Chapter 1 HLA-Mediated Control of HIV and HIV Adaptation to HLA

Advances in Parasitology

Volumn 68, Issue , 2009, Pages 1-20

  Payne, Rebecca P ^a   Matthews, Philippa C ^a   Prado, Julia G ^a   Goulder, Philip J R ^a,b,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; GAG PROTEIN; HLA ANTIGEN CLASS 1; HLA B ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; HLA ANTIGEN;

ADAPTATION; CD8+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; DISEASE CONTROL; DISEASE COURSE; DNA FOOTPRINTING; EVOLUTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HLA SYSTEM; HOST PATHOGEN INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; VERTICAL TRANSMISSION; VIREMIA; VIRUS CELL INTERACTION; VIRUS LOAD; VIRUS MUTATION; VIRUS REPLICATION; VIRUS TRANSMISSION; ARTICLE; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN FOOTPRINTING; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS;

ADAPTATION, PHYSIOLOGICAL; EVOLUTION; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HLA ANTIGENS; HUMANS; PROTEIN FOOTPRINTING; T-LYMPHOCYTES, CYTOTOXIC; VIREMIA;

EID: 61849109833     PISSN: 0065308X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-308X(08)00601-5     Document Type: Review

References (76)

1. Barouch D.H., Kunstman J., Kuroda M.J., Schmitz J.E., Santra S., Peyerl F.W., Krivulka G.R., Beaudry K., Lifton M.A., Gorgone D.A., Montefiori D.C., Lewis M.G., et al. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415 (2002) 335-339
2. Belich M.P., Madrigal J.A., Hildebrand W.H., Zemmour J., Williams R.C., Luz R., Petzl-Erler M.L., and Parham P. Unusual HLA-B alleles in two tribes of Brazilian Indians. Nature 357 (1992) 326-329
3. Bhattacharya T., Daniels M., Heckerman D., Foley B., Frahm N., Kadie C., Carlson J., Yusim K., McMahon B., Gaschen B., Mallal S., Mullins J.I., et al. Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 315 (2007) 1583-1586
4. Borrow P., Lewicki H., Hahn B.H., Shaw G.M., and Oldstone M.B. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68 (1994) 6103-6110
5. Briggs J.A., Simon M.N., Gross I., Krausslich H.G., Fuller S.D., Vogt V.M., and Johnson M.C. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11 (2004) 672-675
6. Brumme Z.L., Brumme C.J., Carlson J., Streeck H., John M., Eichbaum Q., Block B.L., Baker B., Kadie C., Markowitz M., Jessen H., Kelleher A.D., et al. Marked epitope and allele-specific differences in rates of mutation in HIV-1 Gag, Pol and Nef CTL epitopes in acute/early HIV-1 infection. J. Virol. 82 (2008) 9216-9227
7. Carrington M., and O'Brien S.J. The influence of HLA genotype on AIDS. Annu. Rev. Med. 54 (2003) 535-551
8. Chopera D.R., Woodman Z., Mlisana K., Mlotshwa M., Martin D.P., Seoighe C., Treurnicht F., de Rosa D.A., Hide W., Karim S.A., Gray C.M., and Willianson C. Transmission of HIV-1 CTL escape variants provides HLA-mismatched recipients with a survival advantage. PLoS. Pathog. 4 (2008) e1000033
9. Collins K.L., Chen B.K., Kalams S.A., Walker B.D., and Baltimore D. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391 (1998) 397-401
10. Crawford H., Prado J.G., Leslie A., Hue S., Honeyborne I., Reddy S., van der Stok M., Mncube Z., Brander C., Rousseau C., Mullins J.I., Kaslow R., et al. Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLA-B*5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J. Virol. 81 (2007) 8346-8351
11. Edwards B.H., Bansal A., Sabbaj S., Bakari J., Mulligan M.J., and Goepfert P.A. Magnitude of functional CD8+ T-cell responses to the Gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J. Virol. 76 (2002) 2298-2305
12. Feeney M.E., Tang Y., Roosevelt K.A., Leslie A.J., McIntosh K., Karthas N., Walker B.D., and Goulder P.J. Immune escape precedes breakthrough human immunodeficiency virus type 1 viremia and broadening of the cytotoxic T-lymphocyte response in an HLA-B27-positive long-term-nonprogressing child. J. Virol. 78 (2004) 8927-8930
