The HIV-1 pandemic: Does the selective sweep in chimpanzees mirror humankind's future?

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  de Groot, Natasja G ^a   Bontrop, Ronald E ^a,b  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

AIDS; Chimpanzee; HIV 1; HLA; Human; MHC; Repertoire reduction; SIVcpz; Zoonosis

Indexed keywords

CHEMOKINE RECEPTOR CCR5; HLA A ANTIGEN; HLA A1 ANTIGEN; HLA A11 ANTIGEN; HLA A3 ANTIGEN; HLA B ANTIGEN; HLA B27 ANTIGEN; HLA B57 ANTIGEN; HLA C ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALLOTYPE; CCR5 GENE; CHIMPANZEE; GENE LOCUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION CONTROL; MICA GENE; MICB GENE; MICC GENE; MICD GENE; MICE GENE; MICF GENE; MICG GENE; NONHUMAN; PANDEMIC; PROMOTER REGION; REVIEW; SELECTIVE SWEEP; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENE; VIRUS GENOME; VIRUS TRANSMISSION;

ANIMALS; DISEASE RESISTANCE; HIV INFECTIONS; HIV-1; HUMANS; PAN TROGLODYTES; PANDEMICS; SELECTION, GENETIC; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; WORLD HEALTH;

HUMAN IMMUNODEFICIENCY VIRUS 1; PAN; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84878009023     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-53     Document Type: Review

References (133)

1. Hemelaar J. The origin and diversity of the HIV-1 pandemic. Trends Mol Med 2012, 18:182-192. 10.1016/j.molmed.2011.12.001, 22240486.
2. Thomson MM, Perez-Alvarez L, Najera R. Molecular epidemiology of HIV-1 genetic forms and its significance for vaccine development and therapy. Lancet Infect Dis 2002, 2:461-471. 10.1016/S1473-3099(02)00343-2, 12150845.
3. Chun TW, Fauci AS. HIV reservoirs: pathogenesis and obstacles to viral eradication and cure. AIDS 2012, 26:1261-1268. 10.1097/QAD.0b013e328353f3f1, 22472858.
4. Chun TW, Davey RT, Ostrowski M, Shawn Justement J, Engel D, Mullins JI, Fauci AS. Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nat Med 2000, 6:757-761. 10.1038/77481, 10888923.
5. Davey RT, Bhat N, Yoder C, Chun TW, Metcalf JA, Dewar R, Natarajan V, Lempicki RA, Adelsberger JW, Miller KD. HIV-1 and T cell dynamics after interruption of highly active antiretroviral therapy (HAART) in patients with a history of sustained viral suppression. Proc Natl Acad Sci USA 1999, 96:15109-15114. 10.1073/pnas.96.26.15109, 24781, 10611346.
6. Garcia F, Plana M, Vidal C, Cruceta A, O'Brien WA, Pantaleo G, Pumarola T, Gallart T, Miro JM, Gatell JM. Dynamics of viral load rebound and immunological changes after stopping effective antiretroviral therapy. AIDS 1999, 13:F79-F86. 10.1097/00002030-199907300-00002, 10449278.
7. Harrigan PR, Whaley M, Montaner JS. Rate of HIV-1 RNA rebound upon stopping antiretroviral therapy. AIDS 1999, 13:F59-F62. 10.1097/00002030-199905280-00001, 10371167.
8. Friedland GH, Williams A. Attaining higher goals in HIV treatment: the central importance of adherence. AIDS 1999, 13(Suppl 1):S61-S72.
9. Wain-Hobson S, Sonigo P, Danos O, Cole S, Alizon M. Nucleotide sequence of the AIDS virus, LAV. Cell 1985, 40:9-17. 10.1016/0092-8674(85)90303-4, 2981635.
10. Subbramanian RA, Cohen EA. Molecular biology of the human immunodeficiency virus accessory proteins. J Virol 1994, 68:6831-6835. 237118, 7933064.
11. Ho DD. Perspectives series: host/pathogen interactions. Dynamics of HIV-1 replication in vivo. J Clin Invest 1997, 99:2565-2567. 10.1172/JCI119443, 508100, 9169484.
12. Wei X, Ghosh SK, Taylor ME, Johnson VA, Emini EA, Deutsch P, Lifson JD, Bonhoeffer S, Nowak MA, Hahn BH. Viral dynamics in human immunodeficiency virus type 1 infection. Nature 1995, 373:117-122. 10.1038/373117a0, 7529365.
13. Mansky LM, Temin HM. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol 1995, 69:5087-5094. 189326, 7541846.
14. Levy JA. HIV and the Pathogenesis of AIDS 2007, Washington, DC: American Society of Microbiology.
15. Bomsel M, David V. Mucosal gatekeepers: selecting HIV viruses for early infection. Nat Med 2002, 8:114-116. 10.1038/nm0202-114, 11821891.
