Haplotype diversity generated by ancient recombination-like events in the MHC of Indian rhesus macaques

Immunogenetics

Volumn 65, Issue 8, 2013, Pages 569-584

  Doxiadis, Gaby G M ^a   De Groot, Nanine ^a   Otting, Nel ^a   De Vos Rouweler, Annemiek J M ^a   Bolijn, Maria J ^a   Heijmans, Corrine M C ^a   De Groot, Natasja G ^a   Van Der Wiel, Marit K H ^a   Remarque, Edmond J ^a   Vangenot, Christelle ^b   Nunes, José M ^b   Sanchez Mazas, Alicia ^b   Bontrop, Ronald E ^a,c  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Evolution; Haplotypes; Macaques; MHC; Microsatellites; Non human primates

Indexed keywords

GENOMIC DNA; HLA A ANTIGEN; HLA B ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN;

ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; CLONING; COPY NUMBER VARIATION; EVOLUTION; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC ORIGIN; HAPLOTYPE; INDIAN; INDONESIA; MOUSE; NONHUMAN; PLEISTOCENE; POPULATION; PRIORITY JOURNAL; PROGENY; RHESUS MONKEY;

ANIMALS; CELL LINE; CHROMOSOMES, MAMMALIAN; EVOLUTION, MOLECULAR; EXONS; FEMALE; GENETIC VARIATION; GENOTYPING TECHNIQUES; HAPLOTYPES; INDIA; LINKAGE DISEQUILIBRIUM; MACACA MULATTA; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MICROSATELLITE REPEATS; MYANMAR; PEDIGREE; RECOMBINATION, GENETIC;

ANIMALIA; MACACA; MACACA FASCICULARIS; MACACA MULATTA; PRIMATES;

EID: 84880513414     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-013-0707-8     Document Type: Article

References (66)

