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Rapid Evolution of Major Histocompatibility Complex Class I Genes in Primates Generates New Disease Alleles in Humans via Hitchhiking Diversity

Identifieur interne : 009816 ( Main/Exploration ); précédent : 009815; suivant : 009817

Rapid Evolution of Major Histocompatibility Complex Class I Genes in Primates Generates New Disease Alleles in Humans via Hitchhiking Diversity

Auteurs : Takashi Shiina [Japon] ; Masao Ota [Japon] ; Sayoko Shimizu [Japon] ; Yoshihiko Katsuyama [Japon] ; Nami Hashimoto [Japon] ; Miwa Takasu [Japon] ; Tatsuya Anzai [Japon] ; Jerzy K. Kulski [Japon, Australie] ; Eri Kikkawa [Japon] ; Taeko Naruse [Japon] ; Natsuki Kimura [Japon] ; Kazuyo Yanagiya [Japon] ; Atsushi Watanabe [Japon] ; Kazuyoshi Hosomichi [Japon] ; Sakae Kohara [Japon] ; Chie Iwamoto [Japon] ; Yumi Umehara [Japon] ; Alice Meyer [France] ; Valérie Wanner [France] ; Kazumi Sano [Japon, France] ; Cécile Macquin [France] ; Kazuho Ikeo [Japon] ; Katsushi Tokunaga [Japon] ; Takashi Gojobori [Japon] ; Hidetoshi Inoko [Japon] ; Seiamak Bahram [France]

Source :

RBID : PMC:1526686

Abstract

A plausible explanation for many MHC-linked diseases is lacking. Sequencing of the MHC class I region (coding units or full contigs) in several human and nonhuman primate haplotypes allowed an analysis of single nucleotide variations (SNV) across this entire segment. This diversity was not evenly distributed. It was rather concentrated within two gene-rich clusters. These were each centered, but importantly not limited to, the antigen-presenting HLA-A and HLA-B/-C loci. Rapid evolution of MHC-I alleles, as evidenced by an unusually high number of haplotype-specific (hs) and hypervariable (hv) (which could not be traced to a single species or haplotype) SNVs within the classical MHC-I, seems to have not only hitchhiked alleles within nearby genes, but also hitchhiked deleterious mutations in these same unrelated loci. The overrepresentation of a fraction of these hvSNV (hv1SNV) along with hsSNV, as compared to those that appear to have been maintained throughout primate evolution (trans-species diversity; tsSNV; included within hv2SNV) tends to establish that the majority of the MHC polymorphism is de novo (species specific). This is most likely reminiscent of the fact that these hsSNV and hv1SNV have been selected in adaptation to the constantly evolving microbial antigenic repertoire.


Url:
DOI: 10.1534/genetics.106.057034
PubMed: 16702430
PubMed Central: 1526686


Affiliations:


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Le document en format XML

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<title xml:lang="en" level="a" type="main">Rapid Evolution of Major Histocompatibility Complex Class I Genes in Primates Generates New Disease Alleles in Humans via Hitchhiking Diversity</title>
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<name sortKey="Shiina, Takashi" sort="Shiina, Takashi" uniqKey="Shiina T" first="Takashi" last="Shiina">Takashi Shiina</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
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</affiliation>
</author>
<author>
<name sortKey="Ota, Masao" sort="Ota, Masao" uniqKey="Ota M" first="Masao" last="Ota">Masao Ota</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Legal Medicine, Shinshu University School of Medicine, Matsumoto, Nagano 390-8621, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Department of Legal Medicine, Shinshu University School of Medicine, Matsumoto, Nagano 390-8621</wicri:regionArea>
<wicri:noRegion>Nagano 390-8621</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Shimizu, Sayoko" sort="Shimizu, Sayoko" uniqKey="Shimizu S" first="Sayoko" last="Shimizu">Sayoko Shimizu</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
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<author>
<name sortKey="Katsuyama, Yoshihiko" sort="Katsuyama, Yoshihiko" uniqKey="Katsuyama Y" first="Yoshihiko" last="Katsuyama">Yoshihiko Katsuyama</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Pharmacy, Shinshu University Hospital, Matsumoto, Nagano 390-8621, Japan,</nlm:aff>
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<wicri:regionArea>Department of Pharmacy, Shinshu University Hospital, Matsumoto, Nagano 390-8621</wicri:regionArea>
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</affiliation>
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<name sortKey="Hashimoto, Nami" sort="Hashimoto, Nami" uniqKey="Hashimoto N" first="Nami" last="Hashimoto">Nami Hashimoto</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
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</author>
<author>
<name sortKey="Takasu, Miwa" sort="Takasu, Miwa" uniqKey="Takasu M" first="Miwa" last="Takasu">Miwa Takasu</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Human Genetics, Graduate School of Medicine, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan,</nlm:aff>
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<author>
<name sortKey="Anzai, Tatsuya" sort="Anzai, Tatsuya" uniqKey="Anzai T" first="Tatsuya" last="Anzai">Tatsuya Anzai</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
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<author>
<name sortKey="Kulski, Jerzy K" sort="Kulski, Jerzy K" uniqKey="Kulski J" first="Jerzy K." last="Kulski">Jerzy K. Kulski</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
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<affiliation wicri:level="1">
<nlm:aff id="N0x9acfad0N0x9f1b1ec">Centre for Bioinformatics and Biological Computing, Murdoch University, Murdoch, Western Australia 6150, Australia,</nlm:aff>
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<name sortKey="Kikkawa, Eri" sort="Kikkawa, Eri" uniqKey="Kikkawa E" first="Eri" last="Kikkawa">Eri Kikkawa</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
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<name sortKey="Naruse, Taeko" sort="Naruse, Taeko" uniqKey="Naruse T" first="Taeko" last="Naruse">Taeko Naruse</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
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<name sortKey="Kimura, Natsuki" sort="Kimura, Natsuki" uniqKey="Kimura N" first="Natsuki" last="Kimura">Natsuki Kimura</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143</wicri:regionArea>
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<author>
<name sortKey="Yanagiya, Kazuyo" sort="Yanagiya, Kazuyo" uniqKey="Yanagiya K" first="Kazuyo" last="Yanagiya">Kazuyo Yanagiya</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143</wicri:regionArea>
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</affiliation>
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<author>
<name sortKey="Watanabe, Atsushi" sort="Watanabe, Atsushi" uniqKey="Watanabe A" first="Atsushi" last="Watanabe">Atsushi Watanabe</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
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<author>
<name sortKey="Hosomichi, Kazuyoshi" sort="Hosomichi, Kazuyoshi" uniqKey="Hosomichi K" first="Kazuyoshi" last="Hosomichi">Kazuyoshi Hosomichi</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
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<name sortKey="Kohara, Sakae" sort="Kohara, Sakae" uniqKey="Kohara S" first="Sakae" last="Kohara">Sakae Kohara</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Pharmacokinetics and Bioanalysis Center, Shin Nippon Biomedical Laboratories, Kainan, Wakayama 642-0017, Japan,</nlm:aff>