16. Pope M, Haase AT. Transmission, acute HIV-1 infection and the quest for strategies to prevent infection. Nat Med 2003, 9:847-852. 10.1038/nm0703-847, 12835704.
17. van Kooyk Y, Geijtenbeek TB. DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol 2003, 3:697-709. 10.1038/nri1182, 12949494.
18. McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D, Hope TJ. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 2003, 300:1295-1297. 10.1126/science.1084238, 12730499.
19. Gorry PR, Churchill M, Crowe SM, Cunningham AL, Gabuzda D. Pathogenesis of macrophage tropic HIV-1. Curr HIV Res 2005, 3:53-60. 10.2174/1570162052772951, 15638723.
20. Pierson T, McArthur J, Siliciano RF. Reservoirs for HIV-1: mechanisms for viral persistence in the presence of antiviral immune responses and antiretroviral therapy. Annu Rev Immunol 2000, 18:665-708. 10.1146/annurev.immunol.18.1.665, 10837072.
21. Pandrea I, Apetrei C, Gordon S, Barbercheck J, Dufour J, Bohm R, Sumpter B, Roques P, Marx PA, Hirsch VM. Paucity of CD4 + CCR5+ T cells is a typical feature of natural SIV hosts. Blood 2007, 109:1069-1076. 1785133, 17003371.
22. Sodora DL, Allan JS, Apetrei C, Brenchley JM, Douek DC, Else JG, Estes JD, Hahn BH, Hirsch VM, Kaur A. Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat Med 2009, 15:861-865. 10.1038/nm.2013, 2782707, 19661993.
23. Santiago ML, Range F, Keele BF, Li Y, Bailes E, Bibollet-Ruche F, Fruteau C, Noe R, Peeters M, Brookfield JF. Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Tai Forest, Cote d'Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol 2005, 79:12515-12527. 10.1128/JVI.79.19.12515-12527.2005, 1211554, 16160179.
24. Santiago ML, Rodenburg CM, Kamenya S, Bibollet-Ruche F, Gao F, Bailes E, Meleth S, Soong SJ, Kilby JM, Moldoveanu Z. SIVcpz in wild chimpanzees. Science 2002, 295:465. 10.1126/science.295.5554.465, 11799233.
25. Bowden R, MacFie TS, Myers S, Hellenthal G, Nerrienet E, Bontrop RE, Freeman C, Donnelly P, Mundy NI. Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes ellioti is a genetically distinct population. PLoS Genet 2012, 8:e1002504. 10.1371/journal.pgen.1002504, 3291532, 22396655.
26. Gagneux P, Wills C, Gerloff U, Tautz D, Morin PA, Boesch C, Fruth B, Hohmann G, Ryder OA, Woodruff DS. Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc Natl Acad Sci USA 1999, 96:5077-5082. 10.1073/pnas.96.9.5077, 21819, 10220421.
27. Morin PA, Moore JJ, Chakraborty R, Jin L, Goodall J, Woodruff DS. Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science 1994, 265:1193-1201. 10.1126/science.7915048, 7915048.
28. Bailes E, Gao F, Bibollet-Ruche F, Courgnaud V, Peeters M, Marx PA, Hahn BH, Sharp PM. Hybrid origin of SIV in chimpanzees. Science 2003, 300:1713. 10.1126/science.1080657, 12805540.
29. Hahn BH, Shaw GM, De Cock KM, Sharp PM. AIDS as a zoonosis: scientific and public health implications. Science 2000, 287:607-614. 10.1126/science.287.5453.607, 10649986.
30. Plantier JC, Leoz M, Dickerson JE, De Oliveira F, Cordonnier F, Lemee V, Damond F, Robertson DL, Simon F. A new human immunodeficiency virus derived from gorillas. Nat Med 2009, 15:871-872. 10.1038/nm.2016, 19648927.
31. Van Heuverswyn F, Li Y, Neel C, Bailes E, Keele BF, Liu W, Loul S, Butel C, Liegeois F, Bienvenue Y. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 2006, 444:164. 10.1038/444164a, 17093443.
32. Takehisa J, Kraus MH, Ayouba A, Bailes E, Van Heuverswyn F, Decker JM, Li Y, Rudicell RS, Learn GH, Neel C. Origin and biology of simian immunodeficiency virus in wild-living western gorillas. J Virol 2009, 83:1635-1648. 10.1128/JVI.02311-08, 2643789, 19073717.
33. Hatziioannou T, Ambrose Z, Chung NP, Piatak M, Yuan F, Trubey CM, Coalter V, Kiser R, Schneider D, Smedley J. A macaque model of HIV-1 infection. Proc Natl Acad Sci USA 2009, 106:4425-4429. 10.1073/pnas.0812587106, 2657417, 19255423.
