AIDS in chimpanzees: the role of MHC genes

Abstract

The ancestral progenitor of common chimpanzees and bonobos experienced a selective sweep that ravaged its major histocompatibility complex (MHC) class I repertoire. The causative agent was probably an ancestral retrovirus, highly related to the contemporary HIV-1 strain, which initiated the acquired immunodeficiency syndrome pandemic in the human population. As a direct result, MHC class I allotypes with the capability of targeting conserved retroviral elements were enriched in the ancestral progenitor. Even today, the impact can be traced back by studying the functional capacities of the contemporary MHC class I allotypes of common chimpanzees. Viruses, however, have developed several strategies to manipulate the cell-surface expression of MHC class I genes. Monitoring the presence and absence of the MHC class I allotypes on the cell surface is conducted, for instance, by the hosts’ gene products of the killer cell immunoglobulin-like receptor (KIR) complex. Hence, one may wonder whether—in the future—any clues with regard to the signature of the MHC class I selective sweep might be unearthed for the KIR genes as well.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abi-Rached L, Moesta AK, Rajalingam R, Guethlein LA, Parham P (2010) Human-specific evolution and adaptation led to major qualitative differences in the variable receptors of human and chimpanzee natural killer cells. PLoS Genet 6:e1001192

    Article  PubMed  PubMed Central  Google Scholar 

  2. Adams EJ, Thomson G, Parham P (1999) Evidence for an HLA-C-like locus in the orangutan Pongo pygmaeus. Immunogenetics 49:865–871

    CAS  Article  PubMed  Google Scholar 

  3. Adams EJ, Cooper S, Thomson G, Parham P (2000) Common chimpanzees have greater diversity than humans at two of the three highly polymorphic MHC class I genes. Immunogenetics 51:410–424

    CAS  Article  PubMed  Google Scholar 

  4. Adams EJ, Cooper S, Parham P (2001) A novel, nonclassical MHC class I molecule specific to the common chimpanzee. J Immunol 167:3858–3869

    CAS  Article  PubMed  Google Scholar 

  5. Alter G, Heckerman D, Schneidewind A, Fadda L, Kadie CM, Carlson JM, Oniangue-Ndza C, Martin M, Li B, Khakoo SI, Carrington M, Allen TM, Altfeld M (2011) HIV-1 adaptation to NK-cell-mediated immune pressure. Nature 476:96–100

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Anzai T, Shiina T, Kimura N, Yanagiya K, Kohara S, Shigenari A, Yamagata T, Kulski JK, Naruse TK, Fujimori Y, Fukuzumi Y, Yamazaki M, Tashiro H, Iwamoto C, Umehara Y, Imanishi T, Meyer A, Ikeo K, Gojobori T, Bahram S, Inoko H (2003) Comparative sequencing of human and chimpanzee MHC class I regions unveils insertions/deletions as the major path to genomic divergence. Proc Natl Acad Sci U S A 100:7708–7713

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Apps R, Del Prete GQ, Chatterjee P, Lara A, Brumme ZL, Brockman MA, Neil S, Pickering S, Schneider DK, Piechocka-Trocha A, Walker BD, Thomas R, Shaw GM, Hahn BH, Keele BF, Lifson JD, Carrington M (2016) HIV-1 Vpu mediates HLA-C downregulation. Cell Host Microbe 19:686–695

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Auton A, Fledel-Alon A, Pfeifer S, Venn O, Segurel L, Street T, Leffler EM, Bowden R, Aneas I, Broxholme J, Humburg P, Iqbal Z, Lunter G, Maller J, Hernandez RD, Melton C, Venkat A, Nobrega MA, Bontrop R, Myers S, Donnelly P, Przeworski M, McVean G (2012) A fine-scale chimpanzee genetic map from population sequencing. Science 336:193–198

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Bailes E, Gao F, Bibollet-Ruche F, Courgnaud V, Peeters M, Marx PA, Hahn BH, Sharp PM (2003) Hybrid origin of SIV in chimpanzees. Science 300:1713

    CAS  Article  PubMed  Google Scholar 

  10. Balla-Jhagjhoorsingh SS, Koopman G, Mooij P, Haaksma TG, Teeuwsen VJ, Bontrop RE, Heeney JL (1999) Conserved CTL epitopes shared between HIV-infected human long-term survivors and chimpanzees. J Immunol 162:2308–2314

