Detection of Ancestry Informative HLA Alleles Confirms the Admixed Origins of Japanese Population

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Nakaoka, Hirofumi ^a   Mitsunaga, Shigeki ^b,c   Hosomichi, Kazuyoshi ^a   Shyh Yuh, Liou ^d   Sawamoto, Taiji ^e   Fujiwara, Tsutomu ^f   Tsutsui, Naohisa ^g   Suematsu, Koji ^h   Shinagawa, Akira ⁱ   Inoko, Hidetoshi ^b,c   Inoue, Ituro ^a,b  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b TOKAI UNIVERSITY   (Japan)

^c GenoDive Pharma   (Japan)

^d TAKEDA PHARMACEUTICAL COMPANY LIMITED   (Japan)

^e ASTELLAS PHARMA INC   (Japan)

^f OTSUKA PHARMACEUTICAL CO LTD   (Japan)

^g MITSUBISHI TANABE PHARMA CORPORATION   (Japan)

^h TAISHO PHARMACEUTICAL CO LTD   (Japan)

ⁱ DAIICHI SANKYO CO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN;

ARTICLE; CONTROLLED STUDY; ETHNIC GROUP; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GEOGRAPHIC ORIGIN; HAPLOTYPE; HUMAN; HUMAN CELL; JAPANESE; NORMAL HUMAN; PLESIOMORPHY; POPULATION GENETIC STRUCTURE; POPULATION MIGRATION; RACE DIFFERENCE; SOUTH KOREAN;

ALLELES; ASIAN CONTINENTAL ANCESTRY GROUP; EVOLUTION, MOLECULAR; GENETIC LOCI; HAPLOTYPES; HLA ANTIGENS; HUMANS; LINKAGE DISEQUILIBRIUM; PHYLOGENY; POLYMORPHISM, GENETIC; PRINCIPAL COMPONENT ANALYSIS;

EID: 84875924099     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060793     Document Type: Article

References (61)