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<wicri:noRegion>Wakayama 642-0017</wicri:noRegion>
</affiliation>
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<author>
<name sortKey="Iwamoto, Chie" sort="Iwamoto, Chie" uniqKey="Iwamoto C" first="Chie" last="Iwamoto">Chie Iwamoto</name>
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<nlm:aff wicri:cut=" and" id="N0x9acfad0N0x9f1b1ec">Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540, Japan</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540</wicri:regionArea>
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</affiliation>
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<author>
<name sortKey="Umehara, Yumi" sort="Umehara, Yumi" uniqKey="Umehara Y" first="Yumi" last="Umehara">Yumi Umehara</name>
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<nlm:aff wicri:cut=" and" id="N0x9acfad0N0x9f1b1ec">Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540, Japan</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540</wicri:regionArea>
<wicri:noRegion>Shizuoka 411-8540</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Meyer, Alice" sort="Meyer, Alice" uniqKey="Meyer A" first="Alice" last="Meyer">Alice Meyer</name>
<affiliation wicri:level="1">
<nlm:aff id="N0x9acfad0N0x9f1b1ec">Human Molecular Immunogenetics, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, 67085 Strasbourg, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Human Molecular Immunogenetics, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, 67085 Strasbourg</wicri:regionArea>
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<name sortKey="Wanner, Valerie" sort="Wanner, Valerie" uniqKey="Wanner V" first="Valérie" last="Wanner">Valérie Wanner</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Human Molecular Immunogenetics, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, 67085 Strasbourg, France</nlm:aff>
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<name sortKey="Sano, Kazumi" sort="Sano, Kazumi" uniqKey="Sano K" first="Kazumi" last="Sano">Kazumi Sano</name>
<affiliation wicri:level="1">
<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143</wicri:regionArea>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Human Molecular Immunogenetics, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, 67085 Strasbourg, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Human Molecular Immunogenetics, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, 67085 Strasbourg</wicri:regionArea>
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<name sortKey="Macquin, Cecile" sort="Macquin, Cecile" uniqKey="Macquin C" first="Cécile" last="Macquin">Cécile Macquin</name>
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<nlm:aff id="N0x9acfad0N0x9f1b1ec">Human Molecular Immunogenetics, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, 67085 Strasbourg, France</nlm:aff>
<country xml:lang="fr">France</country>
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<settlement type="city">Strasbourg</settlement>
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<author>
<name sortKey="Ikeo, Kazuho" sort="Ikeo, Kazuho" uniqKey="Ikeo K" first="Kazuho" last="Ikeo">Kazuho Ikeo</name>
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<nlm:aff wicri:cut=" and" id="N0x9acfad0N0x9f1b1ec">Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540, Japan</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540</wicri:regionArea>
<wicri:noRegion>Shizuoka 411-8540</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Tokunaga, Katsushi" sort="Tokunaga, Katsushi" uniqKey="Tokunaga K" first="Katsushi" last="Tokunaga">Katsushi Tokunaga</name>
<affiliation wicri:level="4">
<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Human Genetics, Graduate School of Medicine, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Department of Human Genetics, Graduate School of Medicine, University of Tokyo, Bunkyo-ku, Tokyo 113-0033</wicri:regionArea>
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<settlement type="city">Tokyo</settlement>
<region type="région">Région de Kantō</region>
<settlement type="city">Tokyo</settlement>
</placeName>
<orgName type="university">Université de Tokyo</orgName>
</affiliation>
</author>
<author>
<name sortKey="Gojobori, Takashi" sort="Gojobori, Takashi" uniqKey="Gojobori T" first="Takashi" last="Gojobori">Takashi Gojobori</name>
<affiliation wicri:level="1">
<nlm:aff wicri:cut=" and" id="N0x9acfad0N0x9f1b1ec">Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540, Japan</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Research Organization of Information and Systems, Mishima, Shizuoka 411-8540</wicri:regionArea>
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</affiliation>
</author>
<author>
<name sortKey="Inoko, Hidetoshi" sort="Inoko, Hidetoshi" uniqKey="Inoko H" first="Hidetoshi" last="Inoko">Hidetoshi Inoko</name>
<affiliation wicri:level="1">