1. Averdam A, Seelke S, Grutzner I, Rosner C, Roos C, Westphal N, Stahl-Hennig C, Muppala V, Schrod A, Sauermann U, Dressel R, Walter L (2007) Genotyping and segregation analyses indicate the presence of only two functional MIC genes in rhesus macaques. Immunogenetics 59:247-251
2. Benjamini Y, and,Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Annals of Statistics1165-1188
3. Blancher A, Tisseyre P, Dutaur M, Apoil PA, Maurer C, Quesniaux V, Raulf F, Bigaud M, Abbal M (2006) Study of cynomolgus monkey (Macaca fascicularis) MhcDRB (Mafa-DRB) polymorphism in two populations. Immunogenetics 58:269-282
4. Blancher A, Aarnink A, Tanaka K, Ota M, Inoko H, Yamanaka H, Nakagawa H, Apoil PA, Shiina T (2012) Study of cynomolgus monkey (Macaca fascicularis) Mhc DRB gene polymorphism in four populations. Immunogenetics 64:605-614
5. Bonhomme M et al (2008) Genomic plasticity of the immune-related Mhc class I B region in macaque species. BMC Genomics 9:514
6. Bontrop RE, Otting N, Slierendregt BL, Lanchbury JS (1995) Evolution of major histocompatibility complex polymorphisms and T-cell receptor diversity in primates. Immunol Rev 143:33-62
7. Bontrop RE, Otting N, de Groot NG, Doxiadis GG (1999) Major histocompatibility complex class II polymorphisms in primates. Immunol Rev 167:339-350
8. Boyson JE, Shufflebotham C, Cadavid LF, Urvater JA, Knapp LA, Hughes AL, Watkins DI (1996) The MHC class I genes of the rhesus monkey. Different evolutionary histories of MHC class I and II genes in primates. J Immunol 156:4656-4665
9. 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 62:773-780
10. 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 61:177-187
11. Dawkins R, Leelayuwat C, Gaudieri S, Tay G, Hui J, Cattley S, Martinez P, Kulski J (1999) Genomics of the major histocompatibility complex: haplotypes, duplication, retroviruses and disease. Immunol Rev 167:275-304
12. Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE (2004) Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res 14:1501-1515
13. de Groot N, Doxiadis GG, De Groot NG, Otting N, Heijmans C, Rouweler AJ, Bontrop RE (2004) Genetic makeup of the DR region in rhesus macaques: gene content, transcripts, and pseudogenes. J Immunol 172:6152-6157
14. de Groot N, Doxiadis GG, de Vos-Rouweler AJ, de Groot NG, Verschoor EJ, Bontrop RE (2008a) Comparative genetics of a highly divergent DRB microsatellite in different macaque species. Immunogenetics 60:737-748
15. 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 USA 99:11748-11753
16. 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 (2008b) Pinpointing a selective sweep to the chimpanzee MHC class I region by comparative genomics. Mol Ecol 17:2074-2088
17. de Groot NG, Heijmans CM, de Groot N, Doxiadis GG, Otting N, Bontrop RE (2009) The chimpanzee Mhc-DRB region revisited: gene content, polymorphism, pseudogenes, and transcripts. Mol Immunol 47:381-389
18. Doxiadis GG, Otting N, de Groot NG, Noort R, Bontrop RE (2000) Unprecedented polymorphism of Mhc-DRB region configurations in rhesus macaques. J Immunol 164:3193-3199
19. Doxiadis GG, Otting N, de Groot NG, Bontrop RE (2001) Differential evolutionary MHC class II strategies in humans and rhesus macaques: relevance for biomedical studies. Immunol Rev 183:76-85
20. Doxiadis GG, Otting N, de Groot NG, de Groot N, Rouweler AJ, Noort R, Verschoor EJ, Bontjer I, Bontrop RE (2003) Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations. Immunogenetics 55:540-551
21. Doxiadis GG, Rouweler AJ, de Groot NG, Louwerse A, Otting N, Verschoor EJ, Bontrop RE (2006) Extensive sharing of MHC class II alleles between rhesus and cynomolgus macaques. Immunogenetics 58:259-268
22. Doxiadis GG, de Groot N, Claas FH, Doxiadis II, van Rood JJ, Bontrop RE (2007a) A highly divergent microsatellite facilitating fast and accurate DRB haplotyping in humans and rhesus macaques. Proc Natl Acad Sci USA 104:8907-8912