1. Shiina T, Hosomichi K, Inoko H, Kulski JK, (2009) The HLA genomic loci map: Expression, interaction, diversity and disease. J Hum Genet 54: 15-39 10.1038/jhg.2008.5.
2. Robinson J, Waller MJ, Parham P, de Groot N, Bontrop R, et al. (2003) IMGT/HLA and IMGT/MHC: Sequence databases for the study of the major histocompatibility complex. Nucleic Acids Res 31: 311-314.
3. Vina MA, Hollenbach JA, Lyke KE, Sztein MB, Maiers M, et al. (2012) Tracking human migrations by the analysis of the distribution of HLA alleles, lineages and haplotypes in closed and open populations. Philos Trans R Soc Lond B Biol Sci 367: 820-829 10.1098/rstb.2011.0320.
4. Mallal S, Nolan D, Witt C, Masel G, Martin AM, et al. (2002) Association between presence of HLA-B*5701, HLA-DR7, and HLA-DQ3 and hypersensitivity to HIV-1 reverse-transcriptase inhibitor abacavir. Lancet 359: 727-732.
5. Chung WH, Hung SI, Hong HS, Hsih MS, Yang LC, et al. (2004) Medical genetics: A marker for Stevens-Johnson syndrome. Nature 428: 486 10.1038/428486a.
6. Hung SI, Chung WH, Liou LB, Chu CC, Lin M, et al. (2005) HLA-B*5801 allele as a genetic marker for severe cutaneous adverse reactions caused by allopurinol. Proc Natl Acad Sci U S A 102: 4134-4139 10.1073/pnas.0409500102.
7. Tohkin M, Kaniwa N, Saito Y, Sugiyama E, Kurose K, et al. (2011) A whole-genome association study of major determinants for allopurinol-related Stevens-Johnson syndrome and toxic epidermal necrolysis in Japanese patients. Pharmacogenomics J 10.1038/tpj.2011.41; 10.1038/tpj.2011.41.
8. Cardon LR, Bell JI, (2001) Association study designs for complex diseases. Nat Rev Genet 2: 91-99.
9. Cardon LR, Palmer LJ, (2003) Population stratification and spurious allelic association. Lancet 361: 598-604.
10. Wellcome Trust Case Control Consortium (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447: 661-678.
11. Hanihara K, (1991) Dual structure model for the population history of the Japanese. Japan Review 2: 1-33.
12. Omoto K, Saitou N, (1997) Genetic origins of the Japanese: A partial support for the dual structure hypothesis. Am J Phys Anthropol 102: 437-446 2-P.
13. Tajima A, Hayami M, Tokunaga K, Juji T, Matsuo M, et al. (2004) Genetic origins of the Ainu inferred from combined DNA analyses of maternal and paternal lineages. J Hum Genet 49: 187-193 10.1007/s10038-004-0131-x.
14. Tajima A, Pan IH, Fucharoen G, Fucharoen S, Matsuo M, et al. (2002) Three major lineages of Asian Y chromosomes: Implications for the peopling of east and southeast Asia. Hum Genet 110: 80-88 10.1007/s00439-001-0651-9.
15. Tanaka M, Cabrera VM, Gonzalez AM, Larruga JM, Takeyasu T, et al. (2004) Mitochondrial genome variation in eastern Asia and the peopling of Japan. Genome Res 14: 1832-1850 10.1101/gr.2286304.
16. Hammer MF, Karafet TM, Park H, Omoto K, Harihara S, et al. (2006) Dual origins of the Japanese: Common ground for hunter-gatherer and farmer Y chromosomes. J Hum Genet 51: 47-58 10.1007/s10038-005-0322-0.
17. Yamaguchi-Kabata Y, Nakazono K, Takahashi A, Saito S, Hosono N, et al. (2008) Japanese population structure, based on SNP genotypes from 7003 individuals compared to other ethnic groups: Effects on population-based association studies. Am J Hum Genet 83: 445-456 10.1016/j.ajhg.2008.08.019.
18. Yamaguchi-Kabata Y, Tsunoda T, Kumasaka N, Takahashi A, Hosono N, et al. (2012) Genetic differences in the two main groups of the Japanese population based on autosomal SNPs and haplotypes. J Hum Genet 57: 326-334 10.1038/jhg.2012.26; 10.1038/jhg.2012.26.
19. Hatta Y, Ohashi J, Imanishi T, Kamiyama H, Iha M, et al. (1999) HLA genes and haplotypes in Ryukyuans suggest recent gene flow to the Okinawa Islands. Hum Biol 71: 353-365.
20. Bannai M, Ohashi J, Harihara S, Takahashi Y, Juji T, et al. (2000) Analysis of HLA genes and haplotypes in Ainu (from Hokkaido, northern Japan) supports the premise that they descent from Upper Paleolithic populations of East Asia. Tissue Antigens 55: 128-139.