    CAS  PubMed  Google Scholar 

  11. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C, Rozenbaum W, Montagnier L (1983) Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220:868–871

    CAS  Article  PubMed  Google Scholar 

  12. Bashirova AA, Thomas R, Carrington M (2011) HLA/KIR restraint of HIV: surviving the fittest. Annu rev Immunol 29:295–317

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Berezikov E, Thuemmler F, van Laake LW, Kondova I, Bontrop R, Cuppen E, Plasterk RH (2006) Diversity of microRNAs in human and chimpanzee brain. Nat Genet 38:1375–1377

    CAS  Article  PubMed  Google Scholar 

  14. Borghans JA, Molgaard A, de Boer RJ, Kesmir C (2007) HLA alleles associated with slow progression to AIDS truly prefer to present HIV-1 p24. PLoS One 2:e920

    Article  PubMed  PubMed Central  Google Scholar 

  15. Boue V, Locatelli S, Boucher F, Ayouba A, Butel C, Esteban A, Okouga AP, Ndoungouet A, Motsch P, Le Flohic G, Ngari P, Prugnolle F, Ollomo B, Rouet F, Liegeois F (2015) High rate of simian immunodeficiency virus (SIV) infections in wild chimpanzees in northeastern Gabon. Viruses 7:4997–5015

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Bowden R, MacFie TS, Myers S, Hellenthal G, Nerrienet E, Bontrop RE, Freeman C, Donnelly P, Mundy NI (2012) Genomic tools for evolution and conservation in the chimpanzee: Pan troglodytes Ellioti is a genetically distinct population. PLoS Genet 8:e1002504

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Braud V, Jones EY, McMichael A (1997) The human major histocompatibility complex class Ib molecule HLA-E binds signal sequence-derived peptides with primary anchor residues at positions 2 and 9. Eur J Immunol 27:1164–1169

    CAS  Article  PubMed  Google Scholar 

  18. Braud VM, Allan DS, O’Callaghan CA, Soderstrom K, D’Andrea A, Ogg GS, Lazetic S, Young NT, Bell JI, Phillips JH, Lanier LL, McMichael AJ (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795–799

    CAS  Article  PubMed  Google Scholar 

  19. Britten RJ (2002) Divergence between samples of chimpanzee and human DNA sequences is 5%, counting indels. Proc Natl Acad Sci U S A 99:13633–13635

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Canavez F, Young NT, Guethlein LA, Rajalingam R, Khakoo SI, Shum BP, Parham P (2001) Comparison of chimpanzee and human leukocyte Ig-like receptor genes reveals framework and rapidly evolving genes. J Immunol 167:5786–5794

    CAS  Article  PubMed  Google Scholar 

  21. Carrington M, O’Brien SJ (2003) The influence of HLA genotype on AIDS. Annu Rev Med 54:535–551

    CAS  Article  PubMed  Google Scholar 

  22. Chappell P, Meziane el K, Harrison M, Magiera L, Hermann C, Mears L, Wrobel AG, Durant C, Nielsen LL, Buus S, Ternette N, Mwangi W, Butter C, Nair V, Ahyee T, Duggleby R, Madrigal A, Roversi P, Lea SM, Kaufman J (2015) Expression levels of MHC class I molecules are inversely correlated with promiscuity of peptide binding. Elife 4:e05345

    Article  PubMed  PubMed Central  Google Scholar 

  23. Cohen GB, Gandhi RT, Davis DM, Mandelboim O, Chen BK, Strominger JL, Baltimore D (1999) The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10:661–671

    CAS  Article  PubMed  Google Scholar 

  24. Colonna M, Samaridis J (1995) Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268:405–408

    CAS  Article  PubMed  Google Scholar 

  25. Dalmasso C, Carpentier W, Meyer L, Rouzioux C, Goujard C, Chaix ML, Lambotte O, Avettand-Fenoel V, Le Clerc S, de Senneville LD, Deveau C, Boufassa F, Debre P, Delfraissy JF, Broet P, Theodorou I, Association AGW (2008) 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 3:e3907