23. Doxiadis GG, Heijmans CM, Otting N, Bontrop RE (2007b) MIC gene polymorphism and haplotype diversity in rhesus macaques. Tissue Antigens 69:212-219
24. Doxiadis GG, de Groot N, Dauber EM, van Eede PH, Fae I, Faner R, Fischer G, Grubic Z, Lardy NM, Mayr W, Palou E, Swelsen W, Stingl K, Doxiadis II, Bontrop RE (2009a) High resolution definition of HLA-DRB haplotypes by a simplified microsatellite typing technique. Tissue Antigens 74:486-493
25. Doxiadis GG, Heijmans CM, Bonhomme M, Otting N, Crouau-Roy B, Bontrop RE (2009b) Compound evolutionary history of the rhesus macaque MHC class I B region revealed by microsatellite analysis and localization of retroviral sequences. PLoS One 4:e4287
26. 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 63:73-83
27. Doxiadis GG, de Vos-Rouweler AJ, de Groot N, Otting N, Bontrop RE (2012) DR haplotype diversity of the cynomolgus macaque as defined by its transcriptome. Immunogenetics 64:31-37
28. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564-567
29. Ferguson B et al (2007) Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). BMC Genomics 8:43
30. Gaudieri S, Leelayuwat C, Townend DC, Kulski JK, Dawkins RL (1997) Genomic characterization of the region between HLA-B and TNF: implications for the evolution of multicopy gene families. J Mol Evol 44(Suppl 1):S147-S154
31. Greene JM et al (2011) Differential MHC class I expression in distinct leukocyte subsets. BMC Immunol 12:39
32. Guo SW, Thompson EA (1992) A Monte Carlo method for combined segregation and linkage analysis. Am J Hum Genet 51:1111-1126
33. Hernandez RD, Hubisz MJ, Wheeler DA, Smith DG, Ferguson B, Rogers J, Nazareth L, Indap A, Bourquin T, McPherson J, Muzny D, Gibbs R, Nielsen R, Bustamante CD (2007) Demographic histories and patterns of linkage disequilibrium in Chinese and Indian rhesus macaques. Science 316:240-243
34. 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 60:37-46
35. Khazand M, Peiberg C, Nagy M, Sauermann U (1999) Mhc-DQ-DRB haplotype analysis in the rhesus macaque: evidence for a number of different haplotypes displaying a low allelic polymorphism. Tissue Antigens 54:615-624
36. Kita YF, Hosomichi K, Kohara S, Itoh Y, Ogasawara K, Tsuchiya H, Torii R, Inoko H, Blancher A, Kulski JK, Shiina T (2009) MHC class I A loci polymorphism and diversity in three Southeast Asian populations of cynomolgus macaque. Immunogenetics 61:635-648
37. Kulski JK, Gaudieri S, Martin A, Dawkins RL (1999) Coevolution of PERB11 (MIC) and HLA class I genes with HERV-16 and retroelements by extended genomic duplication. J Mol Evol 49:84-97
38. 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 21:2079-2091
39. Li A, Wang X, Liu Y, Zhao Y, Liu B, Sui L, Zeng L, Sun Z (2012) Preliminary observations of MHC class I A region polymorphism in three populations of Chinese-origin rhesus macaques. Immunogenetics 64:887-894
40. Liu Y, Li A, Wang X, Sui L, Li M, Zhao Y, Liu B, Zeng L, Sun Z (2012) Mamu-B genes and their allelic repertoires in different populations of Chinese-origin rhesus macaques. Immunogenetics
41. Ma X, Tang LH, Qu LB, Ma J, Chen L (2009) Identification of 17 novel major histocompatibility complex-A alleles in a population of Chinese-origin rhesus macaques. Tissue Antigens 73:184-187
42. Martin M, Mann D, Carrington M (1995a) Corrigendum: recombination rates across the HLA complex: use of microsatellites as a rapid screen for recombinant chromosomes. Hum Mol Genet 4:423-428, (1995). Hum Mol Genet4: 2423
43. Martin M, Mann D, Carrington M (1995b) Recombination rates across the HLA complex: use of microsatellites as a rapid screen for recombinant chromosomes. Hum Mol Genet 4:423-428
44. Mee ET, Badhan A, Karl JA, Wiseman RW, Cutler K, Knapp LA, Almond N, O'Connor DH, Rose NJ (2009) MHC haplotype frequencies in a UK breeding colony of Mauritian cynomolgus macaques mirror those found in a distinct population from the same geographic origin. J Med Primatol 38:1-14
45. 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 62:601-611
