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Corine P. Kruiswijk Evolution of Major Histocompatibility

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Corine P. Kruiswijk Evolution of Major Histocompatibility CORINE P. KRUISWIJK EVOLUTION OF MAJOR HISTOCOMPATIBILITY GENES IN CYPRINID FISH MOLECULAR ANALYSES AND PHYLOGENIES EVOLUTION OF MAJOR HISTOCOMPATIBILITY GENES IN CYPRINID FISH MOLECULAR ANALYSES AND PHYLOGENIES Promotor: Prof. Dr Ir Huub F. J. Savelkoul Hoogleraar in de celbiologie & immunologie Co-promotor: Dr René J. M. Stet Universitair hoofddocent, leerstoelgroep celbiologie & immunologie Leden promotiecommissie: Dr Ronald E. Bontrop Biomedical Primate Research Centre, Rijswijk Prof. Dr Ir Johan L. van Leeuwen Wageningen Universiteit Prof. Dr Rolf F. Hoekstra Wageningen Universiteit Prof. Dr Brian Dixon University of Waterloo, Canada CORINE P. KRUISWIJK EVOLUTION OF MAJOR HISTOCOMPATIBILITY GENES IN CYPRINID FISH MOLECULAR ANALYSES AND PHYLOGENIES PROEFSCHRIFT TER VERKRIJGING VAN DE GRAAD VAN DOCTOR OP GEZAG VAN DE RECTOR MAGNIFICUS VAN WAGENINGEN UNIVERSITEIT, PROF. DR IR L. SPEELMAN IN HET OPENBAAR TE VERDEDIGEN OP VRIJDAG 1 NOVEMBER 2002 DES NAMIDDAGS TE VIER UUR IN DE AULA Evolution of Major Histocompatibility Genes in Cyprinid Fish Molecular Analyses and Phylogenies PhD thesis, Wageningen University with summary in Dutch isbn 90-5808-735-2 C. P. Kruiswijk, 2002 Wageningen Institute of Animal Sciences po box 338, 6700 ah Wageningen, The Netherlands VOORWOORD Het boekwerkje dat u nu vast houdt is het wetenschappelijk resultaat van vier jaar promotieonderzoek. Echter voor mij betekent het veel meer dan dat. Het waren vier lastige maar ook zeer leerzame jaren. Vanaf het prille begin van het promotieonderzoek ontbrak om verschillende redenen de motivatie. De ken- nismaking met de duistere kant van mijn geest was niet erg aangenaam. Maar zoals Albert Einstein schreef ‘In the middle of difficulty lies the oppertunity’.Zo ontstond het idee om naast het promotieonderzoek een doctoraal studie Be- drijfskunde te volgen. En Geert, waarschijnlijk was mijn interesse om je drie jaar lang te assisteren bij de workshop anders stukken minder geweest. Het wa- ren geweldig leuke weken die ik niet had willen missen! U snapt hoe blij ik ben dat het proefschift er, tegen al mijn verwachtingen in, toch is gekomen. Beste René, samen hebben we het dan toch gered en ook nog eens in vier jaar, bedankt! Ook de vele anderen, die een bijdrage hebben gele- verd aan mijn promotieonderzoek, wil ik graag bedanken. Een aantal personen wil ik met naam noemen. Beste Huub, pas in een laat stadium raakte je betrokken 5 voorwoord bij mijn promotieonderzoek. Je motiverende discussies en enthousiasme wa- ren precies het goede duwtje in de rug. Trudi, jij stond altijd weer voor mij klaar, dankjewel! Vele dna fragmenten heb je voor me gesequenced en andere experi- menten voor me uitgevoerd. Daarnaast maakte je altijd weer tijd om die clonen die ik snel nodig had nog even snel te sequencen. Beja, ook jij bedankt voor de hulp bij het sequencen, je enthousiasme en gezelligheid. Nico, bedankt voor de pc en je altijd goede stemming. Na drie jaar slechts stukjes staartvin of spierweefsel van Afrikaanse grote bar- belen te hebben gezien, mocht ik ze in hun natuurlijke omgeving gaan bekij- ken. Nand en Martin, bedankt voor de fantastische tijd in Ethiopië. Ook de mede aio’s, Ank, Heidi, Jeroen, Joop, Krys, Maaike, Marc en Patrycia, mijn studenten, Kim en Joost en alle niet bij naam genoemde cbi-ers en ezo- ers, bedankt voor de gezelligheid en prettige samenwerking. Beste paranimf Geert, dankjewel voor de vele uren peptalk, ze waren onmis- baar. Paranimf Mark, het waren mooie avonden in de kroeg, met ettelijke gla- zen bier en altijd weer een discussie over dat ‘ene onderwerp’ (daar gaan we het vanavond niet over hebben hoor...). Tenslotte familie en vrienden, door de combinatie studie en promotie bleef er vaak weinig tijd voor julie over, bedankt voor de vriendschap! Een speciaal woordje voor een aantal personen. Auryn meiden en partners, dank jullie wel voor jullie geduld, tolerantie en waardering (echter na wintersport 2002, met zo’n fantastische ontvangst, overweeg ik om gewoon altijd later te komen...). Sommige studiegenoten, jullie weten zelf wel wie ik bedoel, bedankt (zag ik daar een karper...) en een aantal huisgenoten voor de versnaperingen als ik weer eens vergat te ontbijten en te luchen, de altijd werkende server en de mooie plaatjes in dit proefschrift. Tot slot, lieve pa en ma, dank jullie voor de onvoorwaardelijke steun en het vertrouwen, zelfs als ik weer eens aan de zoveelste studie begon. Corine Kruiswijk 6 contents chapter 1 9 General Introduction chapter 2 23 Major Histocompatibility Genes in Cyprinid Fishes: Theory and Practice chapter 3 49 Analysis of Genomic and Expressed Major Histocompatibility Class ia and Class ii Genes in a Hexaploid Lake Tana African ‘Large’ Barb Individual (Barbus intermedius) chapter 4 77 Different Modes of Major Histocompatibility Class ia and Class iib Evolution in the Lake Tana African ‘Large’ Barb Species Flock chapter 5 117 A Novel Functional Class