    Article  PubMed  PubMed Central  Google Scholar 

  26. de Groot NG, Otting N, Arguello R, Watkins DI, Doxiadis GG, Madrigal JA, Bontrop RE (2000) Major histocompatibility complex class I diversity in a West African chimpanzee population: implications for HIV research. Immunogenetics 51:398–409

    Article  PubMed  Google Scholar 

  27. de Groot NG, Otting N, Doxiadis GG, Balla-Jhagjhoorsingh SS, Heeney JL, van Rood JJ, Gagneux P, Bontrop RE (2002) Evidence for an ancient selective sweep in the MHC class I gene repertoire of chimpanzees. Proc Natl Acad Sci U S A 99:11748–11753

    Article  PubMed  PubMed Central  Google Scholar 

  28. de Groot NG, Garcia CA, Verschoor EJ, Doxiadis GG, Marsh SG, Otting N, Bontrop RE (2005) Reduced MIC gene repertoire variation in West African chimpanzees as compared to humans. Mol Biol Evol 22:1375–1385

    Article  PubMed  Google Scholar 

  29. 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 (2008) Pinpointing a selective sweep to the chimpanzee MHC class I region by comparative genomics. Mol Ecol 17:2074–2088

    Article  PubMed  Google Scholar 

  30. de Groot NG, Heijmans CM, Zoet YM, de Ru AH, Verreck FA, van Veelen PA, Drijfhout JW, Doxiadis GG, Remarque EJ, Doxiadis II, van Rood JJ, Koning F, Bontrop RE (2010) 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 U S A 107:15175–15180

    Article  PubMed  PubMed Central  Google Scholar 

  31. de Groot NG, Otting N, Robinson J, Blancher A, Lafont BA, Marsh SG, O’Connor DH, Shiina T, Walter L, Watkins DI, Bontrop RE (2012) Nomenclature report on the major histocompatibility complex genes and alleles of Great Ape, Old and New World monkey species. Immunogenetics 64:615–631

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. de Groot NG, Bontrop RE (2013) The HIV-1 pandemic: does the selective sweep in chimpanzees mirror humankind’s future? Retrovirology 10:53

    Article  PubMed  PubMed Central  Google Scholar 

  33. de Groot NG, Heijmans CM, van der Wiel MK, Blokhuis JH, Mulder A, Guethlein LA, Doxiadis GG, Claas FH, Parham P, Bontrop RE (2016) Complex MHC class I gene transcription profiles and their functional impact in orangutans. J Immunol 196:750–758

    Article  PubMed  Google Scholar 

  34. de Groot NG, Heijmans CM, Helsen P, Otting N, Pereboom Z, Stevens JMG, Bontrop RE (2017) Limited MHC class I intron 2 repertoire variation in bonobos. Immunogenetics (In Press)

  35. de Manuel M, Kuhlwilm M, Frandsen P, Sousa VC, Desai T, Prado-Martinez J, Hernandez-Rodriguez J, Dupanloup I, Lao O, Hallast P, Schmidt JM, Heredia-Genestar JM, Benazzo A, Barbujani G, Peter BM, Kuderna LF, Casals F, Angedakin S, Arandjelovic M, Boesch C, Kuhl H, Vigilant L, Langergraber K, Novembre J, Gut M, Gut I, Navarro A, Carlsen F, Andres AM, Siegismund HR, Scally A, Excoffier L, Tyler-Smith C, Castellano S, Xue Y, Hvilsom C, Marques-Bonet T (2016) Chimpanzee genomic diversity reveals ancient admixture with bonobos. Science 354:477–481

    Article  PubMed  Google Scholar 

  36. Enard W, Khaitovich P, Klose J, Zollner S, Heissig F, Giavalisco P, Nieselt-Struwe K, Muchmore E, Varki A, Ravid R, Doxiadis GM, Bontrop RE, Paabo S (2002) Intra- and interspecific variation in primate gene expression patterns. Science 296:340–343

    CAS  Article  PubMed  Google Scholar 

  37. Etienne L, Nerrienet E, LeBreton M, Bibila GT, Foupouapouognigni Y, Rousset D, Nana A, Djoko CF, Tamoufe U, Aghokeng AF, Mpoudi-Ngole E, Delaporte E, Peeters M, Wolfe ND, Ayouba A (2011) Characterization of a new simian immunodeficiency virus strain in a naturally infected Pan troglodytes troglodytes chimpanzee with AIDS related symptoms. Retrovirology 8:4

