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Discovery of novel MHC-class I alleles and haplotypes in Filipino cynomolgus macaques (Macaca fascicularis) by pyrosequencing and Sanger sequencing

Mafa-class I polymorphism

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Abstract

Although the low polymorphism of the major histocompatibility complex (MHC) transplantation genes in the Filipino cynomolgus macaque (Macaca fascicularis) is expected to have important implications in the selection and breeding of animals for medical research, detailed polymorphism information is still lacking for many of the duplicated class I genes. To better elucidate the degree and types of MHC polymorphisms and haplotypes in the Filipino macaque population, we genotyped 127 unrelated animals by the Sanger sequencing method and high-resolution pyrosequencing and identified 112 different alleles, 28 at cynomolgus macaque MHC (Mafa)-A, 54 at Mafa-B, 12 at Mafa-I, 11 at Mafa-E, and seven at Mafa-F alleles, of which 56 were newly described. Of them, the newly discovered Mafa-A8*01:01 lineage allele had low nucleotide similarities (<86 %) with primate MHC class I genes, and it was also conserved in the Vietnamese and Indonesian populations. In addition, haplotype estimations revealed 17 Mafa-A, 23 Mafa-B, and 12 Mafa-E haplotypes integrated with 84 Mafa-class I haplotypes and Mafa-F alleles. Of these, the two Mafa-class I haplotypes, F/A/E/B-Hp1 and F/A/E/B-Hp2, had the highest haplotype frequencies at 10.6 and 10.2 %, respectively. This suggests that large scale genetic screening of the Filipino macaque population would identify these and other high-frequency Mafa-class I haplotypes that could be used as MHC control animals for the benefit of biomedical research.

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References

  • Aarnink A, Apoil PA, Takahashi I, Osada N, Blancher A (2011) Characterization of MHC class I transcripts of a Malaysian cynomolgus macaque by high-throughput pyrosequencing and EST libraries. Immunogenetics 63:703–13

    Article  CAS  PubMed  Google Scholar 

  • 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 100:7708–13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arikata M, Itoh Y, Okamatsu M, Maeda T, Shiina T, Tanaka K, Suzuki S, Nakayama M, Sakoda Y, Ishigaki H, Takada A, Ishida H, Soda K, Pham VL, Tsuchiya H, Nakamura S, Torii R, Shimizu T, Inoko H, Ohkubo I, Kida H, Ogasawara K (2012) Memory immune responses against pandemic (H1N1) 2009 influenza virus induced by a whole particle vaccine in cynomolgus monkeys carrying Mafa-A1*052:02. PLoS One 7:e37220

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Babik W, Taberlet P, Ejsmond MJ, Radwan J (2009) New generation sequencers as a tool for genotyping of highly polymorphic multilocus MHC system. Mol Ecol Resour 9:713–9

    Article  CAS  PubMed  Google Scholar 

  • 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 58:269–82

    Article  CAS  PubMed  Google Scholar 

  • Blancher A, Bonhomme M, Crouau-Roy B, Terao K, Kitano T, Saitou N (2008) Mitochondrial DNA sequence phylogeny of 4 populations of the widely distributed cynomolgus macaque (Macaca fascicularis fascicularis). J Hered 99:254–64

    Article  CAS  PubMed  Google Scholar 

  • 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 64:605–14

    Article  PubMed  Google Scholar 

  • Blancher A, Aarnink A, Yamada Y, Tanaka K, Yamanaka H, Shiina T (2014) Study of MHC class II region polymorphism in the Filipino cynomolgus macaque population. Immunogenetics 66:219–30

    Article  CAS  PubMed  Google Scholar 

  • Boyson JE, McAdam SN, Gallimore A, Golos TG, Liu X, Gotch FM, Hughes AL, Watkins DI (1995) The MHC E locus in macaques is polymorphic and is conserved between macaques and humans. Immunogenetics 41:59–68

    Article  CAS  PubMed  Google Scholar 

  • 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 156:4656–65

    CAS  PubMed  Google Scholar 

  • 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 62:773–80

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 61:177–87

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE (2004) Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res 14:1501–15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 64:615–31

