Protective HLA class I alleles that restrict acute-phase CD8+ T-cell responses are associated with viral escape mutations located in highly conserved regions of human immunodeficiency virus type 1

Journal of Virology

Volumn 83, Issue 4, 2009, Pages 1845-1855

  Wang, Yaoyu E ^a   Li, Bin ^a   Carlson, Jonathan M ^b   Streeck, Hendrik ^a   Gladden, Adrianne D ^a   Goodman, Robert ^a   Schneidewind, Arne ^a   Power, Karen A ^a   Toth, Ildiko ^a   Frahm, Nicole ^a   Alter, Galit ^a   Brander, Christian ^a,e   Carrington, Mary ^c   Walker, Bruce D ^a,d   Altfeld, Marcus ^a   Heckerman, David ^b   Allen, Todd M ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MICROSOFT RESEARCH   (United States)

^c SAIC FREDERICK INC   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; GAG PROTEIN; NEF PROTEIN; POL PROTEIN;

ACUTE PHASE RESPONSE; ALLELE; ARTICLE; CD8+ T LYMPHOCYTE; CELL MUTANT; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE LOCATION; GENE NUMBER; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC CORRELATION; GENOME ANALYSIS; HLA SYSTEM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGENETICS; LYMPHOCYTE SUBPOPULATION; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERTANT; VIRUS GENOME; VIRUS MUTATION; VIRUS REPLICATION;

CD8-POSITIVE T-LYMPHOCYTES; EPITOPES, T-LYMPHOCYTE; HIV CORE PROTEIN P24; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; POL GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; SEQUENCE ANALYSIS, DNA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 59649108841     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01061-08     Document Type: Article

References (85)

1. + T effector cells are more frequently detectable in controlled than in progressive HIV-1 infection. PLoS ONE 2:e321.
2. Addo, M. M., X. G. Yu, A. Rathod, D. Cohen, R. L. Eldridge, D. Strick, M. N. Johnston, C. Corcoran, A. G. Wurcel, C. A. Fitzpatrick, M. E. Feeney, W. R. Rodriguez, N. Basgoz, R. Draenert, D. R. Stone, C. Brander, P. J. Goulder, E. S. Rosenberg, M. Altfeld, and B. D. Walker. 2003. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J. Virol. 77:2081-2092.
3. + T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J. Virol. 79:13239-13249.
4. 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.
5. 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.
6. Altfeld, M., and T. M. Allen. 2006. Hitting HIV where it hurts: an alternative approach to HIV vaccine design. Trends Immunol. 27:504-510.
7. + T-cell responses containing replication of the primary virus. Nature 420:434-439.
8. + T cell response against HIV-1. PLoS Med. 3:e403.
9. Anonymous. 2007. HIV vaccine failure prompts Merck to halt trial. Nature 449:390.
10. Barouch, D. H., J. Kunstman, J. Glowczwskie, K. J. Kunstman, M. A. Egan, F. W. Peyerl, S. Santra, M. J. Kuroda, J. E. Schmitz, K. Beaudry, G. R. Krivulka, M. A. Lifton, D. A. Gorgone, S. M. Wolinsky, and N. L. Letvin. 2003. Viral escape from dominant simian immunodeficiency virus epitope-specific cytotoxic T lymphocytes in DNA-vaccinated rhesus monkeys. J. Virol. 77:7367-7375.
11. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57:289.
12. Bhattacharya, T., M. Daniels, D. Heckerman, B. Foley, N. Frahm, C. Kadie, J. Carlson, K. Yusim, B. McMahon, B. Gaschen, S. Mallal, J. I. Mullins, D. C. Nickle, J. Herbeck, C. Rousseau, G. H. Learn, T. Miura, C. Brander, B. Walker, and B. Korber. 2007. Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 315:1583-1586.
13. Borrow, P., H. Lewicki, X. Wei, M. S. Horwitz, N. Peffer, H. Meyers, J. A. Nelson, J. E. Gairin, B. H. Hahn, M. B. Oldstone, and G. M. Shaw. 1997. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3:205-211.
14. Boutwell, C. L., and M. Essex. 2007. Identification of HLA class I-associated amino acid polymorphisms in the HIV-1C proteome. AIDS Res. Hum. Retrovir. 23:165-174.
15. 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.
16. 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.
17. Caffrey, D. R., P. H. Dana, V. Mathur, M. Ocano, E. J. Hong, Y. E. Wang, S. Somaroo, B. E. Caffrey, S. Potluri, and E. S. Huang. 2007. PFAAT version 2.0: a tool for editing, annotating, and analyzing multiple sequence alignments. BMC Bioinform. 8:381.
