Immunogenetics

, Volume 64, Issue 2, pp 131–141 | Cite as

Diversity of MHC class I haplotypes in cynomolgus macaques

  • Yusuke Saito
  • Taeko K. Naruse
  • Hirofumi Akari
  • Tetsuro Matano
  • Akinori Kimura
Original Paper

Abstract

Cynomolgus macaques are widely used as a primate model for human diseases associated with an immunological process. Because there are individual differences in immune responsiveness, which are controlled by the polymorphic nature of the major histocompatibility (MHC) locus, it is important to reveal the diversity of MHC in the model animal. In this study, we analyzed 26 cynomolgus macaques from five families for MHC class I genes. We identified 32 Mafa-A, 46 Mafa-B, 6 Mafa-I, and 3 Mafa-AG alleles in which 14, 20, 3, and 3 alleles were novel. There were 23 MHC class I haplotypes and each haplotype was composed of one to three Mafa-A alleles and one to five Mafa-B alleles. Family studies revealed that there were two haplotypes which contained two Mafa-A1 alleles. These observations demonstrated further the complexity of MHC class I locus in the Old World monkey.

Keywords

Cynomolgus macaque MHC Mafa class I gene Haplotype Polymorphism 

References

  1. Aarnink A, Dereuddre-Bosquet N, Vaslin B, Le Grand R, Winterton P, Apoil PA, Blancher A (2011a) Influence of the MHC genotype on the progression of experimental SIV infection in the Mauritian cynomolgus macaque. Immunogenetics 63:267–274PubMedCrossRefGoogle Scholar
  2. Aarnink A, Apoil PA, Takahashi I, Osada N, Blancher (2011b) Characterization of MHC class I transcripts of a Malaysian cynomolgus macaque by high-throughput pyrosequencing and EST libraries. Immunogenetics. doi:10.1007/s00251-011-0550-8
  3. Bonhomme M, Cuartero S, Blancher A, Crouau-Roy B (2009) Assessing natural introgression in 2 biomedical model species, the rhesus macaque (Macaca mulatta) and the long-tailed macaque (Macaca fascicularis). J Hered 100:158–169PubMedCrossRefGoogle Scholar
  4. Budde ML, Wiseman RW, Karl JA, Hanczaruk B, Simen BB, O’connor DH (2010) Characterization of Mauritian cynomolgus macaque major histocompatibility complex class I haplotypes by high-resolution pyrosequencing. Immunogenetics 62:773–780PubMedCrossRefGoogle Scholar
  5. Burwitz BJ, Pendley CJ, Greene JM, Detmer AM, Lhost JJ, Karl JA, Piaskowski SM, Rudersdorf RA, Wallace LT, Bimber BN, Loffredo JT, Cox DG, Bardet W, Hildebrand W, Wiseman RW, O’Connor SL, O’Connor DH (2009) Mauritian cynomolgus macaques share two exceptionally common major histocompatibility complex class I alleles that restrict simian immunodeficiency virus-specific CD8+ T cells. J Virol 83:6011–6019PubMedCrossRefGoogle Scholar
  6. Campbell KJ, Detmer AM, Karl JA, Wiseman RW, Blasky AJ, Hughes AL, Bimber BN, O’Connor SL, O’Connor DH (2009) Characterization of 47 MHC class I sequences in Filipino cynomolgus macaques. Immunogenetics 61:177–187PubMedCrossRefGoogle Scholar
  7. Doxiadis GG, de Groot N, Otting N, Blokhuis JH, Bontrop RE (2011) Genomic plasticity of the MHC class I A region in rhesus macaques: extensive haplotype diversity at the population level as revealed by microsatellites. Immunogenetics 63:73–83PubMedCrossRefGoogle Scholar
  8. Gibbs RA, Rogers J, Katze MG et al (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–234PubMedCrossRefGoogle Scholar
  9. Karl JA, Wiseman RW, Campbell KJ, Blasky AJ, Hughes AL, Ferguson B, Read DS, O’Connor DH (2008) Identification of MHC class I sequences in Chinese-origin rhesus macaques. Immunogenetics 60:37–46PubMedCrossRefGoogle Scholar