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ericsen AJ, Starrett GJ, Greene JM, Lauck M, Raveendran M, Deiros DR, Mohns MS, Vince N, Cain BT, Pham NH, Weinfurter JT, Bailey AL, Budde ML, Wiseman RW, Gibbs R, Muzny D, Friedrich TC, Rogers J, O'Connor DH (2014) Whole genome sequencing of SIV-infected macaques identifies candidate loci that may contribute to host control of virus replication. Genome Biol 15:478

    Article  PubMed Central  PubMed  Google Scholar 

  • Fuentes A, Gumert MD, Jones-Engel L (2011) Monkeys on the edge : ecology and management of long-tailed macaques and their interface with humans. Cambridge University Press, Cambridge, UK ; New York

  • Gardner MB, Luciw PA (2008) Macaque models of human infectious disease. ILAR J 49:220–55

    Article  CAS  PubMed  Google Scholar 

  • Goodridge JP, Burian A, Lee N, Geraghty DE (2013) HLA-F and MHC class I open conformers are ligands for NK cell Ig-like receptors. J Immunol 191:3553–62

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hedges SB, Dudley J, Kumar S (2006) TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971–2

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karl JA, Wiseman RW, O'Connor DH (2009) Cost-effective sequence-based nonhuman primate MHC class I genotyping from RNA. Methods 49:11–7

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kawamoto Y, Kawamoto S, Matsubayashi K, Nozawa K, Watanabe T, Stanley MA, Perwitasari-Farajallah D (2008) Genetic diversity of longtail macaques (Macaca fascicularis) on the island of Mauritius: an assessment of nuclear and mitochondrial DNA polymorphisms. J Med Primatol 37:45–54

    CAS  PubMed  Google Scholar 

  • 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 61:635–48

    Article  CAS  PubMed  Google Scholar 

  • Kita YF, Ando A, Tanaka K, Suzuki S, Ozaki Y, Uenishi H, Inoko H, Kulski JK, Shiina T (2012) Application of high-resolution, massively parallel pyrosequencing for estimation of haplotypes and gene expression levels of swine leukocyte antigen (SLA) class I genes. Immunogenetics 64:187–99

    Article  CAS  PubMed  Google Scholar 

  • Klimanskaya I, Chung Y, Becker S, Lu SJ, Lanza R (2006) Human embryonic stem cell lines derived from single blastomeres. Nature 444:481–5

    Article  CAS  PubMed  Google Scholar 

  • Kono A, Brameier M, Roos C, Suzuki S, Shigenari A, Kametani Y, Kitaura K, Matsutani T, Suzuki R, Inoko H, Walter L, Shiina T (2014) Genomic sequence analysis of the MHC class I G/F segment in common marmoset (Callithrix jacchus). J Immunol 192:3239–46

    Article  CAS  PubMed  Google Scholar 

  • 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 175:5230–9

    Article  CAS  PubMed  Google Scholar 

  • Kulski JK, Shiina T, Anzai T, Kohara S, Inoko H (2002) Comparative genomic analysis of the MHC: the evolution of class I duplication blocks, diversity and complexity from shark to man. Immunol Rev 190:95–122

    Article  CAS  PubMed  Google Scholar 

  • 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 21:2079–91

    Article  CAS  PubMed  Google Scholar 

  • Lafont BA, Buckler-White A, Plishka R, Buckler C, Martin MA (2003) Characterization of pig-tailed macaque classical MHC class I genes: implications for MHC evolution and antigen presentation in macaques. J Immunol 171:875–85

    Article  CAS  PubMed  Google Scholar 

  • Lafont BA, Buckler-White A, Plishka R, Buckler C, Martin MA (2004) Pig-tailed macaques (Macaca nemestrina) possess six MHC-E families that are conserved among macaque species: implication for their binding to natural killer receptor variants. Immunogenetics 56:142–54

    Article  CAS  PubMed  Google Scholar 

  • Lawrence J, Orysiuk D, Prashar T, Pilon R, Fournier J, Rud E, Sandstrom P, Plummer FA, Luo M (2012) Identification of 23 novel MHC class I alleles in cynomolgus macaques of Philippine and Philippine/Mauritius origins. Tissue Antigens 79:306–7