18. Campbell, T. B., N. S. Shulman, S. C. Johnson, A. R. Zolopa, R. K. Young, L. Bushman, C. V. Fletcher, E. R. Lanier, T. C. Merigan, and D. R. Kuritzkes. 2005. Antiviral activity of lamivudine in salvage therapy for multidrug-resistant HIV-1 infection. Clin. Infect. Dis. 41:236-242.
19. Carlson, J., C. Kadie, S. Mallal, and D. Heckerman. 2007. Leveraging hierarchical population structure in discrete association studies. PLoS ONE 2:e591.
20. Carrington, M., G. W. Nelson, M. P. Martin, T. Kissner, D. Vlahov, J. J. Goedert, R. Kaslow, S. Buchbinder, K. Hoots, and S. J. O'Brien. 1999. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283:1748-1752.
21. Casimiro, D. R., F. Wang, W. A. Schleif, X. Liang, Z. Q. Zhang, T. W. Tobery, M. E. Davies, A. B. McDermott, D. H. O'Connor, A. Fridman, A. Bagchi, L. G. Tussey, A. J. Bett, A. C. Finnefrock, T. M. Fu, A. Tang, K. A. Wilson, M. Chen, H. C. Perry, G. J. Heidecker, D. C. Freed, A. Carella, K. S. Punt, K. J. Sykes, L. Huang, V. I. Ausensi, M. Bachinsky, U. Sadasivan-Nair, D. I. Watkins, E. A. Emini, and J. W. Shiver. 2005. Attenuation of simian immunodeficiency virus SIVmac239 infection by prophylactic immunization with DNA and recombinant adenoviral vaccine vectors expressing Gag. J. Virol. 79:15547-15555.
22. Cook, R. D. 2000. Detection of influential observation in linear regression. Technometrics 42:65-68.
23. Crawford, H., J. G. Prado, A. Leslie, S. Hue, I. Honeyborne, S. Reddy, M. van der Stok, Z. Mncube, C. Brander, C. Rousseau, J. I. Mullins, R. Kaslow, P. Goepfert, S. Allen, E. Hunter, J. Mulenga, P. Kiepiela, B. D. Walker, and P. J. Goulder. 2007. Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLAB* 5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J. Virol. 81:8346-8351.
24. de Sorrentino, A. H., K. Marinic, P. Motta, A. Sorrentino, R. Lopez, and E. Illiovich. 2000. HLA class I alleles associated with susceptibility or resistance to human immunodeficiency virus type 1 infection among a population in Chaco Province, Argentina. J. Infect. Dis. 182:1523-1526.
25. + T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J. Virol. 76:2298-2305.
26. Emu, B., E. Sinclair, H. Hatano, A. Ferre, B. Shacklett, J. N. Martin, J. M. McCune, and S. G. Deeks. 2008. HLA class I-restricted T cell responses may contribute to the control of HIV infection, but such responses are not always necessary for long-term virus control. J. Virol. 82:5398-5407.
27. Frahm, N., D. E. Kaufmann, K. Yusim, M. Muldoon, C. Kesmir, C. H. Linde, W. Fischer, T. M. Allen, B. Li, B. H. McMahon, K. L. Faircloth, H. S. Hewitt, E. W. Mackey, T. Miura, A. Khatri, S. Wolinsky, A. McMichael, R. K. Funkhouser, B. D. Walker, C. Brander, and B. T. Korber. 2007. Increased sequence diversity coverage improves detection of HIV-specific T-cell responses. J. Immunol. 179:6638-6650.
28. Frahm, N., B. T. Korber, C. M. Adams, J. J. Szinger, R. Draenert, M. M. Addo, M. E. Feeney, K. Yusim, K. Sango, N. V. Brown, D. SenGupta, A. Piechocka-Trocha, T. Simonis, F. M. Marincola, A. G. Wurcel, D. R. Stone, C. J. Russell, P. Adolf, D. Cohen, T. Roach, A. St. John, A. Khatri, K. Davis, J. Mullins, P. J. Goulder, B. D. Walker, and C. Brander. 2004. Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J. Virol. 78:2187-2200.
29. 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.
30. 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.
31. Friedrich, T. C., A. B. McDermott, M. R. Reynolds, S. Piaskowski, S. Fuenger, I. P. De Souza, R. Rudersdorf, C. Cullen, L. J. Yant, L. Vojnov, J. Stephany, S. Martin, D. H. O'Connor, N. Wilson, and D. I. Watkins. 2004. Consequences of cytotoxic T-lymphocyte escape: common escape mutations in simian immunodeficiency virus are poorly recognized in naive hosts. J. Virol. 78:10064-10073.