  10. Kita YF, Hosomichi K, Kohara S, Itoh Y, Ogasawara K, Tsuchiya H, Torii R, Inoko H, Blancher A, Kulski K, Shiina T (2009) MHC class I A loci polymorphism and diversity in three Southeast Asian populations of cynomolgus macaques. Immunogenetics 61:635–648PubMedCrossRefGoogle Scholar
  11. Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, Feldmann F, Alimonti JB, Fernando L, Li Y, Katze MG, Feldmann H, Kawaoka Y (2007) Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319–323PubMedCrossRefGoogle Scholar
  12. Krebs KC, Jin Z, Rudersdorf R, Hughes AL, O’Connor DH (2005) Unusually high frequency MHC class I alleles in Mauritian origin cynomolgus macaques. J Immunol 175:5230–5239PubMedGoogle Scholar
  13. Kulski JK, Anzai T, Shiina T, Inoko H (2004) Rhesus macaque class I duplicon structures, organization, and evolution within the alpha block of the major histocompatibility complex. Mol Biol Evol 21:2079–2091PubMedCrossRefGoogle Scholar
  14. Lawler JV, Endy TP, Hensley LE, Garrison A, Frinz EA, Lesar M, Baric RS, Kulesh DA, Norwood DA, Wasieloski LP, Ulrich MP, Slezak TR, Vitalis E, Hugging JW, Jahrling PB, Paragas J (2006) Cynomolgus macaque as an animal model for severe acute respiratory syndrome. PLoS Med 3:677–686CrossRefGoogle Scholar
  15. Loffredo JT, Bean AT, Beal DR, León EJ, May GE, Piaskowski SM, Furlott JR, Reed J, Musani SK, Rakasz EG, Friedrich TC, Wilson NA, Allison DB, Watkins DI (2008) Patterns of CD8+ immunodominance may influence the ability of Mamu-B*08-positive macaques to naturally control simian immunodeficiency virus SIVmac239 replication. J Virol 82:1723–1738PubMedCrossRefGoogle Scholar
  16. Matano T, Kobayashi M, Igarashi H, Takeda A, Nakamura H, Kano M, Sugimoto C, Mori K, Iida A, Hirata T, Hasegawa M, Yuasa T, Miyazawa M, Takahashi Y, Yasunami M, Kimura A, O’Connor DH, Watkins DI, Nagai Y (2004) Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J Exp Med 199:1709–1718PubMedCrossRefGoogle Scholar
  17. Mee ET, Berry N, Ham C, Sauermann U, Maggiorella MT, Martinon F, Verschoor EJ, Heeney JL, Le Grand R, Titti F, Almond N, Rose NJ (2009) Mhc haplotype H6 is associated with sustained control of SIVmac251 infection in Mauritian cynomolgus macaques. Immunogenetics 61:327–339PubMedCrossRefGoogle Scholar
  18. Naruse TK, Chen Z, Yanagida R, Yamashita T, Saito Y, Mori K, Akari H, Yasutomi Y, Miyazawa M, Matano T, Kimura A (2010) Diversity of MHC class I genes in Burmese-origin rhesus macaques. Immunogenetics 62:601–611PubMedCrossRefGoogle Scholar
  19. Otting N, deVos-Rouweler AJM, Heijmans CMC, de Groot NG, Doxiadis GG, Bontrop RE (2007) MHC class I A region diversity and polymorphism in macaque species. Immunogenetics 59:367–375PubMedCrossRefGoogle Scholar
  20. Otting N, Heijmans CM, van der Wiel M, de Groot NG, Doxiadis GG, Bontrop RE (2008) A snapshot of the Mamu-B genes and their allelic repertoire in rhesus macaques of Chinese origin. Immunogenetics 60:507–514PubMedCrossRefGoogle Scholar
  21. Otting N, Doxiadis GG, Bontrop RE (2009) Definition of Mafa-A and -B haplotypes in pedigreed cynomolgus macaques (Macaca fascicularis). Immunogenetics 61:745–753PubMedCrossRefGoogle Scholar
  22. Pendley CJ, Becker EA, Karl JA, Blasky AJ, Wiseman RW, Hughes AL, O’Connor SL, O’connor DH (2008) MHC class I characterization of Indonesian cynomolgus macaques. Immunogenetics 60:339–351PubMedCrossRefGoogle Scholar
  23. Robinson J, Waller MJ, Parham P, de Groot N, Bontrop R, Kennedy LJ, Stoehr P, Marsh SGE (2003) IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucl Acid Res 31:311–314CrossRefGoogle Scholar
  24. Rosner C, Kruse PH, Lübke T, Walter L (2010) Rhesus macaque MHC class I molecules show differential subcellular localization. Immunogenetics 62:149–158PubMedCrossRefGoogle Scholar