    Article  CAS  PubMed  Google Scholar 

  • Lee N, Llano M, Carretero M, Ishitani A, Navarro F, Lopez-Botet M, Geraghty DE (1998) HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci U S A 95:5199–204

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leuchte N, Berry N, Kohler B, Almond N, LeGrand R, Thorstensson R, Titti F, Sauermann U (2004) MhcDRB-sequences from cynomolgus macaques (Macaca fascicularis) of different origin. Tissue Antigens 63:529–37

    Article  CAS  PubMed  Google Scholar 

  • Muhl T, Krawczak M, Ten Haaft P, Hunsmann G, Sauermann U (2002) MHC class I alleles influence set-point viral load and survival time in simian immunodeficiency virus-infected rhesus monkeys. J Immunol 169:3438–46

    Article  CAS  PubMed  Google Scholar 

  • O'Leary CE, Wiseman RW, Karl JA, Bimber BN, Lank SM, Tuscher JJ, O'Connor DH (2009) Identification of novel MHC class I sequences in pig-tailed macaques by amplicon pyrosequencing and full-length cDNA cloning and sequencing. Immunogenetics 61:689–701

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 U S A 102:1626–31

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 59:367–75

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 60:339–51

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Piontkivska H, Nei M (2003) Birth-and-death evolution in primate MHC class I genes: divergence time estimates. Mol Biol Evol 20:601–9

    Article  CAS  PubMed  Google Scholar 

  • Robinson J, Mistry K, McWilliam H, Lopez R, Parham P, Marsh SG (2011) The IMGT/HLA database. Nucleic Acids Res 39:D1171–6

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Robinson J, Halliwell JA, McWilliam H, Lopez R, Marsh SG (2013) IPD—the Immuno Polymorphism Database. Nucleic Acids Res 41:D1234–40

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–25

    CAS  PubMed  Google Scholar 

  • Sano K, Shiina T, Kohara S, Yanagiya K, Hosomichi K, Shimizu S, Anzai T, Watanabe A, Ogasawara K, Torii R, Kulski JK, Inoko H (2006) Novel cynomolgus macaque MHC-DPB1 polymorphisms in three South-East Asian populations. Tissue Antigens 67:297–306

    Article  CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–8

    Article  CAS  PubMed  Google Scholar 

  • Shiina T, Tamiya G, Oka A, Takishima N, Inoko H (1999) Genome sequencing analysis of the 1.8 Mb entire human MHC class I region. Immunol Rev 167:193–9

    Article  CAS  PubMed  Google Scholar 

  • Shiina T, Inoko H, Kulski JK (2004) An update of the HLA genomic region, locus information and disease associations: 2004. Tissue Antigens 64:631–49

    Article  CAS  PubMed  Google Scholar 

  • 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, Macquin C, Ikeo K, Tokunaga K, Gojobori T, Inoko H, Bahram S (2006) Rapid evolution of major histocompatibility complex class I genes in primates generates new disease alleles in humans via hitchhiking diversity. Genetics 173:1555–70

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–89

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–72

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–9

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tosi AJ, Coke CS (2007) Comparative phylogenetics offer new insights into the biogeographic history of Macaca fascicularis and the origin of the Mauritian macaques. Mol Phylogenet Evol 42:498–504

    Article  CAS  PubMed  Google Scholar 

  • 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 56:155–63

    Article  CAS  PubMed  Google Scholar 

  • Urvater JA, Otting N, Loehrke JH, Rudersdorf R, Slukvin II, Piekarczyk 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 164:1386–98

    Article  CAS  PubMed  Google Scholar 

  • Vallender EJ (2014) Bringing non-human primate research into the post-genomic era: how monkeys are teaching us about elite controllers of HIV/AIDS. Genome Biol 15:507

    Article  PubMed Central  PubMed  Google Scholar 

  • Vallender EJ, Miller GM (2013) Nonhuman primate models in the genomic era: a paradigm shift. ILAR J 54:154–65