13. Fernandez C.S., Smith M.Z., Batten C.J., De Rose R., Reece J.C., Rollman E., Venturi V., Davenport M.P., and Kent S.J. Vaccine-induced T cells control reversion of AIDS virus immune escape mutants. J. Virol. 81 (2007) 4137-4144
14. Fernandez C.S., Stratov I., DeRose R., Walsh K., Dale C.J., Smith M.Z., Agy M.B., Hu S.L., Krebs K., Watkins D.I., O'Connor D.H., Davenport M.P., et al. Rapid viral escape at an immunodominant simian-human immunodeficiency virus cytotoxic T-lymphocyte epitope exacts a dramatic fitness cost. J. Virol. 79 (2005) 5721-5731
15. Friedrich T.C., Dodds E.J., Yant L.J., Vojnov L., Rudersdorf R., Cullen C., Evans D.T., Desrosiers R.C., Mothe B.R., Sidney J., Sette A., Kunstman K., et al. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat. Med. 10 (2004) 275-281
16. Gaschen B., Taylor J., Yusim K., Foley B., Gao F., Lang D., Novitsky V., Haynes B., Hahn B.H., Bhattacharya T., and Korber B. Diversity considerations in HIV-1 vaccine selection. Science 296 (2002) 2354-2360
17. Geldmacher C., Currier J.R., Herrmann E., Haule A., Kuta E., McCutchan F., Njovu L., Geis S., Hoffmann O., Maboko L., Williamson C., Birx D., et al. CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J. Virol. 81 (2007) 2440-2448
18. Gilbert M.T., Rambaut A., Wlasiuk G., Spira T.J., Pitchenik A.E., and Worobey M. The emergence of HIV/AIDS in the Americas and beyond. Proc. Natl. Acad. Sci. USA 104 (2007) 18566-18570
19. Goepfert P.A., Lumm W., Farmer P., Matthews P., Prendergast A., Carlson J.M., Derdeyn C.A., Tang J., Kaslow R.A., Bansal A., Yusim K., Heckerman D., et al. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. J. Exp. Med. 205 (2008) 1009-1017
20. Goulder P.J., and Watkins D.I. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat. Rev. Immunol. 8 (2008) 619-630
21. Goulder P.J., Brander C., Tang Y., Tremblay C., Colbert R.A., Addo M.M., Rosenberg E.S., Nguyen T., Allen R., Trocha A., Altfeld M., He S., et al. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412 (2001) 334-338
22. Goulder P.J., Phillips R.E., Colbert R.A., McAdam S., Ogg G., Nowak M.A., Giangrande P., Luzzi G., Morgan B., Edwards A., McMichael A.J., et al. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3 (1997) 212-217
23. Honeyborne I., Prendergast A., Pereyra F., Leslie A., Crawford H., Payne R., Reddy S., Bishop K., Moodley E., Nair K., van der Stok M., McCarthy N., et al. Control of human immunodeficiency virus type 1 is associated with HLA-B*13 and targeting of multiple Gag-specific CD8+ T-cell epitopes. J. Virol. 81 (2007) 3667-3672
24. Jin X., Bauer D.E., Tuttleton S.E., Lewin S., Gettie A., Blanchard J., Irwin C.E., Safrit J.T., Mittler J., Weinberger L., Kostrikis L.G., Zhang L., et al. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189 (1999) 991-998
25. Kawada M., Igarashi H., Takeda A., Tsukamoto T., Yamamoto H., Dohki S., Takiguchi M., and Matano T. Involvement of multiple epitope-specific cytotoxic T-lymphocyte responses in vaccine-based control of simian immunodeficiency virus replication in rhesus macaques. J. Virol. 80 (2006) 1949-1958
26. Kelley C.F., Barbour J.D., and Hecht F.M. The relation between symptoms, viral load, and viral load set point in primary HIV infection. J. Acquir. Immune. Defic. Syndr. 45 (2007) 445-448
27. Kiepiela P., Leslie A.J., Honeyborne I., Ramduth D., Thobakgale C., Chetty S., Rathnavalu P., Moore C., Pfafferott K.J., Hilton L., Zimbwa P., Moore S., et al. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432 (2004) 769-775
28. Kiepiela P., Ngumbela K., Thobakgale C., Ramduth D., Honeyborne I., Moodley E., Reddy S., de Pierres C., Mncube Z., Mkhwanazi N., Bishop K., van der Stok M., et al. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13 (2007) 46-53