  38. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, Weale M, Zhang K, Gumbs C, Castagna A, Cossarizza A, Cozzi-Lepri A, De Luca A, Easterbrook P, Francioli P, Mallal S, Martinez-Picado J, Miro JM, Obel N, Smith JP, Wyniger J, Descombes P, Antonarakis SE, Letvin NL, McMichael AJ, Haynes BF, Telenti A, Goldstein DB (2007) A whole-genome association study of major determinants for host control of HIV-1. Science 317:944–947

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Gagneux P, Wills C, Gerloff U, Tautz D, Morin PA, Boesch C, Fruth B, Hohmann G, Ryder OA, Woodruff DS (1999) Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc Natl Acad Sci U S A 96:5077–5082

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Geller R, Adams EJ, Guethlein LA, Little AM, Madrigal JA, Parham P (2002) Linkage of Patr-AL to Patr-A and -B in the major histocompatibility complex of the common chimpanzee (Pan troglodytes). Immunogenetics 54:212–215

    CAS  Article  PubMed  Google Scholar 

  41. Gleimer M, Wahl AR, Hickman HD, Abi-Rached L, Norman PJ, Guethlein LA, Hammond JA, Draghi M, Adams EJ, Juo S, Jalili R, Gharizadeh B, Ronaghi M, Garcia KC, Hildebrand WH, Parham P (2011) 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 186:1575–1588

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Gonzalez JP, Prugnolle F, Leroy E (2013) Men, primates, and germs: an ongoing affair. Curr Top Microbiol Immunol 365:337–353

    PubMed  Google Scholar 

  43. Goulder PJ, Bunce M, Krausa P, McIntyre K, Crowley S, Morgan B, Edwards A, Giangrande P, Phillips RE, McMichael AJ (1996) Novel, cross-restricted, conserved, and immunodominant cytotoxic T lymphocyte epitopes in slow progressors in HIV type 1 infection. AIDS Res Hum Retrovir 12:1691–1698

    CAS  Article  PubMed  Google Scholar 

  44. Goyos A, Guethlein LA, Horowitz A, Hilton HG, Gleimer M, Brodsky FM, Parham P (2015) A distinctive cytoplasmic tail contributes to low surface expression and intracellular retention of the Patr-AL MHC class I molecule. J Immunol 195:3725–3736

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Guethlein LA, Flodin LR, Adams EJ, Parham P (2002) NK cell receptors of the orangutan (Pongo pygmaeus): a pivotal species for tracking the coevolution of killer cell Ig-like receptors with MHC-C. J Immunol 169:220–229

    CAS  Article  PubMed  Google Scholar 

  46. Guethlein LA, Norman PJ, Hilton HG, Parham P (2015) Co-evolution of MHC class I and variable NK cell receptors in placental mammals. Immunol Rev 267:259–282

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Hahn BH, Shaw GM, De Cock KM, Sharp PM (2000) AIDS as a zoonosis: scientific and public health implications. Science 287:607–614

    CAS  Article  PubMed  Google Scholar 

  48. Hans JB, Bergl RA, Vigilant L (2017) Gorilla MHC class I gene and sequence variation in a comparative context. Immunogenetics

  49. Heeney JL, Dalgleish AG, Weiss RA (2006) Origins of HIV and the evolution of resistance to AIDS. Science 313:462–466

    CAS  Article  PubMed  Google Scholar 

  50. Horstmann DM, Melnick JL (1950) Poliomyelitis in chimpanzees; studies in homologous and heterologous immunity following inapparent infection. J Exp med 91:573–597

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Huet T, Cheynier R, Meyerhans A, Roelants G, Wain-Hobson S (1990) Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature 345:356–359

