Rapid viral escape at an immunodominant simian-human immunodeficiency virus cytotoxic T-lymphocyte epitope exacts a dramatic fitness cost

Journal of Virology

Volumn 79, Issue 9, 2005, Pages 5721-5731

  Fernandez, Caroline S ^a   Stratov, Ivan ^a   De Rose, Robert ^a   Walsh, Katrina ^a   Dale, C Jane ^a   Smith, Miranda Z ^a   Agy, Michael B ^b   Hu, Shiu Lok ^b   Krebs, Kendall ^c   Watkins, David I ^c   O'Connor, David H ^c   Davenport, Miles P ^d   Kent, Stephen J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

^d PRINCE OF WALES HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE;

ARTICLE; CYTOTOXIC LYMPHOCYTE; GENE MAPPING; GENE MUTATION; GENE SEQUENCE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MACACA; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS MUTANT; VIRUS TRANSMISSION;

ANIMALS; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; GENE PRODUCTS, GAG; IMMUNODOMINANT EPITOPES; LENTIVIRUS INFECTIONS; LENTIVIRUSES, PRIMATE; MACACA NEMESTRINA; MUTATION; REASSORTANT VIRUSES; T-LYMPHOCYTES, CYTOTOXIC; VIRULENCE;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA NEMESTRINA; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 20244386270     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.9.5721-5731.2005     Document Type: Article

References (32)