29. Klein M.R., van Baalen C.A., Holwerda A.M., Kerkhof Garde S.R., Bende R.J., Keet I.P., Eeftinck-Schattenkerk J.K., Osterhaus A.D., Schuitemaker H., and Miedema F. Kinetics of Gag-specific cytotoxic T lymphocyte responses during the clinical course of HIV-1 infection: A longitudinal analysis of rapid progressors and long-term asymptomatics. J. Exp. Med. 181 (1995) 1365-1372
30. Kobayashi M., Igarashi H., Takeda A., Kato M., and Matano T. Reversion in vivo after inoculation of a molecular proviral DNA clone of simian immunodeficiency virus with a cytotoxic-T-lymphocyte escape mutation. J. Virol. 79 (2005) 11529-11532
31. Korber B., Muldoon M., Theiler J., Gao F., Gupta R., Lapedes A., Hahn B.H., Wolinsky S., and Bhattacharya T. Timing the ancestor of the HIV-1 pandemic strains. Science 288 (2000) 1789-1796
32. Koup R.A., Safrit J.T., Cao Y., Andrews C.A., McLeod G., Borkowsky W., Farthing C., and Ho D.D. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68 (1994) 4650-4655
33. Lemey P., Derdelinckx I., Rambaut A., Van Laethem K., Dumont S., Vermeulen S., Van Wijngaerden E., and Vandamme A.M. Molecular footprint of drug-selective pressure in a human immunodeficiency virus transmission chain. J. Virol. 79 (2005) 11981-11989
34. Leslie A., Kavanagh D., Honeyborne I., Pfafferott K., Edwards C., Pillay T., Hilton L., Thobakgale C., Ramduth D., Draenert R., Le Gall S., Luzzi G., et al. Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA. J. Exp. Med. 201 (2005) 891-902
35. Leslie A., Price D.A., Mkhize P., Bishop K., Rathod A., Day C., Crawford H., Honeyborne I., Asher T.E., Luzzi G., Edwards A., Rousseau C.M., et al. Differential selection pressure exerted on HIV by CTL targeting identical epitopes but restricted by distinct HLA alleles from the same HLA supertype. J. Immunol. 177 (2006) 4699-4708
36. Leslie A.J., Pfafferott K.J., Chetty P., Draenert R., Addo M.M., Feeney M., Tang Y., Holmes E.C., Allen T., Prado J.G., Altfeld M., Brander C., et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10 (2004) 282-289
37. Little S.J., Frost S.D., Wong J.K., Smith D.M., Pond S.L., Ignacio C.C., Parkin N.T., Petropoulos C.J., and Richman D.D. Persistence of transmitted drug resistance among subjects with primary human immunodeficiency virus infection. J. Virol. 82 (2008) 5510-5518
38. Marsh S.G.E.P.P., and Barber L.D. The HLA Facts Book (2000), Academic Press, London
39. Martinez-Picado J., Prado J.G., Fry E.E., Pfafferott K., Leslie A., Chetty S., Thobakgale C., Honeyborne I., Crawford H., Matthews P., Pillay T., Rousseau C., et al. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J. Virol. 80 (2006) 3617-3623
40. Masemola A., Mashishi T., Khoury G., Mohube P., Mokgotho P., Vardas E., Colvin M., Zijenah L., Katzenstein D., Musonda R., Allen S., Kumwenda N., et al. Hierarchical targeting of subtype C human immunodeficiency virus type 1 proteins by CD8+ T cells: Correlation with viral load. J. Virol. 78 (2004) 3233-3243
41. Matano T., Kobayashi M., Igarashi H., Takeda A., Nakamura H., Kano M., Sugimoto C., Mori K., Iida A., Hirata T., Hasegawa M., Yuasa T., et al. Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J. Exp. Med. 199 (2004) 1709-1718
42. Matano T., Shibata R., Siemon C., Connors M., Lane H.C., and Martin M.A. Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J. Virol. 72 (1998) 164-169
43. Matthews P.C., Prendergast A., Leslie A., Crawford H., Payne R., Rousseau C., Rolland M., Honeyborne I., Carlson J., Kadie C., Brander C., Bishop K., et al. Central role of reverting mutations in HLA associations with human immunodeficiency virus set point. J. Virol. 82 (2008) 8548-8559