    CAS  Article  PubMed  Google Scholar 

  52. International HIVCS, Pereyra F, Jia X, McLaren PJ, Telenti A, de Bakker PI, Walker BD, Ripke S, Brumme CJ, Pulit SL, Carrington M, Kadie CM, Carlson JM, Heckerman D, Graham RR, Plenge RM, Deeks SG, Gianniny L, Crawford G, Sullivan J, Gonzalez E, Davies L, Camargo A, Moore JM, Beattie N, Gupta S, Crenshaw A, Burtt NP, Guiducci C, Gupta N, Gao X, Qi Y, Yuki Y, Piechocka-Trocha A, Cutrell E, Rosenberg R, Moss KL, Lemay P, O’Leary J, Schaefer T, Verma P, Toth I, Block B, Baker B, Rothchild A, Lian J, Proudfoot J, Alvino DM, Vine S, Addo MM, Allen TM, Altfeld M, Henn MR, Le Gall S, Streeck H, Haas DW, Kuritzkes DR, Robbins GK, Shafer RW, Gulick RM, Shikuma CM, Haubrich R, Riddler S, Sax PE, Daar ES, Ribaudo HJ, Agan B, Agarwal S, Ahern RL, Allen BL, Altidor S, Altschuler EL, Ambardar S, Anastos K, Anderson B, Anderson V, Andrady U, Antoniskis D, Bangsberg D, Barbaro D, Barrie W, Bartczak J, Barton S, Basden P, Basgoz N, Bazner S, Bellos NC, Benson AM, Berger J, Bernard NF, Bernard AM, Birch C, Bodner SJ, Bolan RK, Boudreaux ET, Bradley M, Braun JF, Brndjar JE, Brown SJ, Brown K et al (2010) The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 330:1551–1557

    Article  Google Scholar 

  53. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, Goedert JJ, Winkler C, O’Brien SJ, Rinaldo C, Detels R, Blattner W, Phair J, Erlich H, Mann DL (1996) Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 2:405–411

    CAS  Article  PubMed  Google Scholar 

  54. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, Li Y, Learn GH, Beasley TM, Schumacher-Stankey J, Wroblewski E, Mosser A, Raphael J, Kamenya S, Lonsdorf EV, Travis DA, Mlengeya T, Kinsel MJ, Else JG, Silvestri G, Goodall J, Sharp PM, Shaw GM, Pusey AE, Hahn BH (2009) Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460:515–519

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Khakoo SI, Rajalingam R, Shum BP, Weidenbach K, Flodin L, Muir DG, Canavez F, Cooper SL, Valiante NM, Lanier LL, Parham P (2000) Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12:687–698

    CAS  Article  PubMed  Google Scholar 

  56. Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, Chetty S, Rathnavalu P, Moore C, Pfafferott KJ, Hilton L, Zimbwa P, Moore S, Allen T, Brander C, Addo MM, Altfeld M, James I, Mallal S, Bunce M, Barber LD, Szinger J, Day C, Klenerman P, Mullins J, Korber B, Coovadia HM, Walker BD, Goulder PJ (2004) Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432:769–775

    CAS  Article  PubMed  Google Scholar 

  57. Lanier LL (2005) NK cell recognition. Annu Rev Immunol 23:225–274

    CAS  Article  PubMed  Google Scholar 

  58. Leendertz SA, Locatelli S, Boesch C, Kucherer C, Formenty P, Liegeois F, Ayouba A, Peeters M, Leendertz FH (2011) No evidence for transmission of SIVwrc from western red colobus monkeys (Piliocolobus badius badius) to wild West African chimpanzees (Pan troglodytes Verus) despite high exposure through hunting. BMC Microbiol 11:24

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. Li Y, Ndjango JB, Learn GH, Ramirez MA, Keele BF, Bibollet-Ruche F, Liu W, Easlick JL, Decker JM, Rudicell RS, Inogwabini BI, Ahuka-Mundeke S, Leendertz FH, Reynolds V, Muller MN, Chancellor RL, Rundus AS, Simmons N, Worobey M, Shaw GM, Peeters M, Sharp PM, Hahn BH (2012) Eastern chimpanzees, but not bonobos, represent a simian immunodeficiency virus reservoir. J Virol 86:10776–10791

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. Locatelli S, Harrigan RJ, Sesink Clee PR, Mitchell MW, McKean KA, Smith TB, Gonder MK (2016) Why are Nigeria-Cameroon chimpanzees (Pan troglodytes Ellioti) free of SIVcpz infection? PLoS One 11:e0160788

    Article  PubMed  PubMed Central  Google Scholar 

  61. Maccari G, Robinson J, Ballingall K, Guethlein LA, Grimholt U, Kaufman J, Ho CS, de Groot NG, Flicek P, Bontrop RE, Hammond JA, Marsh SG (2017) IPD-MHC 2.0: an improved inter-species database for the study of the major histocompatibility complex. Nucleic Acids res 45:D860–D864

