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Comparative Genomics of the Major Histocompatibility Complex in the Family Equidae

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Comparative Genomics of the Major Histocompatibility Complex in the Family Equidae MASARYK UNIVERSITY FACULTY OF SCIENCE Comparative genomics of the major histocompatibility complex in the family Equidae Ph.D. Dissertation Marie Klumplerová Supervisor: prof. MVDr. RNDr. Petr Hořín, CSc Brno 2015 Bibliographic entry Author: Mgr. Marie Klumplerová Institute of Animal Genetics University of Veterinary and Pharmaceutical Sciences Brno Title of Dissertation: Comparative genomics of the major histocompatibility complex in the family Equidae Degree Programme: Biology Field of Study: General and Molecular Genetics Supervisor: prof. MVDr. RNDr. Petr Hořín, CSc. Academic year: 2014/2015 Number of pages: 125 Keywords: Horse; Donkey; Equidae; selection; association; genetic diversity Bibliografická identifikace Jméno a příjmení autora: Mgr. Marie Klumplerová Ústav genetiky Veterinární a farmaceutická univerzita Brno Název disertační práce: Komparativní genomika hlavního histokompatibilitního komplexu u čeledi Equidae Studijní program: Biologie Studijní obor: Obecná a molekulární genetika Školitel: prof. MVDr. RNDr. Petr Hořín, CSc. Akademický rok: 2014/2015 Počet stran: 125 Klíčová slova: Kůň; osel; koňovití; selekce; asociace; genetická diverzita Abstract Genes of the major histocompatibility complex (MHC) are crucial for the adaptive immune system of jawed vertebrates. Variation at the MHC loci affect many important biological traits, including immune recognition, susceptibility to infectious and other diseases, mating preferences, and/or maternal-fetal interaction and pregnancy outcome. MHC has become a paradigm for how pathogens are shaping the patterns of adaptive genetic variation. It is used, as one of the most preferred marker, in many different research fields ranging from human medicine, molecular evolutionary studies to conservation genetics. The family Equidae is a rapidly evolving mammalian group comprising domesticated as well as free-ranging animals occupying a wide range of habitats differing in climatic conditions and pathogen pressure. In this thesis, genetic diversity, molecular evolution and selection of MHC class II loci in equids were characterized. In addition, an extraordinary feature of the equine MHC, polymorphism of its DRA locus, was used to seek for associations with infection and allergy as well as for analyzing the diversity of a model endangered horse population. Abstrakt Geny hlavního histokompatibilitního komplexu (MHC) jsou nezbytné pro správnou funkci získané imunity u čelistnatých obratlovců. Proměnlivost v genech MHC má vliv na řadu důležitých biologických znaků, které zahrnují imunitní rozpoznání vlastního od cizího, vnímavost k infekčním a dalším typům onemocnění, výběr partnera i průběh těhotenství. MHC je považováno za typický příklad adaptivní genetické variability utvářené pod vlivem patogenů. Z těchto důvodů se stal hlavní histokompatibilitní komplex jedním z nevíce preferovaných markerů používaným pro studium genetické proměnlivosti v mnoha vědních disciplínách od humánní medicíny, přes evoluční studie až po ochranářskou genetiku. Koňovití jsou rychle se vyvíjející čeleď, do které patří domestikované i volně žijící druhy obývající různá prostředí lišící se jak klimatickými podmínkami, tak výskytem patogenů. V předkládané disertační práci jsem se zabývala genetickou diverzitou, molekulární evolucí a selekcí u jednotlivých lokusů dvou genů třídy II u koňovitých. Dále jsem se věnovala výjimečnému rysu koňského MHC, kterým je polymorfismus genu DRA, a využila jsem variability v tomto lokusu pro asociační studie s infekcí, alergickým onemocněním a k analýze genetické variability v modelové ohrožené koňské populaci. © Marie Klumplerová, Masaryk University, 2015 Contents ACKNOWLEDGMENT ...................................................................................... viii INTRODUCTION ................................................................................................... 1 The major histocompatibility complex .............................................................. 1 MHC molecules structure ................................................................................. 2 MHC polymorphism, its origins and maintenance in populations................... 3 Signatures of selection ...................................................................................... 6 Evolution of major histocompatibility complexes ............................................ 7 MHC and disease ............................................................................................... 8 The family Equidae as model for immunogenetic studies ................................ 9 The equine MHC .............................................................................................. 11 SPECIFIC OBJECTIVES OF THE DISSERTATION ...........................................14 MATERIALS AND METHODS ............................................................................ 15 Animals ............................................................................................................. 15 Methods ............................................................................................................16 RESULTS ............................................................................................................. 17 List of attached manuscripts and the contribution of the author .................... 17 Synopsis of the results obtained .......................................................................19 MS I...............................................................................................................19 MS II ............................................................................................................ 20 MS III ............................................................................................................21 MS IV ........................................................................................................... 22 MS V ............................................................................................................ 23 MS VI ........................................................................................................... 24 DISCUSSION ...................................................................................................... 25 GENERAL CONCLUSIONS ................................................................................ 29 REFERENCES .................................................................................................... 30 LIST OF ABREVIATIONS................................................................................... 39 APPENDIX .......................................................................................................... 40 MS I ................................................................................................................. 40 MS II ................................................................................................................ 80 MS III .............................................................................................................. 87 MS IV ............................................................................................................... 96 MS V .............................................................................................................. 106 MS VI .............................................................................................................. 115 ACKNOWLEDGMENT I would like to express my gratitude to my supervisor prof. Petr Hořín. Without the opportunity and trust he gave me, I would not be the person I am today. I would like to thank him for his inspiring, kind yet demanding leadership and many hours of discussions, which were usually spiced with his unique sense of humor. I am thankful to my colleagues for creating a friendly atmosphere during everyday work. Many thanks go to Zuzana Bayerová for our, not always scientific, chats and for her help with routine laboratory tasks at the end of my pregnancy. Last but not least, I wish to sincerely thank to my parents and family for their support and love. viii INTRODUCTION The major histocompatibility complex The immune system allows living organisms to discriminate between self and non-self and thus contributes to maintaining their homeostasis. By providing them with defense against pathogens, the immune system also represents a critical determinant of the mechanisms of adaptation. Pathogens are one of the major driving forces of evolution leaving signatures of selection in the host genomes. Therefore, studies of immunity-related genes (the immunogenome) are important for our understanding of immunity, susceptibility to disease, adaptation and evolution. In jawed vertebrates, two main branches of immune responses can be distinguished: the innate and adaptive immunity. Molecules of the major histocompatibility complex (MHC) play an essential role in the activation of adaptive immune responses. These cell surface molecules are trans-membrane proteins which can bind antigens of both intracellular and extracellular origin and present them to T- lymphocytes. MHC molecules are encoded in a large genetic region. In mammals, this region spans almost 4 Mb and contains about 230 translatable highly polymorphic genes. Organization of human MHC is shown in Figure 1. Genes coding for antigen presenting molecules are assembled into 2 regions, class I and class II, separated by a class III region. Class III genes are more diverse in function, not always connected to immune response. Class I MHC molecules can be
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