i Lineage in Zebrafish (Danio rerio), Common Carp (Cyprinus carpio) and African ‘Large’ Barb (Barbus intermedius), Showing an Unusual Conservation of the Peptide Binding Domains chapter 6 147 General Discussion references 161 summary 175 samenvatting 179 curriculum vitæ 183 7 Voor Menna chapter 1 GENERAL INTRODUCTION Corine P. Kruiswijk Cell Biology and Immunology Group, Wageningen Institute of Animal Sciences, Wageningen University, po box 338, 6700 ah Wageningen, The Netherlands. introduction All living organisms are exposed to pathogens in all life history stages and must prevent invasion or destruction by them to survive. Various phyla of the animal kingdom exploit different strategies to achieve defence against patho- gens. Broadly speaking these strategies fall in two categories: innate (or non- specific) immune responses and adaptive (or specific) immune responses. Dur- ing evolutionary processes, both categories have not always coexisted. Through- out the animal kingdom, defence strategies involving adaptive immunity appear to have arisen first in members of the vertebrate monophyletic lineage of Gnathostomes (from sharks to man), while adaptive immunity is absent in more primitive vertebrates belonging to the superclass Agnatha (e.g. lamprey, hagfish) and invertebrates. Among Gnathostomes, the essential architecture of the adaptive immune system, as we know it in mammals, seems well preserved with only some minor variations. 9 chapter 1 A. Class i molecule Class ii molecule peptide binding groove Alpha-2 Alpha-1 Alpha-1 Beta-1 s-s membrane distal s s Alpha-3 Alpha-2 Beta-2 S S membrane-proximal S (Ig-fold structure) S S S S S ß2microglobulin transmembrane cytoplasmic region B. C. peptide binding groove Alpha-1 Alpha-2 Alpha-1 Alpha helix Beta strands ß2 microglobulin Alpha-3 Alpha-2 Disulphide bonds Figure 1: The structure of mhc molecules. (a) Schematic representation of the mhc class i and class ii molecules. Disulphide bonds are indicated by s-s.(b) Three dimensional structure of a mhc class i molecule as seen from the side or (c) from the top (Modified82). 10 chapter 1 Two subfamilies of cell surface glycoproteins that play a crucial role in adaptive immunity are the major histocompatibility complex (mhc) class i and class ii molecules. The history of major histocompatibility complex molecules starts at the beginning of the previous century with the discovery of their role in trans- plant rejections1. However,their biological function remained unknown until the end of the sixties2, 3. Mhc class i and class ii genes encode structurally sim- ilar molecules that are equipped to bind degraded self and non-self peptides which they display to particular cells of the immune system. Displaying degrad- ed non-self peptides derived from viral,bacterial or parasitic pathogens will trigger an immune response. The first mhc gene was isolated from human4 in 1980,while eight years later the first non-mammalian mhc equivalent was isolated from chicken5. The last to follow were class i and class ii genes in teleosts6 (bony fishes) in 1990.Approx- imately half of all extant vertebrate species belong to the group of bony fishes, with 20,000 representative species with an immense variety, which are found in many different aquatic ecosystems. This large group of bony fishes include cyprinids like the African ‘large’ barb (Barbus intermedius),common carp (Cypri- nus carpio),and zebrafish (Danio rerio). structure and function of mhc molecules Mhc class i molecules are transmembrane heterodimers of a heavy alpha chain ™ (Mr 45,000) non-covalently associated with a light chain ß -microglobulin (Mr 12,000). The heavy chain consists of three extra-cellular domains designated alpha-1 to alpha-3,a transmembrane and a cytoplasmic regionfig. 1(). The alpha-2 and alpha-3 domains both possess intrachain disulphide bridges enclosing approxi- mately 60 to 85 amino acids. The membrane proximal alpha-3 domain of the alpha chain and the ß™-microglobulin are both homologous with the immunoglob- ulin c1 domains. The membrane distal alpha-1 and alpha-2 domains constitute a platform of eight anti-parallel beta-strands supporting two anti-parallel alpha- helices. The disulphide bridge in the alpha-2 domain connects the n-terminal beta-strand with the alpha-helix of this domain. The two alpha-helices of the alpha-1 and alpha-2 domain are separated by a long groove with occluded ends which accommodates peptides of nine to twelve amino acids in length7,8. The extra-cellular domains of mhc molecules are encoded by single exons, 11 chapter 1 with exception of the class iib exon-3 of the Acanthopterygii which has acquired an intron9. Several exon-intron organisations of mhc genes have been observed among vertebrates. The exon-intron organisations differ in the number of exons encoding regions other than the extra-cellular domains. Mhc class i genes usu- ally consist of eight exons and seven introns, while class ii genes consist of four to six exons separated by three to five introns. Large differences are known to exist for intron lengths (reviewed10,11).
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