    Article  PubMed  Google Scholar 

  62. MacFie TS, Nerrienet E, de Groot NG, Bontrop RE, Mundy NI (2009) Patterns of diversity in HIV-related loci among subspecies of chimpanzee: concordance at CCR5 and differences at CXCR4 and CX3CR1. Mol Biol Evol 26:719–727

    CAS  Article  PubMed  Google Scholar 

  63. Maibach V, Hans JB, Hvilsom C, Marques-Bonet T, Vigilant L (2017) MHC class I diversity in chimpanzees and bonobos. Immunogenetics (In Press)

  64. Mallick S, Li H, Lipson M, Mathieson I, Gymrek M, Racimo F, Zhao M, Chennagiri N, Nordenfelt S, Tandon A, Skoglund P, Lazaridis I, Sankararaman S, Fu Q, Rohland N, Renaud G, Erlich Y, Willems T, Gallo C, Spence JP, Song YS, Poletti G, Balloux F, van Driem G, de Knijff P, Romero IG, Jha AR, Behar DM, Bravi CM, Capelli C, Hervig T, Moreno-Estrada A, Posukh OL, Balanovska E, Balanovsky O, Karachanak-Yankova S, Sahakyan H, Toncheva D, Yepiskoposyan L, Tyler-Smith C, Xue Y, Abdullah MS, Ruiz-Linares A, Beall CM, Di Rienzo A, Jeong C, Starikovskaya EB, Metspalu E, Parik J, Villems R, Henn BM, Hodoglugil U, Mahley R, Sajantila A, Stamatoyannopoulos G, Wee JT, Khusainova R, Khusnutdinova E, Litvinov S, Ayodo G, Comas D, Hammer MF, Kivisild T, Klitz W, Winkler CA, Labuda D, Bamshad M, Jorde LB, Tishkoff SA, Watkins WS, Metspalu M, Dryomov S, Sukernik R, Singh L, Thangaraj K, Paabo S, Kelso J, Patterson N, Reich D (2016) The Simons genome diversity project: 300 genomes from 142 diverse populations. Nature 538:201–206

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Marsh SG (2017) Nomenclature for factors of the HLA system, update December 2016. Hum Immunol

  66. McAdam SN, Boyson JE, Liu X, Garber TL, Hughes AL, Bontrop RE, Watkins DI (1995) Chimpanzee MHC class I A locus alleles are related to only one of the six families of human A locus alleles. J Immunol 154:6421–6429

    CAS  PubMed  Google Scholar 

  67. Nakimuli A, Chazara O, Hiby SE, Farrell L, Tukwasibwe S, Jayaraman J, Traherne JA, Trowsdale J, Colucci F, Lougee E, Vaughan RW, Elliott AM, Byamugisha J, Kaleebu P, Mirembe F, Nemat-Gorgani N, Parham P, Norman PJ, Moffett A (2015) A KIR B centromeric region present in Africans but not Europeans protects pregnant women from pre-eclampsia. Proc Natl Acad Sci U S A 112:845–850

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. Nielsen R, Akey JM, Jakobsson M, Pritchard JK, Tishkoff S, Willerslev E (2017) Tracing the peopling of the world through genomics. Nature 541:302–310

    CAS  Article  PubMed  Google Scholar 

  69. Novembre FJ, Saucier M, Anderson DC, Klumpp SA, O’Neil SP, Brown CR 2nd, Hart CE, Guenthner PC, Swenson RB, McClure HM (1997) Development of AIDS in a chimpanzee infected with human immunodeficiency virus type 1. J Virol 71:4086–4091

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Novembre FJ, de Rosayro J, Nidtha S, O’Neil SP, Gibson TR, Evans-Strickfaden T, Hart CE, McClure HM (2001) Rapid CD4(+) T-cell loss induced by human immunodeficiency virus type 1(NC) in uninfected and previously infected chimpanzees. J Virol 75:1533–1539

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  71. Parham P, Moffett A (2013) Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat Rev Immunol 13:133–144

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. Parham P (2015) Co-evolution of lymphocyte receptors with MHC class I. Immunol rev 267:1–5