  25. Slukvin II, Lunn DD, Watkins DI, Golos TG (2000) Placental expression of the nonclassical MHC class I molecule Mamu-AG at implantation in the rhesus monkey. Proc Natl Acad Sci USA 97:9104–9109PubMedCrossRefGoogle Scholar
  26. Tanaka-Takahashi Y, Yasunami M, Naruse T, Hinohara K, Matano T, Mori K, Miyazawa M, Honda M, Yasutomi Y, Nagai Y, Kimura A (2007) Reference strand-mediated conformation analysis-based typing of multiple alleles in the rhesus macaque MHC class I Mamu-A and Mamu-B loci. Electrophoresis 28:918–924PubMedCrossRefGoogle Scholar
  27. Tsukamoto T, Dohki S, Ueno T, Kawada M, Takeda A, Yasunami M, Naruse T, Kimura A, Takiguchi M, Matano T (2008) Determination of a major histocompatibility complex class I restricting simian immunodeficiency virus Gag241-249 epitope. AIDS 22:993–998PubMedCrossRefGoogle Scholar
  28. Uda A, Tanabayashi K, Yamada YK, Akari H, Lee YJ, Mukai R, Terao K, Yamada A (2004) Detection of 14 alleles derived from the MHC class I A locus in cynomolgus monkeys. Immunogenetics 56:155–163PubMedCrossRefGoogle Scholar
  29. Uda A, Tanabayashi K, Fujita O, Hotta A, Terao K, Yamada A (2005) Identification of the MHC class I B locus in cynomolgus monkeys. Immunogenetics 57:189–197PubMedCrossRefGoogle Scholar
  30. Urvater JA, Otting N, Loehrke JH, Rudersdorf R, Slukvin II, Piekarcyk MS, Golos TG, Hughes AL, Bontrop RE, Watkins DI (2000) Mamu-I: a novel primate MHC class I B-related locus with unusually low variability. J Immunol 164:1386–1398PubMedGoogle Scholar
  31. Watanabe A, Shiina T, Shimizu S, Hosomichi K, Yanagiya K, Kita YF, Kimura T, Soeda E, Torii R, Ogasawara K, Kulski JK, Inoko H (2006) A BAC-based contig map of the cynomolgus macaque (Macaca fascicularis) major histocompatibility complex genomic region. Genomics 89:402–412PubMedCrossRefGoogle Scholar
  32. Wiseman RW, O’Connor DH (2007) Major histocompatibility complex-defined macaques in transplantation research. Transplant Rev 21:17–25CrossRefGoogle Scholar
  33. Wiseman RW, Wojcechowskyj JA, Greene JM, Blasly AJ, GoponT SomaT, FriedrichT C, O’Connor SL, O’Connor DH (2007) Simian immunodeficiency virus SIV mac239 infection of major histocompatibility complex-identical cynomolgus macaques from Mauritius. J Virol 81:349–361PubMedCrossRefGoogle Scholar
  34. Wiseman RW, Karl JA, Bimber BN, O’Leary CE, Lank SM, Tuscher JJ, Detmer AM, Bouffard P, Levenkova N, Turcotte CL, Szekeres E Jr, Wright C, Harkins T, O’Connor DH (2009) Major histocompatibility complex genotyping with massively parallel pyrosequencing. Nat Med 15:1322–1326PubMedCrossRefGoogle Scholar
  35. Wu J, Bassinger S, Montoya GD, Chavez L, Jones CE, Holder-Lockyer B, Masten B, Williams TM, Prilliman KR (2008) Allelic diversity within the high frequency Mamu-A2*05/Mane-A2*05(Mane-A*06)/Mafa-A2*05 family of macaque MHC-A loci. Tissue Antigens 72:29–38PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Yusuke Saito
    • 1
    • 2
  • Taeko K. Naruse
    • 1
  • Hirofumi Akari
    • 3
  • Tetsuro Matano
    • 4
    • 5
  • Akinori Kimura
    • 1
    • 2
  1. 1.Department of Molecular Pathogenesis, Medical Research InstituteTokyo Medical and Dental UniversityBunkyo-kuJapan
  2. 2.Laboratory of Genome Diversity, Graduate School of Biomedical ScienceTokyo Medical and Dental UniversityTokyoJapan
  3. 3.Primate Research InstituteKyoto UniversityInuyamaJapan
  4. 4.AIDS Research CenterNational Institute of Infectious DiseasesTokyoJapan
  5. 5.The Institute of Medical ScienceThe University of TokyoTokyoJapan

Personalised recommendations