34. Thippeshappa R, Polacino P, Yu Kimata MT, Siwak EB, Anderson D, Wang W, Sherwood L, Arora R, Wen M, Zhou P. Vif substitution enables persistent infection of pig-tailed macaques by human immunodeficiency virus type 1. J Virol 2011, 85:3767-3779. 10.1128/JVI.02438-10, 3126129, 21289128.
35. Gotz N, Sauter D, Usmani SM, Fritz JV, Goffinet C, Heigele A, Geyer M, Bibollet-Ruche F, Learn GH, Fackler OT. Reacquisition of Nef-mediated tetherin antagonism in a single in vivo passage of HIV-1 through its original chimpanzee host. Cell Host Microbe 2012, 12:373-380. 10.1016/j.chom.2012.07.008, 22980333.
36. Heeney JL. AIDS: a disease of impaired Th-cell renewal?. Immunol Today 1995, 16:515-520. 10.1016/0167-5699(95)80043-3, 7495487.
37. Huet T, Cheynier R, Meyerhans A, Roelants G, Wain-Hobson S. Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature 1990, 345:356-359. 10.1038/345356a0, 2188136.
38. Peeters M, Fransen K, Delaporte E, Van den Haesevelde M, Gershy-Damet GM, Kestens L, van der Groen G, Piot P. Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wild-captured chimpanzee. AIDS 1992, 6:447-451. 10.1097/00002030-199205000-00002, 1616649.
39. Peeters M, Honore C, Huet T, Bedjabaga L, Ossari S, Bussi P, Cooper RW, Delaporte E. Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. AIDS 1989, 3:625-630. 10.1097/00002030-198910000-00001, 2512955.
40. Nerrienet E, Santiago ML, Foupouapouognigni Y, Bailes E, Mundy NI, Njinku B, Kfutwah A, Muller-Trutwin MC, Barre-Sinoussi F, Shaw GM. Simian immunodeficiency virus infection in wild-caught chimpanzees from cameroon. J Virol 2005, 79:1312-1319. 10.1128/JVI.79.2.1312-1319.2005, 538556, 15613358.
41. Santiago ML, Lukasik M, Kamenya S, Li Y, Bibollet-Ruche F, Bailes E, Muller MN, Emery M, Goldenberg DA, Lwanga JS. Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). J Virol 2003, 77:7545-7562. 10.1128/JVI.77.13.7545-7562.2003, 164799, 12805455.
42. Heeney JL, Rutjens E, Verschoor EJ, Niphuis H, ten Haaft P, Rouse S, McClure H, Balla-Jhagjhoorsingh S, Bogers W, Salas M. Transmission of simian immunodeficiency virus SIVcpz and the evolution of infection in the presence and absence of concurrent human immunodeficiency virus type 1 infection in chimpanzees. J Virol 2006, 80:7208-7218. 10.1128/JVI.00382-06, 1489021, 16809326.
43. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, Li Y, Learn GH, Beasley TM, Schumacher-Stankey J. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 2009, 460:515-519. 10.1038/nature08200, 2872475, 19626114.
44. Etienne L, Nerrienet E, LeBreton M, Bibila GT, Foupouapouognigni Y, Rousset D, Nana A, Djoko CF, Tamoufe U, Aghokeng AF. Characterization of a new simian immunodeficiency virus strain in a naturally infected Pan troglodytes troglodytes chimpanzee with AIDS related symptoms. Retrovirology 2011, 8:4. 3034674, 21232091.
45. Novembre FJ, Saucier M, Anderson DC, Klumpp SA, O'Neil SP, Brown CR, Hart CE, Guenthner PC, Swenson RB, McClure HM. Development of AIDS in a chimpanzee infected with human immunodeficiency virus type 1. J Virol 1997, 71:4086-4091. 191562, 9094687.
46. Novembre FJ, de Rosayro J, Nidtha S, O'Neil SP, Gibson TR, Evans-Strickfaden T, Hart CE, McClure HM. Rapid CD4(+) T-cell loss induced by human immunodeficiency virus type 1(NC) in uninfected and previously infected chimpanzees. J Virol 2001, 75:1533-1539. 10.1128/JVI.75.3.1533-1539.2001, 114058, 11152525.
47. Deeks SG, Walker BD. Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 2007, 27:406-416. 10.1016/j.immuni.2007.08.010, 17892849.
48. Carrington M, O'Brien SJ. The influence of HLA genotype on AIDS. Annu Rev Med 2003, 54:535-551. 10.1146/annurev.med.54.101601.152346, 12525683.
49. Dalmasso C, Carpentier W, Meyer L, Rouzioux C, Goujard C, Chaix ML, Lambotte O, Avettand-Fenoel V, Le Clerc S, de Senneville LD. Distinct genetic loci control plasma HIV-RNA and cellular HIV-DNA levels in HIV-1 infection: the ANRS genome wide association 01 study. PLoS One 2008, 3:e3907. 10.1371/journal.pone.0003907, 2603319, 19107206.
50. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, Weale M, Zhang K, Gumbs C, Castagna A, Cossarizza A. A whole-genome association study of major determinants for host control of HIV-1. Science 2007, 317:944-947. 10.1126/science.1143767, 1991296, 17641165.
51. Goulder PJ, Bunce M, Krausa P, McIntyre K, Crowley S, Morgan B, Edwards A, Giangrande P, Phillips RE, McMichael AJ. Novel, cross-restricted, conserved, and immunodominant cytotoxic T lymphocyte epitopes in slow progressors in HIV type 1 infection. AIDS Res Hum Retroviruses 1996, 12:1691-1698. 10.1089/aid.1996.12.1691, 8959245.
52. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, Goedert JJ, Winkler C, O'Brien SJ, Rinaldo C. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 1996, 2:405-411. 10.1038/nm0496-405, 8597949.
53. Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, Chetty S, Rathnavalu P, Moore C, Pfafferott KJ, Hilton L. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 2004, 432:769-775. 10.1038/nature03113, 15592417.
54. Pereyra F, Jia X, McLaren PJ, Telenti A, de Bakker PI, Walker BD, Ripke S, Brumme CJ, Pulit SL, Carrington M. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 2010, 330:1551-1557. 3235490, 21051598.
55. Marsh SG, Albert ED, Bodmer WF, Bontrop RE, Dupont B, Erlich HA, Fernandez-Vina M, Geraghty DE, Holdsworth R, Hurley CK. An update to HLA nomenclature, 2010. Bone Marrow Transplant 2010, 45:846-848. 10.1038/bmt.2010.79, 20348972.
56. Hansen TH, Bouvier M. MHC class I antigen presentation: learning from viral evasion strategies. Nat Rev Immunol 2009, 9:503-513. 10.1038/nri2575, 19498380.
57. Harding CV, Boom WH. Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat Rev Microbiol 2010, 8:296-307. 10.1038/nrmicro2321, 3037727, 20234378.
58. Horst D, Verweij MC, Davison AJ, Ressing ME, Wiertz EJ. Viral evasion of T cell immunity: ancient mechanisms offering new applications. Curr Opin Immunol 2011, 23:96-103. 10.1016/j.coi.2010.11.005, 21146386.
59. Jackson SE, Mason GM, Wills MR. Human cytomegalovirus immunity and immune evasion. Virus Res 2011, 157:151-160. 10.1016/j.virusres.2010.10.031, 21056604.
60. Goulder PJ, Walker BD. HIV and HLA Class I: an evolving relationship. Immunity 2012, 37:426-440. 10.1016/j.immuni.2012.09.005, 22999948.
61. Luo M, Daniuk CA, Diallo TO, Capina RE, Kimani J, Wachihi C, Kimani M, Bielawny T, Peterson T, Mendoza MG. For protection from HIV-1 infection, more might not be better: a systematic analysis of HIV Gag epitopes of two alleles associated with different outcomes of HIV-1 infection. J Virol 2012, 86:1166-1180. 10.1128/JVI.05721-11, 3255815, 22072744.
62. Adams EJ, Cooper S, Parham P. A novel, nonclassical MHC class I molecule specific to the common chimpanzee. J Immunol 2001, 167:3858-3869.
63. Geller R, Adams EJ, Guethlein LA, Little AM, Madrigal JA, Parham P. Linkage of Patr-AL to Patr-A and- B in the major histocompatibility complex of the common chimpanzee (Pan troglodytes). Immunogenetics 2002, 54:212-215. 10.1007/s00251-002-0452-x, 12073151.
64. van Rood JJ, van Leeuwen A, Balner H. HL-A and ChL-A: similarities and differences. Transplant Proc 1972, 4:55-62.
65. Domena JD, Hildebrand WH, Bias WB, Parham P. A sixth family of HLA-A alleles defined by HLA-A*8001. Tissue Antigens 1993, 42:156-159. 10.1111/j.1399-0039.1993.tb02186.x, 8284791.
66. Kato K, Trapani JA, Allopenna J, Dupont B, Yang SY. Molecular analysis of the serologically defined HLA-Aw19 antigens. A genetically distinct family of HLA-A antigens comprising A29, A31, A32, and Aw33, but probably not A30. J Immunol 1989, 143:3371-3378.
67. McAdam SN, Boyson JE, Liu X, Garber TL, Hughes AL, Bontrop RE, Watkins DI. Chimpanzee MHC class I A locus alleles are related to only one of the six families of human A locus alleles. J Immunol 1995, 154:6421-6429.
68. Fujiyama A, Watanabe H, Toyoda A, Taylor TD, Itoh T, Tsai SF, Park HS, Yaspo ML, Lehrach H, Chen Z. Construction and analysis of a human-chimpanzee comparative clone map. Science 2002, 295:131-134. 10.1126/science.1065199, 11778049.
