Virol. 78:2581-2585.
16. Ganusov, V. V., and R. J. De Boer. 2006. Estimating costs and benefits of CTL escape mutations in SIV/HIV infection. PLoS Comput. Biol. 2:e24.
17. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4:630-640.
18. Goulder, P. J. R., R. E. Phillips, R. A. 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 T-lymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217.
19. Harcourt, G. C., S. Garrard, M. P. Davenport, A. Edwards, and R. E. Phillips. 1998. HIV-1 variation diminishes CD4 T lymphocyte recognition. J. Exp. Med. 188:1785-1793.
20. Jones, N. A., X. Wei, D. R. Flower, M. Wong, F. Michor, M. S. Saag, B. H. Hahn, M. A. Nowak, G. M. Shaw, and P. Borrow. 2004. Determinants of human immunodeficiency virus type 1 escape from the primary CD8+ cytotoxic T lymphocyte response. J. Exp. Med. 200:1243-1256.
21. Kent, S. J., C. S. Fernandez, C. Jane Dale, and M. P. Davenport. 2005. Reversion of immune escape HIV variants upon transmission: insights into effective viral immunity. Trends Microbiol. 13:243-246.
22. 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. S. 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.
23. 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 for macaques. J. Virol. 81:5418-5422.
24. Loh, L., J. Petravic, C. J. Batten, M. P. Davenport, and S. J. Kent. Vaccination and timing influence SIV immune escape viral dynamics in vivo. PLoS Pathog. 4:e12.
25. + T cells from the dynamics of viral immune escape. J. Virol. 81:11982-11991.
26. Marée, A. F., W. Keulen, C. A. Boucher, and R. J. De Boer. 2000. Estimating relative fitness in viral competition experiments. J. Virol. 74:11067-11072.
27. Martinez-Picado, J., J. G. Prado, E. E. Fry, K. Pfafferott, A. Leslie, S. Chetty, C. Thobakgale, I. Honeyborne, H. Crawford, P. Matthews, T. Pillay, C. Rousseau, J. I. Mullins, C. Brander, B. D. Walker, D. I. Stuart, P. Kiepiela, and P. Goulder. 2006. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J. Virol. 80:3617-3623.
28. Moore, C. B., M. John, I. R. James, F. T. Christiansen, C. S. Witt, and S. A. Mallal. 2002. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296:1439-1443.
29. Nature. 2007. HIV vaccine failure prompts Merck to halt trial. Nature 449:390.
30. Nishimura, Y., T. Igarashi, O. K. Donau, A. Buckler-White, C. Buckler, B. A. Lafont, R. M. Goeken, S. Goldstein, V. M. Hirsch, and M. A. Martin. 2004. Highly pathogenic SHIVs and SIVs target different CD4+ T cell subsets in rhesus monkeys, explaining their divergent clinical courses. Proc. Natl. Acad. Sci. USA 101:12324-12329.
31. Nowak, M. A., A. L. Lloyd, G. M. Vasquez, T. A. Wiltrout, L. M. Wahl, N. Bischofberger, J. Williams, A. Kinter, A. S. Fauci, V. M. Hirsch, and J. D. Lifson. 1997. Viral dynamics of primary viremia and antiretroviral therapy in simian immunodeficiency virus infection. J. Virol. 71:7518-7525.
32. 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. M. Bangham, C. R. Rizza, and A. J. McMichael. 1991. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 354:453-459.
33. Ribeiro, R. M., M. D. Hazenberg, A. S. Perelson, and M. P. Davenport. 2006. Naive and memory cell turnover as drivers of CCR5-to-CXCR4 tropism switch in human immunodeficiency virus type 1: implications for therapy. J. Virol. 80:802-809.
34. 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.
35. Schwartz, E. J., A. U. Neumann, A. V. Teixeira, L. A. Bruggeman, J. Rappaport, A. S. Perelson, and P. E. Klotman. 2002. Effect of target cell availability on HIV-1 production in vitro. AIDS 16:341-345.
36. 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.
37. mac25I in the gut. J. Virol. 81:8025-8029.
38. + T-cell responses following acute HIV-1 infection. J. Virol. 76:8690-8701.
39. Zhang, Z. Q., S. W. Wietgrefe, Q. Li, M. D. Shore, L. Duan, C. Reilly, J. D. Lifson, and A. T. Haase. 2004. Roles of substrate availability and infection of resting and activated CD4+ T cells in transmission and acute simian immunodeficiency virus infection. Proc. Natl. Acad. Sci. USA 101:5640-5645.