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ANALYSIS of HAPLOTYPE STRUCTURE in the BOVINE MAJOR HISTOCOMPATIBILITY COMPLEX a Dissertation by KRISTA L. FRITZ Submitted to T

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ANALYSIS OF HAPLOTYPE STRUCTURE IN THE BOVINE MAJOR HISTOCOMPATIBILITY COMPLEX A Dissertation by KRISTA L. FRITZ Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY December 2009 Major Subject: Genetics ANALYSIS OF HAPLOTYPE STRUCTURE IN THE BOVINE MAJOR HISTOCOMPATIBILITY COMPLEX A Dissertation by KRISTA L. FRITZ Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Approved by: Chair of Committee, Loren C. Skow Committee Members, Bhanu P. Chowdhary Chistine G. Elsik James E. Womack Intercollegiate Faculty Chair, Craig J. Coates December 2009 Major Subject: Genetics iii ABSTRACT Analysis of Haplotype Structure in the Bovine Major Histocompatibility Complex. (December 2009) Krista L. Fritz, B.S., University of Illinois Chair of Advisory Committee: Dr. Loren C. Skow The goal of this project was to identify and characterize polymorphic markers spanning regions of the bovine major histocompatibility complex (BoLA) to analyze patterns of genetic variation and haplotype structure across diverse cattle breeds with various breed histories and selection pressures. Genetic markers that demonstrated sufficient levels of polymorphism, locus specificity, Mendelian inheritance, and the accurate typing of alleles across diverse haplotypes were chosen to define separate haplotype structures for the BoLA IIb and BoLA IIa-III-I regions and to evaluate breakpoints in linkage disequilibrium within the regions surrounding BoLA IIa-III-I. A total of 23 microsatellites, two SNPSTRs, 62 SNPs, and the alleles of three class IIa genes were selected for use in this study. These markers revealed eleven recombination events, low levels of recombination in BoLA IIa-III-I, a sharp break in haplotype structure in the region centromeric to class IIa, prolonged linkage disequilibrium in the extended class I region, strong conservation of BoLA IIa-III-I haplotype structure, BoLA IIa-III-I homozygous haplotype identity across seven different breeds of cattle, and a small number of common BoLA IIa-III-I haplotypes within the Angus and Holstein breeds. This work demonstrated that 52 SNPs from the Illumina 50K SNPchip could accurately predict BoLA IIa-III-I haplotypes. These 52 SNPs represent tagSNPs that can predict BoLA IIa-III-I genetic variation and could offer a cost-effective means for screening large sample sizes for haplotype/disease association studies in the future. iv DEDICATION This work is dedicated to all the family, friends, and teachers that have encouraged me to pursue a higher education. You have been an invaluable source of optimism and support, and I could not have done this without you! None of us got where we are solely by pulling ourselves up by our bootstraps. We got here because somebody - a parent, a teacher, an Ivy League crony or a few nuns - bent down and helped us pick up our boots. - Thurgood Marshall An educated man should know everything about something, and something about everything. - C.V. Wedgwood If you want immediate change, higher education is not the place for you. - Laura Saunders We must remember that intelligence is not enough. Intelligence plus character - that is the goal of true education. - Martin Luther King, Jr. v ACKNOWLEDGEMENTS I would like to thank my committee chair, Dr. Loren Skow, for his mentorship and unremitting enthusiasm for new scientific discoveries. I would also like to thank my committee members, Dr. James Womack, Dr. Christine Elsik, and Dr. Bhanu Chowdhary; and Texas A&M faculty members Dr. James Derr, Dr. Natalie Halbert, Dr. Clare Gill, Dr. John Huber, Dr. Terje Raudsepp, Dr. Paul Samollow and Dr. Jane Welsh all for their guidance and support throughout the course of this research. Thank you to everyone who has given me DNA samples for this project, including Dr. Clare Gill and the Bovine HapMap Consortium for the Bovine HapMap Project DNA samples, Dr. Robert Schnabel and Dr. Jerry Taylor of the University of Missouri for the BoLA homozygous DNA samples, Dr. James Derr and Dr. Natalie Halbert for Yellowstone National Park Bison DNA samples, Dr. Waithaka Mwangi for the DRB3*1101 defined Holstein DNA samples, Dr. James Womack, Elaine Owens, and Jan Elliott for DNA samples from the Bovine International Reference Families and L1 Dominette, and Dr. Pia Untalan, Dr. Pat Holman, and Dr. Penny Riggs for the DNA samples from the Lone Star tick resistance study. Thanks to Candice Brinkmeyer-Langford for her moral support, her help in making phylogenetic trees, and her countless deliveries of my samples to SeqWright. Thanks to Dr. John Huber for overcoming the odds of generating haplotypes with PHASE, to