69. Klein J. Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. Hum Immunol 1987, 19:155-162. 10.1016/0198-8859(87)90066-8, 3305436.
70. Robinson J, Mistry K, McWilliam H, Lopez R, Parham P, Marsh SG. The IMGT/HLA database. Nucleic Acids Res 2011, 39:D1171-D1176. 10.1093/nar/gkq998, 3013815, 21071412.
71. de Groot NG, Otting N, Robinson J, Blancher A, Lafont BA, Marsh SG, O'Connor DH, Shiina T, Walter L, Watkins DI, Bontrop RE. Nomenclature report on the major histocompatibility complex genes and alleles of Great Ape, Old and New World monkey species. Immunogenetics 2012, 64:615-631. 10.1007/s00251-012-0617-1, 22526602.
72. de Groot NG, Otting N, Arguello R, Watkins DI, Doxiadis GG, Madrigal JA, Bontrop RE. Major histocompatibility complex class I diversity in a West African chimpanzee population: implications for HIV research. Immunogenetics 2000, 51:398-409. 10.1007/s002510050638, 10866106.
73. Adams EJ, Cooper S, Thomson G, Parham P. Common chimpanzees have greater diversity than humans at two of the three highly polymorphic MHC class I genes. Immunogenetics 2000, 51:410-424. 10.1007/s002510050639, 10866107.
74. Caggiari L, Simula MP, Marzotto A, Shiina M, Rehermann B, De Re V. Identification of novel chimpanzee MHC class I and II alleles using an improved sequence-based typing strategy. Hum Immunol 2006, 67:63-72. 10.1016/j.humimm.2006.02.004, 16698427.
75. Chen ZW, Hughes AL, Ghim SH, Letvin NL, Watkins DI. Two more chimpanzee Patr-A locus alleles related to the HLA-A1/A3/A11 family. Immunogenetics 1993, 38:238-240.
76. Kowalski H, Erickson AL, Cooper S, Domena JD, Parham P, Walker CM. Patr-A and B, the orthologues of HLA-A and B, present hepatitis C virus epitopes to CD8+ cytotoxic T cells from two chronically infected chimpanzees. J Exp Med 1996, 183:1761-1775. 10.1084/jem.183.4.1761, 2192520, 8666933.
77. Zhang L, van Bree S, Gijbels Y, van Veen A, van Rood JJ, Class FH. Comparison of the humoral and cytotoxic T-lymphocyte response to individual HLA class I alloantigens in highly immunized patients. Hum Immunol 1991, 30:156-161. 10.1016/0198-8859(91)90029-9, 2055781.
78. de Groot NG, Otting N, Doxiadis GG, Balla-Jhagjhoorsingh SS, Heeney JL, van Rood JJ, Gagneux P, Bontrop RE. Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proc Natl Acad Sci USA 2002, 99:11748-11753. 10.1073/pnas.182420799, 129340, 12186979.
79. de Groot NG, Heijmans CM, de Groot N, Otting N, de Vos-Rouweller AJ, Remarque EJ, Bonhomme M, Doxiadis GG, Crouau-Roy B, Bontrop RE. Pinpointing a selective sweep to the chimpanzee MHC class I region by comparative genomics. Mol Ecol 2008, 17:2074-2088. 10.1111/j.1365-294X.2008.03716.x, 18346126.
80. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, Nguyen PL, Khoruts A, Larson M, Haase AT, Douek DC. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004, 200:749-759. 10.1084/jem.20040874, 2211962, 15365096.
81. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, Hogan C, Boden D, Racz P, Markowitz M. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 2004, 200:761-770. 10.1084/jem.20041196, 2211967, 15365095.
82. Veazey RS, Lackner AA. Getting to the guts of HIV pathogenesis. J Exp Med 2004, 200:697-700. 10.1084/jem.20041464, 2211972, 15381725.
83. Li Q, Duan L, Estes JD, Ma ZM, Rourke T, Wang Y, Reilly C, Carlis J, Miller CJ, Haase AT. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 2005, 434:1148-1152.
84. Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci USA 1996, 93:12445-12450. 10.1073/pnas.93.22.12445, 38011, 8901601.
85. Anzai T, Shiina T, Kimura N, Yanagiya K, Kohara S, Shigenari A, Yamagata T, Kulski JK, Naruse TK, Fujimori Y. Comparative sequencing of human and chimpanzee MHC class I regions unveils insertions/deletions as the major path to genomic divergence. Proc Natl Acad Sci USA 2003, 100:7708-7713. 10.1073/pnas.1230533100, 164652, 12799463.