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Watanabe Y, Tokunaga K, Geraghty DE, Tadokoro K, Juji T (1997) Large-scale comparative mapping of the MHC class I region of predominant haplotypes in Japanese. Immunogenetics 46:135–41

    Article  CAS  PubMed  Google Scholar 

  • Watanabe A, Shiina T, Shimizu S, Hosomichi K, Yanagiya K, Kita YF, Kimura T, Soeda E, Torii R, Ogasawara K, Kulski JK, Inoko H (2007) A BAC-based contig map of the cynomolgus macaque (Macaca fascicularis) major histocompatibility complex genomic region. Genomics 89:402–12

    Article  CAS  PubMed  Google Scholar 

  • Wegner KM (2009) Massive parallel MHC genotyping: titanium that shines. Mol Ecol 18:1818–20

    Article  PubMed  Google Scholar 

  • 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 81:349–61

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 15:1322–6

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 72:29–38

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. Atsushi Toyoda at Center for Information Biology, Comparative Genomics Laboratory, National Institute of Genetics for making sequence data and Mr. Masayuki Tanaka, Mr. Hideki Hayashi, and Mr. Tadayuki Sato at the Education and Research Support Center, Research and Development Division, Tokai University for their technical support. This work was supported by MEXT KAKENHI (no. 221S0002), JSPS KAKENHI (no. 21300155), and was partially supported by the program “Research Center Network for Realization of Regenerative Medicine” in Japan Agency for Medical Research and Development (AMED) and from Adaptable and Seamless Technology transfer Program in AMED.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Molecular Life Science, Division of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa, 259-1143, Japan

    Takashi Shiina, Yukiho Yamada, Shingo Suzuki, Anri Masuya, Sayaka Ito & Jerzy K. Kulski

  2. Ina Research Inc., 2148-188 Nishiminowa, Ina, Nagano, 399-4501, Japan

    Yukiho Yamada, Daisuke Ido & Hisashi Yamanaka

  3. Laboratoire d’Immunogénétique moléculaire, Université Toulouse III, Faculte de Medecine Purpan, Laboratoire d’immunologie, 1 Avenue Jean Poulhes, Hôpital Rangueil, TSA50032, 31059, Toulouse, Cedex 9, France

    Alice Aarnink & Antoine Blancher

  4. Research Center for Animal Life Science, Shiga University of Medical Science, School of Medicine, Setatsukinowa, Ohtsu, Shiga, 520-2192, Japan

    Chizuru Iwatani & Hideaki Tsuchiya

  5. Department of Pathology, Shiga University of Medical Science, Setatsukinowa, Ohtsu, Shiga, 520-2192, Japan

    Hirohito Ishigaki, Yasushi Itoh & Kazumasa Ogasawara

  6. Centre for Forensic Science, The University of Western Australia, Nedlands,, WA, 6008, Australia

    Jerzy K. Kulski

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  1. Takashi Shiina
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Correspondence to Takashi Shiina.

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ESM 1

Figure 1 An example of the haplotype estimation method for the Mafa-A haplotypes. We used the same estimation process for the Mafa-B and Mafa-E haplotypes. (PPTX 89 kb)

ESM 2

Table 1 Sequence read information obtained by the Roche Genome Sequencer 454 FLX system (PDF 169 kb)

ESM 3

Table 2 Nucleotide and amino acid similarities among the Mafa-E and among the Mafa-F alleles (PDF 64 kb)

ESM 4

Table 3 Estimation ofMafa-Fand Mafa-A, Mafa-A and Mafa-E, and Mafa-EandMafa-Bhaplotype information obtained by the PHASE program (PDF 167 kb)

ESM 5

Table 4 Estimation of Mafa-class Ihaplotype information obtained by the PHASE program (PDF 139 kb)

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Shiina, T., Yamada, Y., Aarnink, A. et al. Discovery of novel MHC-class I alleles and haplotypes in Filipino cynomolgus macaques (Macaca fascicularis) by pyrosequencing and Sanger sequencing. Immunogenetics 67, 563–578 (2015). https://doi.org/10.1007/s00251-015-0867-9

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