21. Lee KW, Oh DH, Lee C, Yang SY, (2005) Allelic and haplotypic diversity of HLA-A,-B,-C,-DRB1, and-DQB1 genes in the Korean population. Tissue Antigens 65: 437-447 10.1111/j.1399-0039.2005.00386.x.
22. Saito S, Ota S, Yamada E, Inoko H, Ota M, (2000) Allele frequencies and haplotypic associations defined by allelic DNA typing at HLA class I and class II loci in the Japanese population. Tissue Antigens 56: 522-529.
23. Tokunaga K, Ishikawa Y, Ogawa A, Wang H, Mitsunaga S, et al. (1997) Sequence-based association analysis of HLA class I and II alleles in Japanese supports conservation of common haplotypes. Immunogenetics 46: 199-205.
24. Tokunaga K, Imanishi T, Takahashi K, Juji T (1996) On the origin and dispersal of East Asian populations as viewed from HLA haplotypes. In Akazawa T, Szathmary E.J.E (Eds.), Prehistoric Mongoloid Dispersals, Oxford University Press, Oxford.
25. Tokunaga K, Ohashi J, Bannai M, Juji T, (2001) Genetic link between Asians and native Americans: Evidence from HLA genes and haplotypes. Hum Immunol 62: 1001-1008.
26. Excoffier L, Laval G, Schneider S, (2007) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47-50.
27. Novembre J, Stephens M, (2008) Interpreting principal component analyses of spatial population genetic variation. Nat Genet 40: 646-649 10.1038/ng.139.
28. Browning BL, Browning SR, (2009) A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Genet 84: 210-223.
29. Gonzalez-Galarza FF, Christmas S, Middleton D, Jones AR, (2011) Allele frequency net: A database and online repository for immune gene frequencies in worldwide populations. Nucleic Acids Res 39: D913-9 10.1093/nar/gkq1128.
30. Jeffreys AJ, Kauppi L, Neumann R, (2001) Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nat Genet 29: 217-222 10.1038/ng1001-217.
31. Miretti MM, Walsh EC, Ke X, Delgado M, Griffiths M, et al. (2005) A high-resolution linkage-disequilibrium map of the human major histocompatibility complex and first generation of tag single-nucleotide polymorphisms. Am J Hum Genet 76: 634-646 10.1086/429393.
32. Lewontin RC, (1964) The interaction of selection and linkage. I. general considerations; heterotic models. Genetics 49: 49-67.
33. Shi L, Yao YF, Shi L, Matsushita M, Yu L, et al. (2010) HLA alleles and haplotypes distribution in Dai population in Yunnan province, Southwest China. Tissue Antigens 75: 159-165 10.1111/j.1399-0039.2009.01407.x.
34. Yao Y, Shi L, Shi L, Matsushita M, Yu L, et al. (2009) Distribution of HLA-A,-B,-Cw, and-DRB1 alleles and haplotypes in an isolated Han population in Southwest China. Tissue Antigens 73: 561-568 10.1111/j.1399-0039.2009.01237.x.
35. Yang KL, Chen SP, Shyr MH, Lin PY, (2009) High-resolution human leukocyte antigen (HLA) haplotypes and linkage disequilibrium of HLA-B and-C and HLA-DRB1 and-DQB1 alleles in a Taiwanese population. Hum Immunol 70: 269-276 10.1016/j.humimm.2009.01.015.
36. Hoa BK, Hang NT, Kashiwase K, Ohashi J, Lien LT, et al. (2008) HLA-A,-B,-C,-DRB1 and-DQB1 alleles and haplotypes in the Kinh population in Vietnam. Tissue Antigens 71: 127-134 10.1111/j.1399-0039.2007.00982.x.
37. Chen S, Hu Q, Xie Y, Zhou L, Xiao C, et al. (2007) Origin of Tibeto-Burman speakers: Evidence from HLA allele distribution in Lisu and Nu inhabiting Yunnan of China. Hum Immunol 68: 550-559 10.1016/j.humimm.2007.02.006.
38. Shi L, Ogata S, Yu JK, Ohashi J, Yu L, et al. (2008) Distribution of HLA alleles and haplotypes in Jinuo and Wa populations in Southwest China. Hum Immunol 69: 58-65 10.1016/j.humimm.2007.11.007.
39. Leffell MS, Fallin MD, Erlich HA, Fernandez-Vijna M, Hildebrand WH, et al. (2002) HLA antigens, alleles and haplotypes among the Yup'ik Alaska natives: Report of the ASHI Minority Workshops, Part II. Hum Immunol 63: 614-625.
40. Moscoso J, Crawford MH, Vicario JL, Zlojutro M, Serrano-Vela JI, et al. (2008) HLA genes of Aleutian Islanders living between Alaska (USA) and Kamchatka (Russia) suggest a possible southern Siberia origin. Mol Immunol 45: 1018-1026 10.1016/j.molimm.2007.07.024.