    Article  PubMed  Google Scholar 

  73. Pawlak EN, Dikeakos JD (2015) HIV-1 Nef: a master manipulator of the membrane trafficking machinery mediating immune evasion. Biochim Biophys Acta 1850:733–741

    CAS  Article  PubMed  Google Scholar 

  74. Peeters M, Honore C, Huet T, Bedjabaga L, Ossari S, Bussi P, Cooper RW, Delaporte E (1989) Isolation and partial characterization of an HIV-related virus occurring naturally in chimpanzees in Gabon. Aids 3:625–630

    CAS  Article  PubMed  Google Scholar 

  75. Peeters M, Fransen K, Delaporte E, Van den Haesevelde M, Gershy-Damet GM, Kestens L, van der Groen G, Piot P (1992) Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wild-captured chimpanzee. Aids 6:447–451

    CAS  Article  PubMed  Google Scholar 

  76. Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, Lorente-Galdos B, Veeramah KR, Woerner AE, O’Connor TD, Santpere G, Cagan A, Theunert C, Casals F, Laayouni H, Munch K, Hobolth A, Halager AE, Malig M, Hernandez-Rodriguez J, Hernando-Herraez I, Prufer K, Pybus M, Johnstone L, Lachmann M, Alkan C, Twigg D, Petit N, Baker C, Hormozdiari F, Fernandez-Callejo M, Dabad M, Wilson ML, Stevison L, Camprubi C, Carvalho T, Ruiz-Herrera A, Vives L, Mele M, Abello T, Kondova I, Bontrop RE, Pusey A, Lankester F, Kiyang JA, Bergl RA, Lonsdorf E, Myers S, Ventura M, Gagneux P, Comas D, Siegismund H, Blanc J, Agueda-Calpena L, Gut M, Fulton L, Tishkoff SA, Mullikin JC, Wilson RK, Gut IG, Gonder MK, Ryder OA, Hahn BH, Navarro A, Akey JM, Bertranpetit J, Reich D, Mailund T, Schierup MH, Hvilsom C, Andres AM, Wall JD, Bustamante CD, Hammer MF, Eichler EE, Marques-Bonet T (2013) Great ape genetic diversity and population history. Nature 499:471–475

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  77. Prince AM, Brotman B, Lee DH, Andrus L, Valinsky J, Marx P (2002) Lack of evidence for HIV type 1-related SIVcpz infection in captive and wild chimpanzees (Pan troglodytes Verus) in West Africa. AIDS Res Hum Retrovir 18:657–660

    Article  PubMed  Google Scholar 

  78. Rajalingam R, Hong M, Adams EJ, Shum BP, Guethlein LA, Parham P (2001) Short KIR haplotypes in pygmy chimpanzee (bonobo) resemble the conserved framework of diverse human KIR haplotypes. J Exp Med 193:135–146

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  79. Robinson J, Mistry K, McWilliam H, Lopez R, Marsh SG (2010) IPD—the Immuno Polymorphism Database. Nucleic Acids Res 38:D863–D869

    CAS  Article  PubMed  Google Scholar 

  80. Robinson J, Halliwell JA, Hayhurst JD, Flicek P, Parham P, Marsh SG (2015) The IPD and IMGT/HLA database: allele variant databases. Nucleic Acids Res 43:D423–D431

    CAS  Article  PubMed  Google Scholar 

  81. Rolland M, Heckerman D, Deng W, Rousseau CM, Coovadia H, Bishop K, Goulder PJ, Walker BD, Brander C, Mullins JI (2008) Broad and Gag-biased HIV-1 epitope repertoires are associated with lower viral loads. PLoS One 3:e1424

    Article  PubMed  PubMed Central  Google Scholar 

  82. Rolland M (2016) HIV-1 immune evasion-a threat to effective vaccines? Nat Med 22:580–581

    Article  PubMed  Google Scholar 

  83. Sambrook JG, Bashirova A, Palmer S, Sims S, Trowsdale J, Abi-Rached L, Parham P, Carrington M, Beck S (2005) Single haplotype analysis demonstrates rapid evolution of the killer immunoglobulin-like receptor (KIR) loci in primates. Genome Res 15:25–35