46. Otting N, Doxiadis GG, Versluis L, de Groot NG, Anholts J, Verduin W, Rozemuller E, Claas F, Tilanus MG, Bontrop RE (1998) Characterization and distribution of Mhc-DPB1 alleles in chimpanzee and rhesus macaque populations. Hum Immunol 59:656-664
47. Otting N, de Groot NG, Noort MC, Doxiadis GG, Bontrop RE (2000) Allelic diversity of Mhc-DRB alleles in rhesus macaques. Tissue Antigens 56:58-68
48. Otting N, de Groot NG, Doxiadis GG, Bontrop RE (2002) Extensive Mhc-DQB variation in humans and non-human primate species. Immunogenetics 54:230-239
49. Otting N, Heijmans CM, Noort RC, de Groot NG, Doxiadis GG, van Rood JJ, Watkins DI, Bontrop RE (2005) Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci USA 102:1626-1631
50. Otting N, de Vos-Rouweler AJ, Heijmans CM, de Groot NG, Doxiadis GG, Bontrop RE (2007) MHC class I A region diversity and polymorphism in macaque species. Immunogenetics 59:367-375
51. Otting N, Heijmans CM, van der Wiel M, de Groot NG, Doxiadis GG, Bontrop RE (2008) A snapshot o the Mamu-B genes and their allelic repertoire in rhesus macaques of Chinese origin. Immunogenetics 60:507-514
52. Otting N, de Groot N, de Vos-Rouweler AJ, Louwerse A, Doxiadis GG, Bontrop RE (2012) Multilocus definition of MHC haplotypes in pedigreed cynomolgus macaques (Macaca fascicularis). Immunogenetics 64:755-765
53. 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 60:339-351
54. Penedo MC, Bontrop RE, Heijmans CM, Otting N, Noort R, Rouweler AJ, de Groot N, de Groot NG, Ward T, Doxiadis GG (2005) Microsatellite typing of the rhesus macaque MHC region. Immunogenetics 57:198-209
55. Roger JH, van Vreeswijk W, Dorf ME, Balner H (1976) The major histocompatibility complex of rhesus monkeys. VI. Serology and genetics of Ia-like antigens. Tissue Antigens 8:67-86
56. Saito Y, Naruse TK, Akari H, Matano T, Kimura A (2012) Diversity of MHC class I haplotypes in cynomolgus macaques. Immunogenetics 64:131-141
57. Sanchez-Mazas A, Djoulah S, Busson M, Monnier L, de Gouville I, Poirier JC, Dehay C, Charron D, Excoffier L, Schneider S, Langaney A, Dausset J, Hors J (2000) A linkage disequilibrium map of the MHC region based on the analysis of 14 loci haplotypes in 50 French families. Eur J Hum Genet 8:33-41
58. Sauermann U, Siddiqui R, Suh YS, Platzer M, Leuchte N, Meyer H, Matz-Rensing K, Stoiber H, Nurnberg P, Hunsmann G, Stahl-Hennig C, Krawczak M (2008) Mhc class I haplotypes associated with survival time in simian immunodeficiency virus (SIV)-infected rhesus macaques. Genes Immun 9:69-80
59. Shiina T, Ota M, Shimizu S, Katsuyama Y, Hashimoto N, Takasu M, Anzai T, Kulski JK, Kikkawa E, Naruse T, Kimura N, Yanagiya K, Watanabe A, Hosomichi K, Kohara S, Iwamoto C, Umehara Y, Meyer A, Wanner V, Sano K et al (2006) Rapid evolution of major histocompatibility complex class I genes in primates generates new disease alleles in humans via hitchhiking diversity. Genetics 173:1555-1570
60. Slierendregt BL, Otting N, van Besouw N, Jonker M, Bontrop RE (1994) Expansion and contraction of rhesus macaque DRB regions by duplication and deletion. J Immunol 152:2298-2307
61. Slierendregt BL et al (1995) Identification of an Mhc-DPB1 allele involved in susceptibility to experimental autoimmune encephalomyelitis in rhesus macaques. Int Immunol 7:1671-1679
62. Smith DG, McDonough J (2005) Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta). Am J Primatol 65:1-25
63. 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 57:189-197
64. van Es AA, Balner H (1978) RhLA complex of rhesus monkeys. X. Implications of the association between D and Ia1 locus antigens. Tissue Antigens 12:279-296
65. Wiseman RW, Wojcechowskyj JA, Greene JM, Blasky AJ, Gopon T, Soma T, Friedrich TC, O'Connor SL, O'Connor DH (2007) Simian immunodeficiency virus SIVmac239 infection of major histocompatibility complex-identical cynomolgus macaques from Mauritius. J Virol 81:349-361
66. 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 15:1322-1326