44. McCutchan F.E., Artenstein A.W., Sanders-Buell E., Salminen M.O., Carr J.K., Mascola J.R., Yu X.F., Nelson K.E., Khamboonruang C., Schmitt D., Kieny M.P., McNeil J.G., et al. Diversity of the envelope glycoprotein among human immunodeficiency virus type 1 isolates of clade E from Asia and Africa. J. Virol. 70 (1996) 3331-3338
45. McMichael A., and Klenerman P. HIV/AIDS. HLA leaves its footprints on HIV. Science 296 (2002) 1410-1411
46. Mellors J.W., Rinaldo Jr. C.R., Gupta P., White R.M., Todd J.A., and Kingsley L.A. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272 (1996) 1167-1170
47. Moore C.B., John M., James I.R., Christiansen F.T., Witt C.S., and Mallal S.A. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296 (2002) 1439-1443
48. Mothe B.R., Weinfurter J., Wang C., Rehrauer W., Wilson N., Allen T.M., Allison D.B., and Watkins D.I. Expression of the major histocompatibility complex class I molecule Mamu-A*01 is associated with control of simian immunodeficiency virus SIVmac239 replication. J. Virol. 77 (2003) 2736-2740
49. Mungall A.J., Palmer S.A., Sims S.K., Edwards C.A., Ashurst J.L., Wilming L., Jones M.C., Horton R., Hunt S.E., Scott C.E., Gilbert J.G., Clamp M.E., et al. The DNA sequence and analysis of human chromosome 6. Nature 425 (2003) 805-811
50. Nkengasong J.N., Janssens W., Heyndrickx L., Fransen K., Ndumbe P.M., Motte J., Leonaers A., Ngolle M., Ayuk J., Piot P., et al. Genotypic subtypes of HIV-1 in Cameroon. AIDS 8 (1994) 1405-1412
51. Novitsky V., Gilbert P., Peter T., McLane M.F., Gaolekwe S., Rybak N., Thior I., Ndung'u T., Marlink R., Lee T.H., and Essex M. Association between virus-specific T-cell responses and plasma viral load in human immunodeficiency virus type 1 subtype C infection. J. Virol. 77 (2003) 882-890
52. O'Brien S.J., Gao X., and Carrington M. HLA and AIDS: A cautionary tale. Trends Mol. Med. 7 (2001) 379-381
53. O'Connor D.H., Mothe B.R., Weinfurter J.T., Fuenger S., Rehrauer W.M., Jing P., Rudersdorf R.R., Liebl M.E., Krebs K., Vasquez J., Dodds E., Loffredo J., et al. 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 (2003) 9029-9040
54. Peeters M., and Sharp P.M. Genetic diversity of HIV-1: The moving target. AIDS 14 suppl 3 (2000) S129-S140
55. Phillips R.E., Rowland-Jones S., Nixon D.F., Gotch F.M., Edwards J.P., Ogunlesi A.O., Elvin J.G., Rothbard J.A., Bangham C.R., Rizza C.R., et al. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 354 (1991) 453-459
56. Preston B.D., Poiesz B.J., and Loeb L.A. Fidelity of HIV-1 reverse transcriptase. Science 242 (1988) 1168-1171
57. Rambaut A., Robertson D.L., Pybus O.G., Peeters M., and Holmes E.C. Human immunodeficiency virus. Phylogeny and the origin of HIV-1. Nature 410 (2001) 1047-1048
58. Riviere Y., McChesney M.B., Porrot F., Tanneau-Salvadori F., Sansonetti P., Lopez O., Pialoux G., Feuillie V., Mollereau M., Chamaret S., et al. Gag-specific cytotoxic responses to HIV type 1 are associated with a decreased risk of progression to AIDS-related complex or AIDS. AIDS Res. Hum. Retroviruses 11 (1995) 903-907
59. Riviere Y., Tanneau-Salvadori F., Regnault A., Lopez O., Sansonetti P., Guy B., Kieny M.P., Fournel J.J., and Montagnier L. Multiple cytotoxic effector cells are induced by infection with the human immunodeficiency virus. Res. Immunol. 140 (1989) 110-115 discussion 121
60. Rousseau C.M., Daniels M.G., Carlson J.M., Kadie C., Crawford H., Prendergast A., Matthews P., Payne R., Rolland M., Raugi D.N., Maust B.S., Learn G.H., et al. HLA class-I driven evolution of human immunodeficiency virus type 1 subtype C proteome: Immune escape and viral load. J. Virol. 82 (2008) 6434-6446
61. Sacha J.B., Chung C., Rakasz E.G., Spencer S.P., Jonas A.K., Bean A.T., Lee W., Burwitz B.J., Stephany J.J., Loffredo J.T., Allison D.B., Adnan S., et al. Gag-specific CD8+ T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J. Immunol. 178 (2007) 2746-2754