41. Hollenbach JA, Thomson G, Cao K, Fernandez-Vina M, Erlich HA, et al. (2001) HLA diversity, differentiation, and haplotype evolution in Mesoamerican Natives. Hum Immunol 62: 378-390.
42. Garcia-Ortiz JE, Sandoval-Ramirez L, Rangel-Villalobos H, Maldonado-Torres H, Cox S, et al. (2006) High-resolution molecular characterization of the HLA class I and class II in the Tarahumara Amerindian population. Tissue Antigens 68: 135-146 10.1111/j.1399-0039.2006.00636.x.
43. Lin M, Chu CC, Lee HL, Chang SL, Ohashi J, et al. (2000) Heterogeneity of Taiwan's indigenous population: Possible relation to prehistoric Mongoloid dispersals. Tissue Antigens 55: 1-9.
44. Loo JH, Trejaut JA, Yen JC, Chen ZS, Lee CL, et al. (2011) Genetic affinities between the Yami tribe people of Orchid Island and the Philippine Islanders of the Batanes archipelago. BMC Genet 12: 21 10.1186/1471-2156-12-21.
45. Kavvoura FK, Ioannidis JP, (2008) Methods for meta-analysis in genetic association studies: A review of their potential and pitfalls. Hum Genet 123: 1-14.
46. Sagoo GS, Little J, Higgins JP, (2009) Systematic reviews of genetic association studies. Human Genome Epidemiology Network. PLoS Med 6: e28.
47. Nakaoka H, Inoue I, (2009) Meta-analysis of genetic association studies: Methodologies, between-study heterogeneity and winner's curse. J Hum Genet 54: 615-623 10.1038/jhg.2009.95.
48. Hayes BJ, Visscher PM, McPartlan HC, Goddard ME, (2003) Novel multilocus measure of linkage disequilibrium to estimate past effective population size. Genome Res 13: 635-643 10.1101/gr.387103.
49. Fry AE, Trafford CJ, Kimber MA, Chan MS, Rockett KA, et al. (2006) Haplotype homozygosity and derived alleles in the human genome. Am J Hum Genet 78: 1053-1059 10.1086/504160.
50. Nordborg M, Tavare S, (2002) Linkage disequilibrium: What history has to tell us. Trends Genet 18: 83-90.
51. HUGO Pan-Asian SNP Consortium (2009) Abdulla MA, Ahmed I, Assawamakin A, Bhak J, et al. (2009) Mapping human genetic diversity in Asia. Science 326: 1541-1545 10.1126/science.1177074.
52. Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The history and geography of human genes. Princeton University Press, Princeton.
53. Karafet T, Xu L, Du R, Wang W, Feng S, et al. (2001) Paternal population history of East Asia: Sources, patterns, and microevolutionary processes. Am J Hum Genet 69: 615-628 10.1086/323299.
54. Di D, Sanchez-Mazas A, (2011) Challenging views on the peopling history of East Asia: The story according to HLA markers. Am J Phys Anthropol 145: 81-96 10.1002/ajpa.21470; 10.1002/ajpa.21470.
55. Goebel T, Waters MR, O'Rourke DH, (2008) The late Pleistocene dispersal of modern humans in the Americas. Science 319: 1497-1502 10.1126/science.1153569.
56. Rasmussen M, Li Y, Lindgreen S, Pedersen JS, Albrechtsen A, et al. (2010) Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature 463: 757-762 10.1038/nature08835.
57. Reich D, Patterson N, Campbell D, Tandon A, Mazieres S, et al. (2012) Reconstructing Native American population history. Nature 488: 370-374 10.1038/nature11258.
58. Bortolini MC, Salzano FM, Thomas MG, Stuart S, Nasanen SP, et al. (2003) Y-chromosome evidence for differing ancient demographic histories in the Americas. Am J Hum Genet 73: 524-539 10.1086/377588.
59. Wang C, Krishnakumar S, Wilhelmy J, Babrzadeh F, Stepanyan L, et al. (2012) High-throughput, high-fidelity HLA genotyping with deep sequencing. Proc Natl Acad Sci U S A 109: 8676-8681 10.1073/pnas.1206614109.
60. Abi-Rached L, Jobin MJ, Kulkarni S, McWhinnie A, Dalva K, et al. (2011) The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334: 89-94 10.1126/science.1209202.
61. Song EY, Park MH, Kang SJ, Park HJ, Kim BC, et al. (2002) HLA class II allele and haplotype frequencies in Koreans based on 107 families. Tissue Antigens 59: 475-486.