86. de Groot NG, Garcia CA, Verschoor EJ, Doxiadis GG, Marsh SG, Otting N, Bontrop RE. Reduced MIC gene repertoire variation in West African chimpanzees as compared to humans. Mol Biol Evol 2005, 22:1375-1385. 10.1093/molbev/msi127, 15758205.
87. Gleimer M, Parham P. Stress management: MHC class I and class I-like molecules as reporters of cellular stress. Immunity 2003, 19:469-477. 10.1016/S1074-7613(03)00272-3, 14563312.
88. Steinle A, Groh V, Spies T. Diversification, expression, and gamma delta T cell recognition of evolutionarily distant members of the MIC family of major histocompatibility complex class I-related molecules. Proc Natl Acad Sci USA 1998, 95:12510-12515. 10.1073/pnas.95.21.12510, 22861, 9770516.
89. Shum BP, Flodin LR, Muir DG, Rajalingam R, Khakoo SI, Cleland S, Guethlein LA, Uhrberg M, Parham P. Conservation and variation in human and common chimpanzee CD94 and NKG2 genes. J Immunol 2002, 168:240-252.
90. Gonzalez E, Bamshad M, Sato N, Mummidi S, Dhanda R, Catano G, Cabrera S, McBride M, Cao XH, Merrill G. Race-specific HIV-1 disease-modifying effects associated with CCR5 haplotypes. Proc Natl Acad Sci USA 1999, 96:12004-12009. 10.1073/pnas.96.21.12004, 18402, 10518566.
91. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 1996, 382:722-725. 10.1038/382722a0, 8751444.
92. Benton PA, Lee DR, Kennedy RC. Sequence comparisons of non-human primate HIV-1 coreceptor homologues. Mol Immunol 1998, 35:95-101. 10.1016/S0161-5890(98)00016-9, 9683255.
93. Pretet JL, Zerbib AC, Girard M, Guillet JG, Butor C. Chimpanzee CXCR4 and CCR5 act as coreceptors for HIV type 1. AIDS Res Hum Retroviruses 1997, 13:1583-1587. 10.1089/aid.1997.13.1583, 9430250.
94. Voevodin A, Samilchuk E, Dashti S. A survey for 32 nucleotide deletion in the CCR-5 chemokine receptor gene (deltaccr-5) conferring resistance to human immunodeficiency virus type 1 in different ethnic groups and in chimpanzees. J Med Virol 1998, 55:147-151. 10.1002/(SICI)1096-9071(199806)55:2<147::AID-JMV11>3.0.CO;2-F, 9598936.
95. Bamshad MJ, Mummidi S, Gonzalez E, Ahuja SS, Dunn DM, Watkins WS, Wooding S, Stone AC, Jorde LB, Weiss RB, Ahuja SK. A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5. Proc Natl Acad Sci USA 2002, 99:10539-10544. 10.1073/pnas.162046399, 124967, 12149450.
96. Wooding S, Stone AC, Dunn DM, Mummidi S, Jorde LB, Weiss RK, Ahuja S, Bamshad MJ. Contrasting effects of natural selection on human and chimpanzee CC chemokine receptor 5. Am J Hum Genet 2005, 76:291-301. 10.1086/427927, 1196374, 15625621.
97. MacFie TS, Nerrienet E, de Groot NG, Bontrop RE, Mundy NI. Patterns of diversity in HIV-related loci among subspecies of chimpanzee: concordance at CCR5 and differences at CXCR4 and CX3CR1. Mol Biol Evol 2009, 26:719-727. 10.1093/molbev/msp016, 19182224.
98. Van Heuverswyn F, Li Y, Bailes E, Neel C, Lafay B, Keele BF, Shaw KS, Takehisa J, Kraus MH, Loul S. Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology 2007, 368:155-171. 10.1016/j.virol.2007.06.018, 17651775.
99. Strebel K, Luban J, Jeang KT. Human cellular restriction factors that target HIV-1 replication. BMC Med 2009, 7:48. 10.1186/1741-7015-7-48, 2759957, 19758442.
100. Sawyer SL, Emerman M, Malik HS. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2004, 2:E275. 10.1371/journal.pbio.0020275, 479043, 15269786.
101. Sobieszczyk ME, Lingappa JR, McElrath MJ. Host genetic polymorphisms associated with innate immune factors and HIV-1. Curr Opin HIV AIDS 2011, 6:427-434. 10.1097/COH.0b013e3283497155, 21734565.
102. Duggal NK, Malik HS, Emerman M. The breadth of antiviral activity of Apobec3DE in chimpanzees has been driven by positive selection. J Virol 2011, 85:11361-11371. 10.1128/JVI.05046-11, 3194980, 21835794.
103. Bontrop RE, Broos LA, Otting N, Jonker MJ. Polymorphism of C4 and CYP21 genes in various primate species. Tissue Antigens 1991, 37:145-151. 10.1111/j.1399-0039.1991.tb01862.x, 1681597.