1. 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.
2. Arguello, J. R., A. M. Little, E. Bohan, J. M. Goldman, S. G. Marsh, and J. A. Madrigal. 1998. High resolution HLA class I typing by reference strand mediated conformation analysis (RSCA). Tissue Antigens 52:57-66.
3. Barouch, D. H., S. Santra, J. E. Schmitz, M. J. Kuroda, T. M. Fu, W. Wagner, M. Bilska, A. Craiu, X. X. Zheng, G. R. Krivulka, K. Beaudry, M. A. Lifton, C. E. Nickerson, W. L. Trigona, K. Punt, D. C. Freed, L. Guan, S. Dubey, D. Casimiro, A. Simon, M. E. Davies, M. Chastain, T. B. Strom, R. S. Gelman, D. C. Montefiori, and M. G. Lewis. 2000. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290:486-492.
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 269:1887-1893.
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. Cao, J., J. McNevin, U. Malhotra, and M. J. McElrath. 2003. Evolution of CD8+ T cell immunity and viral escape following acute HIV-1 infection. J. Immunol. 171:3837-3846.
7. Dale, C. J., R. De Rose, I. Stratov, S. Chea, D. Montefiori, S. A. 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.
8. Dale, C. J., X. S. Liu, R. De Rose, D. F. Purcell, J. Andersen, Y. Xu, G. R. Leggatt, I. H. Frazer, and S. J. Kent. 2002. Chimeric human papilloma virus-simian/human immunodeficiency virus virus-like-particle vaccines: immunogenicity and protective efficacy in macaques. Virology 301:176-187.
9. 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.
10. 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.
11. Goulder, P. J., C. Brander, Y. Tang, C. Tremblay, R. A. Colbert, M. M. Addo, E. S. Rosenberg, T. Nguyen, R. Allen, A. Trocha, M. Altfeld, S. He, M. Bunce, R. Funkhouser, S. I. Pelton, S. K. Burchett, K. McIntosh, B. T. Korber, and B. D. Walker. 2001. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412:334-338.
12. Harouse, J. M., A. Gettie, T. Eshetu, R. C. Tan, R. Bohm, J. Blanchard, G. Baskin, and C. Cheng-Mayer. 2001. Mucosal transmission and induction of simian AIDS by CCR5-specific simian/human immunodeficiency virus SHIV(SF162P3). J. Virol. 75:1990-1995.
13. Harouse, J. M., A. Gettie, R. C. Tan, J. Blanchard, and C. Cheng-Mayer. 1999. Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. Science 284:816-819.
14. Kelleher, A. D., C. Long, E. C. Holmes, R. L. Allen, J. Wilson, C. Conlon, C. Workman, S. Shaunak, K. Olson, P. Goulder, C. Brander, G. Ogg, J. S. Sullivan, W. Dyer, I. Jones, A. J. McMichael, S. Rowland-Jones, and R. E. Phillips. 2001. Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J. Exp. Med. 193:375-386.
15. Kent, S. J., A. Zhao, S. Best, J. D. Chandler, D. B. Boyle, and I. A. Ramshaw. 1998. Enhanced T cell immunogenicity and protective efficacy of a human immunodeficiency virus type 1 vaccine regimen consisting of consecutive priming with DNA and boosting with recombinant fowlpox virus. J. Virol. 72:10180-10188.
16. Koup, R. A., J. T. Safrit, Y. Cao, C. A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D. D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
17. 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.
18. Lu, Y., M. S. Salvato, C. D. Pauza, J. Li, J. Sodroski, K. Manson, M. Wyand, N. Letvin, S. Jenkins, N. Touzjian, C. Chutkowski, N. Kushner, M. LeFalle, L. G. Payne, and B. Roberts. 1996. Utility of SHIV for testing HIV-1 vaccine candidates in macaques. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 12:99-106.
19. Maecker, H. T., H. S. Dunn, M. A. Suni, E. Khatamzas, C. J. Pitcher, T. Bunde, N. Persaud, W. Trigona, T. M. Fu, E. Sinclair, B. M. Bredt, J. M. McCune, V. C. Maino, F. Kern, and L. J. Picker. 2001. Use of overlapping peptide mixtures as antigens for cytokine flow cytometry. J. Immunol. Methods 255:27-40.
20. McMichael, A., and P. Klenerman. 2002. HIV/AIDS. HLA leaves its footprints on HIV. Science 296:1410-1411.
21. 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.
22. O'Connor, D. H., T. M. Allen, T. U. Vogel, P. Jing, I. P. DeSouza, E. Dodds, E. J. Dunphy, C. Melsaether, B. Mothe, H. Yamamoto, H. Horton, N. Wilson, A. L. Hughes, and D. I. Watkins. 2002. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat. Med. 8:493-499.
23. O'Connor, D. H., B. R. Mothe, J. T. Weinfurter, S. Fuenger, W. M. Rehrauer, P. Jing, R. R. Rudersdorf, M. E. Liebl, K. Krebs, J. Vasquez, E. Dodds, J. Loffredo, S. Martin, A. B. McDermott, T. M. Allen, C. Wang, G. G. Doxiadis, D. C. Montefiori, A. Hughes, D. R. Burton, D. B. Allison, S. M. Wolinsky, R. Bontrop, L. J. Picker, and D. I. Watkins. 2003. Major histocompatibility complex class I alleles associated with slow simian immunodeficiency virus disease progression bind epitopes recognized by dominant acute-phase cytotoxic-T-lymphocyte responses. J. Virol. 77:9029-9040.
24. Pal, R., D. Venzon, N. L. Letvin, S. Santra, D. C. Montefiori, N. R. Miller, E. Tryniszewska, M. G. Lewis, T. C. VanCott, V. Hirsch, R. Woodward, A. Gibson, M. Grace, E. Dobratz, P. D. Markham, Z. Hel, J. Nacsa, M. Klein, J. Tartaglia, and G. Franchini. 2002. ALVAC-SIV-gag-pol-env-based vaccination and macaque major histocompatibility complex class I (A*01) delay simian immunodeficiency virus SIVmac-induced immunodeficiency. J. Virol. 76:292-302.
25. 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.
26. 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.
27. Russell, N. D., M. G. Hudgens, R. Ha, C. Havenar-Daughton, and M. J. McElrath. 2003. Moving to human immunodeficiency virus type 1 vaccine efficacy trials: defining T cell responses as potential correlates of immunity. J. Infect. Dis. 187:226-242.
28. Schmitz, J. E., M. J. Kuroda, S. Santra, V. G. Sasseville, M. A. Simon, M. A. Lifton, P. Racz, K. Tenner-Racz, M. Dalesandro, B. J. Scallon, J. Ghrayeb, M. A. Forman, D. C. Montefiori, E. P. Rieber, N. L. Letvin, and K. A. Reimann. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283:857-860.
29. Smith, M. Z., C. J. Dale, R. De Rose, I. Stratov, C. S. Fernandez, A. G. Brooks, J. T. Weinfurter, K. Krebs, C. Riek, D. I. Watkins, D. H. O'Connor, and S. J. Kent. 2005. Analysis of pigtail macaque major histocompatibility complex class I molecules presenting immunodominant simian immunodeficiency virus epitopes. J. Virol. 79:684-695.
30. Thompson, J., S. L. Hu, L. Kuller, B. Travis, W. R. Morton, and M. B. Agy. 1996. SHIVIIIB infection of Macaca nemestrina: determination of a macaque infectious dose, 11th Int. Conf. AIDS, abstr. We.A. 142, p. 5.
31. Thompson, J. L., D. Anderson, J. Ranchalis, L. Kuller, H. Mack, and M. B. Agy. 2000. Intravaginal titration of the acutely pathogenic SHIV229 in Macaca nemestrina. J. Med. Primatol. 29:295.
32. 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.