32. Gao, X., A. Bashirova, A. K. Iversen, J. Phair, J. J. Goedert, S. Buchbinder, K. Hoots, D. Vlahov, M. Altfeld, S. J. O'Brien, and M. Carrington. 2005. AIDS restriction HLA allotypes target distinct intervals of HIV-1 pathogenesis. Nat. Med. 11:1290-1292.
33. 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.
34. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4:630-640.
35. Hadi, A. S., and J. S. Simonoff. 1993. Procedures for the identification of multiple outliers in linear models. J. Am. Stat. Assoc. 88:1264-1272.
36. Heckerman, D., C. Kadie, and J. Listgarten. 2007. Leveraging information across HLA alleles/supertypes improves epitope prediction. J. Comput. Biol. 14:736-746.
37. Hu, Z., J. Mellor, J. Wu, M. Kanehisa, J. M. Stuart, and C. DeLisi. 2007. Towards zoomable multidimensional maps of the cell. Nat. Biotechnol. 25:547-554.
38. Hu, Z., D. M. Ng, T. Yamada, C. Chen, S. Kawashima, J. Mellor, B. Linghu, M. Kanehisa, J. M. Stuart, and C. DeLisi. 2007. VisANT 3.0: new modules for pathway visualization, editing, prediction and construction. Nucleic Acids Res. 35:W625-W632.
39. Johnston, M. I., and A. S. Fauci. 2007. An HIV vaccine-evolving concepts. N. Engl. J. Med. 356:2073-2081.
40. 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.
41. 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.
42. Kiepiela, P., A. J. Leslie, I. Honeyborne, D. Ramduth, C. Thobakgale, S. Chetty, P. Rathnavalu, C. Moore, K. J. Pfafferott, L. Hilton, P. Zimbwa, S. Moore, T. Allen, C. Brander, M. M. Addo, M. Altfeld, I. James, S. Mallal, M. Bunce, L. D. Barber, J. Szinger, C. Day, P. Klenerman, J. Mullins, B. Korber, H. M. Coovadia, B. D. Walker, and P. J. Goulder. 2004. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432:769-775.
43. + T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
44. Koff, W. C., P. R. Johnson, D. I. Watkins, D. R. Burton, J. D. Lifson, K. J. Hasenkrug, A. B. McDermott, A. Schultz, T. J. Zamb, R. Boyle, and R. C. Desrosiers. 2006. HIV vaccine design: insights from live attenuated SIV vaccines. Nat. Immunol. 7:19-23.
45. 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.
46. Kuiken, C., B. Korber, and R. W. Shafer. 2003. HIV sequence databases. AIDS Rev. 5:52-61.
47. Kuntzen, T., J. Timm, A. Berical, L. L. Lewis-Ximenez, A. Jones, B. Nolan, J. Schulze Zur Wiesch, B. Li, A. Schneidewind, A. Y. Kim, R. T. Chung, G. M. Lauer, and T. M. Allen. 2007. Viral sequence evolution in acute hepatitis C virus infection. J. Virol. 81:11658-11668.
48. 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.
49. Letvin, N. L., J. E. Schmitz, H. L. Jordan, A. Seth, V. M. Hirsch, K. A. Reimann, and M. J. Kuroda. 1999. Cytotoxic T lymphocytes specific for the simian immunodeficiency virus. Immunol. Rev. 170:127-134.
50. Li, B., A. D. Gladden, M. Altfeld, J. M. Kaldor, D. A. Cooper, A. D. Kelleher, and T. M. Allen. 2007. Rapid reversion of sequence polymorphisms dominates early human immunodeficiency virus type 1 evolution. J. Virol. 81:193-201.
51. 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.
52. + immunodominance may influence the ability of Mamu-B*08- positive macaques to naturally control simian immunodeficiency virus SIVmac239 replication. J. Virol. 82:1723-1738.
53. Loffredo, J. T., T. C. Friedrich, E. J. Leon, J. J. Stephany, D. S. Rodrigues, S. P. Spencer, A. T. Bean, D. R. Beal, B. J. Burwitz, R. A. Rudersdorf, L. T. Wallace, S. M. Piaskowski, G. E. May, J. Sidney, E. Gostick, N. A. Wilson, D. A. Price, E. G. Kallas, H. Piontkivska, A. L. Hughes, A. Sette, and D. I. Watkins. 2007. CD8 T cells from SIV elite controller macaques recognize Mamu-B*08-bound epitopes and select for widespread viral variation. PLoS ONE 2:e1152.