Dr. Clare Gill for analyzing BoLA markers from the HapMap data set with fastPHASE, and to Prasanth Ganta for his bioinformatics assistance in creating an independent approach to analyzing BoLA haplotypes. My special appreciation goes out to former lab technicians Marian Cothran and Renu Chowdhary who made so many genotyping reactions possible! I hope you all feel some sense of ownership for the exciting findings of this research. I would also like to extend my gratitude to the sources of funding for this research, which include the USDA NRI grant 97-35205 5074 and the College of Veterinary Medicine at Texas A&M University. vi TABLE OF CONTENTS Page ABSTRACT............................................................................................................... iii DEDICATION........................................................................................................... iv ACKNOWLEDGEMENTS....................................................................................... v TABLE OF CONTENTS........................................................................................... vi LIST OF FIGURES ................................................................................................... viii LIST OF TABLES..................................................................................................... ix CHAPTER I INTRODUCTION........................................................................................ 1 Project Rationale................................................................................... 1 The Major Histocompatibility Complex............................................... 1 The Value of MHC Disease Association Studies ................................. 29 The Genetic History of Domestic Cattle............................................... 38 The Bovine Genome Project................................................................. 58 Aims and Goals of This Project............................................................ 68 II MATERIALS AND METHODS................................................................. 70 Sources of DNA.................................................................................... 70 Genotyping and Selection of BoLA Microsatellites............................. 74 Observed Recombination Events........................................................... 82 Additional Genetic Markers................................................................... 82 Analysis of BoLA Single Nucleotide Polymorphisms .......................... 89 Haplotypes Inferred from BoLA Heterozygotes.................................... 91 III RESULTS ................................................................................................... 93 Genotyping and Selection of BoLA Microsatellites.............................. 93 Observed Recombination Events........................................................... 97 Additional Genetic Markers................................................................... 104 Analysis of BoLA Single Nucleotide Polymorphisms .......................... 110 Haplotypes Inferred from BoLA Heterozygotes.................................... 137 Summary of Results............................................................................... 140 IV DISCUSSION AND CONCLUSIONS ...................................................... 142 Genotyping and Selection of BoLA Microsatellites.............................. 142 vii Page Observed Recombination Events........................................................... 152 Additional Genetic Markers................................................................... 155 Analysis of BoLA Single Nucleotide Polymorphisms .......................... 159 Haplotypes Inferred from BoLA Heterozygotes.................................... 164 Addressing Criticisms of tagSNPs and Haplotypes............................... 169 Implications for Future Research........................................................... 172 REFERENCES .......................................................................................................... 174 APPENDIX ............................................................................................................... 207 VITA.......................................................................................................................... 290 viii LIST OF FIGURES Page Figure 1 Reduced Gene Map of the Human MHC........................................... 11 Figure 2 The Structure of MHC Class I and II Molecules ............................... 13 Figure 3 Extended Gene Map of the Human MHC.......................................... 19 Figure 4 Reduced Recombination Rate in BoLA IIa-III-I ............................... 25 Figure 5 The Worldwide
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