<nlm:aff id="N0x9acfad0N0x9f1b1ec">Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143, Japan,</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Department of Basic Medical Science and Molecular Medicine, Tokai University School of Medicine, Isehara, Kanagawa 259-1143</wicri:regionArea>
<wicri:noRegion>Kanagawa 259-1143</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Bahram, Seiamak" sort="Bahram, Seiamak" uniqKey="Bahram S" first="Seiamak" last="Bahram">Seiamak Bahram</name>
<affiliation wicri:level="1">
<nlm:aff id="N0x9acfad0N0x9f1b1ec">Human Molecular Immunogenetics, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, 67085 Strasbourg, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Human Molecular Immunogenetics, Centre de Recherche d'Immunologie et d'Hématologie, Faculté de Médecine, 67085 Strasbourg</wicri:regionArea>
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<settlement type="city">Strasbourg</settlement>
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<series>
<title level="j">Genetics</title>
<idno type="ISSN">0016-6731</idno>
<imprint>
<date when="2006">2006</date>
</imprint>
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<front>
<div type="abstract" xml:lang="en">
<p>A plausible explanation for many MHC-linked diseases is lacking. Sequencing of the MHC class I region (coding units or full contigs) in several human and nonhuman primate haplotypes allowed an analysis of single nucleotide variations (SNV) across this entire segment. This diversity was not evenly distributed. It was rather concentrated within two gene-rich clusters. These were each centered, but importantly not limited to, the antigen-presenting
<italic>HLA-A</italic>
and
<italic>HLA-B/-C</italic>
loci. Rapid evolution of MHC-I alleles, as evidenced by an unusually high number of haplotype-specific (hs) and hypervariable (hv) (which could not be traced to a single species or haplotype) SNVs within the classical MHC-I, seems to have not only hitchhiked alleles within nearby genes, but also hitchhiked deleterious mutations in these same unrelated loci. The overrepresentation of a fraction of these hvSNV (hv1SNV) along with hsSNV, as compared to those that appear to have been maintained throughout primate evolution (trans-species diversity; tsSNV; included within hv2SNV) tends to establish that the majority of the MHC polymorphism is
<italic>de novo</italic>
(species specific). This is most likely reminiscent of the fact that these hsSNV and hv1SNV have been selected in adaptation to the constantly evolving microbial antigenic repertoire.</p>
</div>
</front>
</TEI>
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<li>Région de Kantō</li>
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<name sortKey="Kohara, Sakae" sort="Kohara, Sakae" uniqKey="Kohara S" first="Sakae" last="Kohara">Sakae Kohara</name>
<name sortKey="Kulski, Jerzy K" sort="Kulski, Jerzy K" uniqKey="Kulski J" first="Jerzy K." last="Kulski">Jerzy K. Kulski</name>
<name sortKey="Naruse, Taeko" sort="Naruse, Taeko" uniqKey="Naruse T" first="Taeko" last="Naruse">Taeko Naruse</name>
<name sortKey="Ota, Masao" sort="Ota, Masao" uniqKey="Ota M" first="Masao" last="Ota">Masao Ota</name>
<name sortKey="Sano, Kazumi" sort="Sano, Kazumi" uniqKey="Sano K" first="Kazumi" last="Sano">Kazumi Sano</name>
<name sortKey="Shimizu, Sayoko" sort="Shimizu, Sayoko" uniqKey="Shimizu S" first="Sayoko" last="Shimizu">Sayoko Shimizu</name>
<name sortKey="Takasu, Miwa" sort="Takasu, Miwa" uniqKey="Takasu M" first="Miwa" last="Takasu">Miwa Takasu</name>
<name sortKey="Tokunaga, Katsushi" sort="Tokunaga, Katsushi" uniqKey="Tokunaga K" first="Katsushi" last="Tokunaga">Katsushi Tokunaga</name>
<name sortKey="Umehara, Yumi" sort="Umehara, Yumi" uniqKey="Umehara Y" first="Yumi" last="Umehara">Yumi Umehara</name>
<name sortKey="Watanabe, Atsushi" sort="Watanabe, Atsushi" uniqKey="Watanabe A" first="Atsushi" last="Watanabe">Atsushi Watanabe</name>
<name sortKey="Yanagiya, Kazuyo" sort="Yanagiya, Kazuyo" uniqKey="Yanagiya K" first="Kazuyo" last="Yanagiya">Kazuyo Yanagiya</name>
</country>
<country name="Australie">
<noRegion>
<name sortKey="Kulski, Jerzy K" sort="Kulski, Jerzy K" uniqKey="Kulski J" first="Jerzy K." last="Kulski">Jerzy K. Kulski</name>
</noRegion>
</country>
<country name="France">
<region name="Grand Est">
<name sortKey="Meyer, Alice" sort="Meyer, Alice" uniqKey="Meyer A" first="Alice" last="Meyer">Alice Meyer</name>
</region>
<name sortKey="Bahram, Seiamak" sort="Bahram, Seiamak" uniqKey="Bahram S" first="Seiamak" last="Bahram">Seiamak Bahram</name>
<name sortKey="Macquin, Cecile" sort="Macquin, Cecile" uniqKey="Macquin C" first="Cécile" last="Macquin">Cécile Macquin</name>
<name sortKey="Sano, Kazumi" sort="Sano, Kazumi" uniqKey="Sano K" first="Kazumi" last="Sano">Kazumi Sano</name>
<name sortKey="Wanner, Valerie" sort="Wanner, Valerie" uniqKey="Wanner V" first="Valérie" last="Wanner">Valérie Wanner</name>
</country>
</tree>
</affiliations>
</record>

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