54. Maness, N. J., L. J. Yant, C. Chung, J. T. Loffredo, T. C. Friedrich, S. M. Piaskowski, J. Furlott, G. E. May, T. Soma, E. J. León, N. A. Wilson, H. Piontkivska, A. L. Hughes, J. Sidney, A. Sette, and D. I. Watkins. 2008. Comprehensive immunological evaluation reveals surprisingly few differences between elite controller and progressor Mamu-B*17- positive SIV-infected rhesus macaques. J. Virol. 82:5245-5254.
55. 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.
56. + T cells: correlation with viral load. J. Virol. 78:3233-3243.
57. Mellors, J. W., J. B. Margolick, J. P. Phair, C. R. Rinaldo, R. Detels, L. P. Jacobson, and A. Munoz. 2007. Prognostic value of HIV-1 RNA, CD4 cell count, and CD4 Cell count slope for progression to AIDS and death in untreated HIV-1 infection. JAMA 297:2349-2350.
58. 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.
59. Navis, M., I. Schellens, D. van Baarle, J. Borghans, P. van Swieten, F. Miedema, N. Kootstra, and H. Schuitemaker. 2007. Viral replication capacity as a correlate of HLA B57/B5801-associated nonprogressive HIV-1 infection. J. Immunol. 179:3133-3143.
60. Novitsky, V., P. Gilbert, T. Peter, M. F. McLane, S. Gaolekwe, N. Rybak, I. Thior, T. Ndung'u, R. Marlink, T. H. Lee, and M. Essex. 2003. Association between virus-specific T-cell responses and plasma viral load in human immunodeficiency virus type 1 subtype C infection. J. Virol. 77:882-890.
61. O'Brien, S. J., X. Gao, and M. Carrington. 2001. HLA and AIDS: a cautionary tale. Trends Mol. Med. 7:379-381.
62. 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.
63. 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.
64. Pereyra, F., M. M. Addo, D. E. Kaufmann, Y. Liu, T. Miura, A. Rathod, B. Baker, A. Trocha, R. Rosenberg, E. Mackey, P. Ueda, Z. Lu, D. Cohen, T. Wrin, C. J. Petropoulos, E. S. Rosenberg, and B. D. Walker. 2008. Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. J. Infect. Dis. 197:563-571.
65. Poon, A. F., S. L. Kosakovsky Pond, P. Bennett, D. D. Richman, A. J. Leigh Brown, and S. D. Frost. 2007. Adaptation to human populations is revealed by within-host polymorphisms in HIV-1 and hepatitis C virus. PLoS Pathog. 3:e45.
66. Price, D. A., P. J. Goulder, P. Klenerman, A. K. Sewell, P. J. Easterbrook, M. Troop, C. R. Bangham, and R. E. Phillips. 1997. Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc. Natl. Acad. Sci. USA 94:1890-1895.
67. Reimann, K. A., K. Tenner-Racz, P. Racz, D. C. Montefiori, Y. Yasutomi, W. Lin, B. J. Ransil, and N. L. Letvin. 1994. Immunopathogenic events in acute infection of rhesus monkeys with simian immunodeficiency virus of macaques. J. Virol. 68:2362-2370.
68. Rohowsky-Kochan, C., J. Skurnick, D. Molinaro, and D. Louria. 1998. HLA antigens associated with susceptibility/resistance to HIV-1 infection. Hum. Immunol. 59:802-815.
69. Rousseau, C. M., M. G. Daniels, J. M. Carlson, C. Kadie, H. Crawford, A. Prendergast, P. Matthews, R. Payne, M. Rolland, D. N. Raugi, B. S. Maust, G. H. Learn, D. C. Nickle, H. Coovadia, T. Ndung'u, N. Frahm, C. Brander, B. D. Walker, P. J. R. Goulder, T. Bhattacharya, D. E. Heckerman, B. T. Korber, and J. I. Mullins. 2008. HLA class I-driven evolution of human immunodeficiency virus type 1 subtype C proteome: immune escape and viral load. J. Virol. 82:6364-6446.
70. + T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J. Immunol. 178:2746-2754.
71. Salminen, M. O., B. Johansson, A. Sonnerborg, S. Ayehunie, D. Gotte, P. Leinikki, D. S. Burke, and F. E. McCutchan. 1996. Full-length sequence of an ethiopian human immunodeficiency virus type 1 (HIV-1) isolate of genetic subtype C. AIDS Res. Hum. Retrovir. 12:1329-1339.