104. Tassabehji M, Strachan T, Anderson M, Campbell RD, Collier S, Lako M. Identification of a novel family of human endogenous retroviruses and characterization of one family member, HERV-K(C4), located in the complement C4 gene cluster. Nucleic Acids Res 1994, 22:5211-5217. 10.1093/nar/22.24.5211, 332062, 7816608.
105. Schneider PM, Witzel-Schlomp K, Steinhauer C, Stradmann-Bellinghausen B, Rittner C. Rapid detection of the ERV-K(C4) retroviral insertion reveals further structural polymorphism of the complement C4 genes in old world primates. Exp Clin Immunogenet 2001, 18:130-134. 10.1159/000049192, 11549842.
106. Prufer K, Munch K, Hellmann I, Akagi K, Miller JR, Walenz B, Koren S, Sutton G, Kodira C, Winer R. The bonobo genome compared with the chimpanzee and human genomes. Nature 2012, 486:527-531. 3498939, 22722832.
107. Borghans JA, Molgaard A, de Boer RJ, Kesmir C. HLA alleles associated with slow progression to AIDS truly prefer to present HIV-1 p24. PLoS One 2007, 2:e920. 10.1371/journal.pone.0000920, 1976389, 17878955.
108. Rolland M, Heckerman D, Deng W, Rousseau CM, Coovadia H, Bishop K, Goulder PJ, Walker BD, Brander C, Mullins JI. Broad and Gag-biased HIV-1 epitope repertoires are associated with lower viral loads. PLoS One 2008, 3:e1424. 10.1371/journal.pone.0001424, 2170517, 18183304.
109. de Groot NG, Heijmans CM, Zoet YM, de Ru AH, Verreck FA, van Veelen PA, Drijfhout JW, Doxiadis GG, Remarque EJ, Doxiadis II. AIDS-protective HLA-B*27/B*57 and chimpanzee MHC class I molecules target analogous conserved areas of HIV-1/SIVcpz. Proc Natl Acad Sci USA 2010, 107:15175-15180. 10.1073/pnas.1009136107, 2930537, 20696916.
110. van Deutekom HW, Hoof I, Bontrop RE, Kesmir C. A comparative analysis of viral peptides presented by contemporary human and chimpanzee MHC class I molecules. J Immunol 2011, 187:5995-6001. 10.4049/jimmunol.1102236, 22043011.
111. Gleimer M, Wahl AR, Hickman HD, Abi-Rached L, Norman PJ, Guethlein LA, Hammond JA, Draghi M, Adams EJ, Juo S. Although divergent in residues of the peptide binding site, conserved chimpanzee Patr-AL and polymorphic human HLA-A*02 have overlapping peptide-binding repertoires. J Immunol 2011, 186:1575-1588. 10.4049/jimmunol.1002990, 3124313, 21209280.
112. Balla-Jhagjhoorsingh SS, Koopman G, Mooij P, Haaksma TG, Teeuwsen VJ, Bontrop RE, Heeney JL. Conserved CTL epitopes shared between HIV-infected human long-term survivors and chimpanzees. J Immunol 1999, 162:2308-2314.
113. Balla-Jhagjhoorsingh SS, Mooij P, ten Haaft PJ, Bogers WM, Teeuwsen VJ, Koopman G, Heeney JL. Protection from secondary human immunodeficiency virus type 1 infection in chimpanzees suggests the importance of antigenic boosting and a possible role for cytotoxic T cells. J Infect Dis 2001, 184:136-143. 10.1086/322019, 11424009.
114. Hvilsom C, Carlsen F, Siegismund HR, Corbet S, Nerrienet E, Fomsgaard A. Genetic subspecies diversity of the chimpanzee CD4 virus-receptor gene. Genomics 2008, 92:322-328. 10.1016/j.ygeno.2008.07.003, 18718520.
115. Leitner T, Dazza MC, Ekwalanga M, Apetrei C, Saragosti S. Sequence diversity among chimpanzee simian immunodeficiency viruses (SIVcpz) suggests that SIVcpzPts was derived from SIVcpzPtt through additional recombination events. AIDS Res Hum Retroviruses 2007, 23:1114-1118. 10.1089/aid.2007.0071, 17919106.
116. Mothe BR, Sidney J, Dzuris JL, Liebl ME, Fuenger S, Watkins DI, Sette A. Characterization of the peptide-binding specificity of Mamu-B*17 and identification of Mamu-B*17-restricted epitopes derived from simian immunodeficiency virus proteins. J Immunol 2002, 169:210-219.
117. Valentine LE, Loffredo JT, Bean AT, Leon EJ, MacNair CE, Beal DR, Piaskowski SM, Klimentidis YC, Lank SM, Wiseman RW. Infection with " escaped" virus variants impairs control of simian immunodeficiency virus SIVmac239 replication in Mamu-B*08-positive macaques. J Virol 2009, 83:11514-11527. 10.1128/JVI.01298-09, 2772717, 19726517.