62. Sacha J.B., Chung C., Reed J., Jonas A.K., Bean A.T., Spencer S.P., Lee W., Vojnov L., Rudersdorf R., Friedrich T.C., Wilson N.A., Lifson J.D., et al. Pol-specific CD8+ T cells recognize simian immunodeficiency virus-infected cells prior to Nef-mediated major histocompatibility complex class I downregulation. J. Virol. 81 (2007) 11703-11712
63. Schmitz J.E., Kuroda M.J., Santra S., Sasseville V.G., Simon M.A., Lifton M.A., Racz P., Tenner-Racz K., Dalesandro M., Scallon B.J., Ghrayeb J., Forman M.A., et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283 (1999) 857-860
64. Schneidewind A., Brockman M.A., Yang R., Adam R.I., Li B., Le Gall S., Rinaldo C.R., Craggs S.L., Allgaier R.L., Power K.A., Kuntzen T., Tung C.S., et al. 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 (2007) 12382-12393
65. Sekaly R.P. The failed HIV Merck vaccine study: A step back or a launching point for future vaccine development?. J. Exp. Med 205 (2008) 7-12
66. Shehu-Xhilaga M., Kraeusslich H.G., Pettit S., Swanstrom R., Lee J.Y., Marshall J.A., Crowe S.M., and Mak J. Proteolytic processing of the p2/nucleocapsid cleavage site is critical for human immunodeficiency virus type 1 RNA dimer maturation. J. Virol. 75 (2001) 9156-9164
67. Shriner D., Shankarappa R., Jensen M.A., Nickle D.C., Mittler J.E., Margolick J.B., and Mullins J.I. Influence of random genetic drift on human immunodeficiency virus type 1 env evolution during chronic infection. Genetics 166 (2004) 1155-1164
68. Steinbrook R. One step forward, two steps back-will there ever be an AIDS vaccine?. N. Engl. J. Med. 357 (2007) 2653-2655
69. Thomson M.M., de Parga E.V., Vinogradova A., Sierra M., Yakovlev A., Rakhmanova A., Delgado E., Casado G., Munoz M., Carmona R., Vega Y., Perez-Alvarez L., et al. New insights into the origin of the HIV type 1 subtype A epidemic in former soviet union's countries derived from sequence analyses of preepidemically transmitted viruses. AIDS Res. Hum. Retroviruses 23 (2007) 1599-1604
70. Tsomides T.J., Aldovini A., Johnson R.P., Walker B.D., Young R.A., and Eisen H.N. Naturally processed viral peptides recognized by cytotoxic T lymphocytes on cells chronically infected by human immunodeficiency virus type 1. J. Exp. Med. 180 (1994) 1283-1293
71. Tsukamoto T., Dohki S., Ueno T., Kawada M., Takeda A., Yasunami M., Naruse T., Kimura A., Takiguchi M., and Matano T. Determination of a major histocompatibility complex class I restricting simian immunodeficiency virus Gag241-249 epitope. AIDS 22 (2008) 993-994
72. Vidal N., Peeters M., Mulanga-Kabeya C., Nzilambi N., Robertson D., Ilunga W., Sema H., Tshimanga K., Bongo B., and Delaporte E. Unprecedented degree of human immunodeficiency virus type 1 (HIV-1) group M genetic diversity in the Democratic Republic of Congo suggests that the HIV-1 pandemic originated in Central Africa. J. Virol. 74 (2000) 10498-10507
73. Wain L.V., Bailes E., Bibollet-Ruche F., Decker J.M., Keele B.F., Van Heuverswyn F., Li Y., Takehisa J., Ngole E.M., Shaw G.M., Peeters M., Hahn B.H., et al. Adaptation of HIV-1 to its human host. Mol. Biol. Evol. 24 (2007) 1853-1860
74. Watkins D.I., Burton D.R., Kallas E.G., Moore J.P., and Koff W.C. Nonhuman primate models and the failure of the Merck HIV-1 vaccine in humans. Nat. Med. 14 (2008) 617-621
75. Watkins D.I., McAdam S.N., Liu X., Strang C.R., Milford E.L., Levine C.G., Garber T.L., Dogon A.L., Lord C.I., Ghim S.H., et al. New recombinant HLA-B alleles in a tribe of South American Amerindians indicate rapid evolution of MHC class I loci. Nature 357 (1992) 329-333
76. Zuniga R., Lucchetti A., Galvan P., Sanchez S., Sanchez C., Hernandez A., Sanchez H., Frahm N., Linde C.H., Hewitt H.S., Hildebrand W., Altfeld M., et al. Relative dominance of Gag p24-specific cytotoxic T lymphocytes is associated with human immunodeficiency virus control. J. Virol. 80 (2006) 3122-3125