72. Salminen, M. O., C. Koch, E. Sanders-Buell, P. K. Ehrenberg, N. L. Michael, J. K. Carr, D. S. Burke, and F. E. McCutchan. 1995. Recovery of virtually full-length HIV-1 provirus of diverse subtypes from primary virus cultures using the polymerase chain reaction. Virology 213:80-86.
73. Schneidewind, A., M. A. Brockman, J. Sidney, Y. E. Wang, H. Chen, T. J. Suscovich, B. Li, R. I. Adam, R. L. Allgaier, B. R. Mothé, T. Kuntzen, C. Oniangue-Ndza, A. Trocha, X. G. Yu, C. Brander, A. Sette, B. D. Walker, and T. M. Allen. 2008. Structural and functional constraints limit options for cytotoxic T-lymphocyte escape in the immunodominant HLA-B27-restricted epitope in human immunodeficiency virus type 1 capsid. J. Virol. 82:5594-5605.
74. 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.
75. Sekaly, R. P. 2008. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development? J. Exp. Med. 205:7-12.
76. Storey, J. D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100:9440-9445.
77. + T cells during primary human immunodeficiency virus type 1 infection in individuals expressing protective HLA class I alleles. J. Virol. 81:7725-7731.
78. Timm, J., B. Li, M. G. Daniels, T. Bhattacharya, L. L. Reyor, R. Allgaier, T. Kuntzen, W. Fischer, B. E. Nolan, J. Duncan, J. Schulze zur Wiesch, A. Y. Kim, N. Frahm, C. Brander, R. T. Chung, G. M. Lauer, B. T. Korber, and T. M. Allen. 2007. Human leukocyte antigen-associated sequence polymorphisms in hepatitis C virus reveal reproducible immune responses and constraints on viral evolution. Hepatology 46:339-349.
79. Wang, Y. E., and C. DeLisi. 2006. Inferring protein-protein interactions in viral proteins by co-evolution of conserved side chains. Genome Inform. 17:23-35.
80. Wheeler, D. L., T. Barrett, D. A. Benson, S. H. Bryant, K. Canese, V. Chetvernin, D. M. Church, M. DiCuccio, R. Edgar, S. Federhen, L. Y. Geer, W. Helmberg, Y. Kapustin, D. L. Kenton, O. Khovayko, D. J. Lipman, T. L. Madden, D. R. Maglott, J. Ostell, K. D. Pruitt, G. D. Schuler, L. M. Schriml, E. Sequeira, S. T. Sherry, K. Sirotkin, A. Souvorov, G. Starchenko, T. O. Suzek, R. Tatusov, T. A. Tatusova, L. Wagner, and E. Yaschenko. 2006. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 34:D173-D180.
81. Wilson, N. A., J. Reed, G. S. Napoe, S. Piaskowski, A. Szymanski, J. Furlott, E. J. Gonzalez, L. J. Yant, N. J. Maness, G. E. May, T. Soma, M. R. Reynolds, E. Rakasz, R. Rudersdorf, A. B. McDermott, D. H. O'Connor, T. C. Friedrich, D. B. Allison, A. Patki, L. J. Picker, D. R. Burton, J. Lin, L. Huang, D. Patel, G. Heindecker, J. Fan, M. Citron, M. Horton, F. Wang, X. Liang, J. W. Shiver, D. R. Casimiro, and D. I. Watkins. 2006. Vaccine-induced cellular immune responses reduce plasma viral concentrations after repeated low-dose challenge with pathogenic simian immunodeficiency virus SIVmac239. J. Virol. 80:5875-5885.
82. Yang, O. O. 2008. Aiming for successful vaccine-induced HIV-1-specific cytotoxic T lymphocytes. AIDS 22:325-331.
83. Yant, L. J., T. C. Friedrich, R. C. Johnson, G. E. May, N. J. Maness, A. M. Enz, J. D. Lifson, D. H. O'Connor, M. Carrington, and D. I. Watkins. 2006. The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J. Virol. 80:5074-5077.
84. + T-cell responses following acute HIV-1 infection. J. Virol. 76:8690-8701.
85. Zuñiga, R., A. Lucchetti, P. Galvan, S. Sanchez, C. Sanchez, A. Hernandez, H. Sanchez, N. Frahm, C. H. Linde, H. S. Hewitt, W. Hildebrand, M. Altfeld, T. M. Allen, B. D. Walker, B. T. Korber, T. Leitner, J. Sanchez, and C. Brander. 2006. Relative dominance of Gag p24-specific cytotoxic T lymphocytes is associated with human immunodeficiency virus control. J. Virol. 80:3122-3125.