118. Mudd PA, Martins MA, Ericsen AJ, Tully DC, Power KA, Bean AT, Piaskowski SM, Duan L, Seese A, Gladden AD. Vaccine-induced CD8+ T cells control AIDS virus replication. Nature 2012, 491:129-133. 10.1038/nature11443, 23023123.
119. Hoof I, Peters B, Sidney J, Pedersen LE, Sette A, Lund O, Buus S, Nielsen M. NetMHCpan, a method for MHC class I binding prediction beyond humans. Immunogenetics 2009, 61:1-13. 10.1007/s00251-008-0341-z, 3319061, 19002680.
120. McMichael AJ. Environmental and social influences on emerging infectious diseases: past, present and future. Philos Trans R Soc Lond B Biol Sci 2004, 359:1049-1058. 10.1098/rstb.2004.1480, 1693387, 15306389.
121. Silvers L, Inglis B, Labudovic A, Janssens PA, van Leeuwen BH, Kerr PJ. Virulence and pathogenesis of the MSW and MSD strains of Californian myxoma virus in European rabbits with genetic resistance to myxomatosis compared to rabbits with no genetic resistance. Virology 2006, 348:72-83. 10.1016/j.virol.2005.12.007, 16442580.
122. Wenink PW, Groen AF, Roelke-Parker ME, Prins HH. African buffalo maintain high genetic diversity in the major histocompatibility complex in spite of historically known population bottlenecks. Mol Ecol 1998, 7:1315-1322. 10.1046/j.1365-294x.1998.00463.x, 9787443.
123. Domingo M, Visa J, Pumarola M, Marco AJ, Ferrer L, Rabanal R, Kennedy S. Pathologic and immunocytochemical studies of morbillivirus infection in striped dolphins (Stenella coeruleoalba). Vet Pathol 1992, 29:1-10. 10.1177/030098589202900101, 1557861.
124. Geraci JR, St Aubin DJ, Barker IK, Webster RG, Hinshaw VS, Bean WJ, Ruhnke HL, Prescott JH, Early G, Baker AS. Mass mortality of harbor seals: pneumonia associated with influenza A virus. Science 1982, 215:1129-1131. 10.1126/science.7063847, 7063847.
125. Mellars P. Why did modern human populations disperse from Africa ca. 60,000 years ago? A new model. Proc Natl Acad Sci USA 2006, 103:9381-9386. 10.1073/pnas.0510792103, 1480416, 16772383.
126. Parham P, Ohta T. Population biology of antigen presentation by MHC class I molecules. Science 1996, 272:67-74. 10.1126/science.272.5258.67, 8600539.
127. Miura T, Brockman MA, Schneidewind A, Lobritz M, Pereyra F, Rathod A, Block BL, Brumme ZL, Brumme CJ, Baker B. HLA-B57/B*5801 human immunodeficiency virus type 1 elite controllers select for rare gag variants associated with reduced viral replication capacity and strong cytotoxic T-lymphocyte [corrected] recognition. J Virol 2009, 83:2743-2755. 10.1128/JVI.02265-08, 2648254, 19116253.
128. Schneidewind A, Brockman MA, Yang R, Adam RI, Li B, Le Gall S, Rinaldo CR, Craggs SL, Allgaier RL, Power KA. 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 2007, 81:12382-12393. 10.1128/JVI.01543-07, 2169010, 17804494.
129. Troyer RM, McNevin J, Liu Y, Zhang SC, Krizan RW, Abraha A, Tebit DM, Zhao H, Avila S, Lobritz MA. Variable fitness impact of HIV-1 escape mutations to cytotoxic T lymphocyte (CTL) response. PLoS Pathog 2009, 5:e1000365. 10.1371/journal.ppat.1000365, 2659432, 19343217.
130. Carrington M, Nelson GW, Martin MP, Kissner T, Vlahov D, Goedert JJ, Kaslow R, Buchbinder S, Hoots K, O'Brien SJ. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 1999, 283:1748-1752. 10.1126/science.283.5408.1748, 10073943.
131. Matthews PC, Listgarten J, Carlson JM, Payne R, Huang KH, Frater J, Goedhals D, Steyn D, van Vuuren C, Paioni P. Co-operative additive effects between HLA alleles in control of HIV-1. PLoS One 2012, 7:e47799. 10.1371/journal.pone.0047799, 3477121, 23094091.
132. Biella U, Haustein UF, Seifert S, Adler J, Schuppel KF, Eulenberger K. [Psoriasis in a female chimpanzee]. Hautarzt 1991, 42:322-323.
133. Taurog JD. Animal models of spondyloarthritis. Adv Exp Med Biol 2009, 649:245-254. 10.1007/978-1-4419-0298-6_18, 19731634.