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  84. Shepherd BL, Ferrand R, Munyati S, Folkard S, Boyd K, Bandason T, Jallow S, Rowland-Jones SL, Yindom LM (2015) HLA correlates of long-term survival in vertically infected HIV-1-positive adolescents in Harare, Zimbabwe. AIDS Res Hum Retrovir 31:504–507

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  85. Sidney J, Peters B, Frahm N, Brander C, Sette A (2008) HLA class I supertypes: a revised and updated classification. BMC Immunol 9:1

    Article  PubMed  PubMed Central  Google Scholar 

  86. Tregaskes CA, Harrison M, Sowa AK, van Hateren A, Hunt LG, Vainio O, Kaufman J (2016) Surface expression, peptide repertoire, and thermostability of chicken class I molecules correlate with peptide transporter specificity. Proc Natl Acad Sci U S A 113:692–697

    CAS  Article  PubMed  Google Scholar 

  87. Trowsdale J (2001) Genetic and functional relationships between MHC and NK receptor genes. Immunity 15:363–374

    CAS  Article  PubMed  Google Scholar 

  88. Trowsdale J, Knight JC (2013) Major histocompatibility complex genomics and human disease. Annu Rev Genomics Hum Genet 14:301–323

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  89. van Deutekom HW, Hoof I, Bontrop RE, Kesmir C (2011) A comparative analysis of viral peptides presented by contemporary human and chimpanzee MHC class I molecules. J Immunol 187:5995–6001

    Article  PubMed  Google Scholar 

  90. Van Heuverswyn F, Li Y, Bailes E, Neel C, Lafay B, Keele BF, Shaw KS, Takehisa J, Kraus MH, Loul S, Butel C, Liegeois F, Yangda B, Sharp PM, Mpoudi-Ngole E, Delaporte E, Hahn BH, Peeters M (2007) Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology 368:155–171

    Article  PubMed  Google Scholar 

  91. Vermunt MW, Tan SC, Castelijns B, Geeven G, Reinink P, de Bruijn E, Kondova I, Persengiev S, Netherlands Brain B, Bontrop R, Cuppen E, de Laat W, Creyghton MP (2016) Epigenomic annotation of gene regulatory alterations during evolution of the primate brain. Nat Neurosci 19:494–503

    CAS  Article  PubMed  Google Scholar 

  92. Vilches C, Parham P (2002) KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 20:217–251

    CAS  Article  PubMed  Google Scholar 

  93. Vossen MT, Westerhout EM, Soderberg-Naucler C, Wiertz EJ (2002) Viral immune evasion: a masterpiece of evolution. Immunogenetics 54:527–542

    CAS  Article  PubMed  Google Scholar 

  94. Wetterbom A, Sevov M, Cavelier L, Bergstrom TF (2006) Comparative genomic analysis of human and chimpanzee indicates a key role for indels in primate evolution. J Mol Evol 63:682–690

    CAS  Article  PubMed  Google Scholar 

  95. Wroblewski EE, Norman PJ, Guethlein LA, Rudicell RS, Ramirez MA, Li Y, Hahn BH, Pusey AE, Parham P (2015) Signature patterns of MHC diversity in three Gombe communities of wild chimpanzees reflect fitness in reproduction and immune defense against SIVcpz. PLoS Biol 13:e1002144

    Article  PubMed  PubMed Central  Google Scholar 

  96. Wroblewski EE, Guethlein LA, Norman PJ, Li Y, Shaw CM, Han AS, Ndjango JN, Ahuka-Mundeke S, Georgiev AV, Peeters M, Hahn BH, Parham P (2017) Bonobos maintain immune system diversity with three functional types of MHC-B. J Immunol

  97. Zipeto D, Beretta A (2012) HLA-C and HIV-1: friends or foes? Retrovirology 9:39

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank D. Devine for editing the manuscript and F. van Hassel for preparing the figures.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Natasja G. de Groot.

Additional information

This article is published in the Special Issue MHC Genes and Their Ligands in Health and Disease with Editor Prof. Ronald Bontrop.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

de Groot, N.G., Heijmans, C.M.C. & Bontrop, R.E. AIDS in chimpanzees: the role of MHC genes. Immunogenetics 69, 499–509 (2017). https://doi.org/10.1007/s00251-017-1006-6

Download citation

Keywords

  • Chimpanzees
  • Selective sweep
  • Selection
  • Repertoire reduction