Genetic Dissection of Neuromuscular Diseases Affecting Domestic Dogs Caitlin Rinz Clemson University

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Genetic Dissection of Neuromuscular Diseases Affecting Domestic Dogs Caitlin Rinz Clemson University Clemson University TigerPrints All Dissertations Dissertations 12-2014 Genetic Dissection of Neuromuscular Diseases Affecting Domestic Dogs Caitlin Rinz Clemson University Follow this and additional works at: https://tigerprints.clemson.edu/all_dissertations Part of the Genetics and Genomics Commons Recommended Citation Rinz, Caitlin, "Genetic Dissection of Neuromuscular Diseases Affecting Domestic Dogs" (2014). All Dissertations. 1678. https://tigerprints.clemson.edu/all_dissertations/1678 This Dissertation is brought to you for free and open access by the Dissertations at TigerPrints. It has been accepted for inclusion in All Dissertations by an authorized administrator of TigerPrints. For more information, please contact [email protected]. GENETIC DISSECTION OF NEUROMUSCULAR DISEASES AFFECTING DOMESTIC DOGS ________________________________________________________ A Thesis Presented to the Graduate School of Clemson University ________________________________________________________ In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Genetics ________________________________________________________ by Caitlin Rinz December 2014 ________________________________________________________ Accepted by: Dr. Leigh Anne Clark Dr. Amy Lawton-Rauh Dr. Meredith Morris Dr. Christopher Saski ABSTRACT The domestic dog, Canis familiaris, has a unique population structure that lends itself to the study of hereditary diseases. Purebred dogs populations are genetically isolated and as a result are affected by more than 400 naturally occurring diseases, many of which have human counterparts. In the last 15 years, dogs have emerged as a model for the study of human hereditary diseases, fueling the development of resources including a 7.6X coverage reference genome and single nucleotide polymorphism (SNP) genotyping arrays. Congenital myasthenic syndrome (CMS) is a neuromuscular disorder of both humans and dogs in which transmission across the neuromuscular junction is compromised. Affected individuals exhibit generalized muscle weakness that is exacerbated with exercise. To date, 18 genes are known to harbor mutations causative for CMS in humans. We characterized a novel CMS in a family of Labrador Retrievers. Using whole genome SNP profiles we identified COLQ as a candidate gene. In the neuromuscular junction, ColQ acts as an anchor for acetylcholinesterase, which is responsible for terminating the signal for muscle contraction. Sequencing revealed a missense mutation in exon 14 that predicts the substitution of a threonine for an isoleucine at a conserved position. The Jack Russell Terrier (JRT) is the first dog breed in which CMS was reported in the 1970s. Immunohistochemistry revealed an acetylcholine receptor (AChR) deficiency in affected dogs. Analysis of microsatellites flanking the five AChR subunit genes indicated that haplotypes encompassing CHRNB1 and CHRNE are consistent with ii inheritance identical by descent. Sequencing revealed a frameshift mutation in exon 7 of CHRNE (G193RfsX272) that is homozygous in recent CMS cases, as well as those from the 1970s. Congenital idiopathic megaesophagus (ME) is another neuromuscular condition observed in both humans and dogs characterized by an enlarged esophagus. Affected dogs are unable to move food into their stomachs, resulting in regurgitation and frequent aspiration pneumonia. ME is prevalent among German Shepherd Dogs (GSDs). We employed a genome-wide association study to identify genomic regions harboring genes underlying ME. Using 19 affected and 177 unaffected GSDs, we identified an associated region on chromosome 12. iii Acknowledgements I would like to thank my family – my parents Anita and Dave, my sisters Alex and Cyndee, my brothers Josh and Nate – for their love and support during my time as a PhD student and throughout my life. Thank you to everyone in my lab – Dr. Leigh Anne Clark, Dr. Kate Tsai, Dr. Alison Starr-Moss, Dr. Rooksie Noorai – for their instruction, help, and guidance. To Jacquelyn Evans, who joined us as a graduate student, and the various other undergraduate students that worked in our lab, thank you for teaching me patience and reminding me how exciting genetics can be to work with and learn. To my other committee members, Dr. Amy Lawton-Rauh, Dr. Meredith Morris, and Dr. Chris Saski, thank you for your help and your suggestions from other points of view and helping me to see things outside of the scope of my lab. To the dog owners, breeders, and veterinarians, thank you for your enthusiasm for and participation in our studies. Finally, to Lily, Joy, Rylie, Beau, and all the other dogs in my life, thank you for reminding me why I do what I do and why finding the mutations involved in canine genetic diseases is so important. iv TABLE OF CONTENTS Page TITLE PAGE .................................................................................................................... i ABSTRACT ..................................................................................................................... ii ACKNOWLEDGMENTS .............................................................................................. iv LIST OF TABLES ........................................................................................................... v LIST OF FIGURES ........................................................................................................ vi CHAPTERS 1. INTRODUCTION ........................................................................................... 1 Dog as a Model System ........................................................................... 1 Identification of Pathogenic Mutations .................................................... 4 Congenital Myasthenic Syndromes ......................................................... 9 Congenital Idiopathic Megaesophagus .................................................. 16 The Bigger Picture ................................................................................. 17 References .............................................................................................. 20 2. A COLQ MISSENSE MUTATION IN LABRADOR RETRIEVERS HAVING CONGENITAL MYASTHENIC SYNDROME ...................................................................... 27 Abstract .................................................................................................. 28 Introduction ............................................................................................ 29 Materials and Methods ........................................................................... 31 Results .................................................................................................... 37 Discussion .............................................................................................. 45 Acknowledgements ................................................................................ 48 References .............................................................................................. 48 3. A CHRNE FRAMESHIFT MUTATION CAUSES CONGENITAL MYASTHENIC SYNDROME IN JACK RUSSELL TERRIERS .................................................................. 51 Abstract .................................................................................................. 51 Introduction ............................................................................................ 52 Materials and Methods ........................................................................... 54 v Table of Contents (Continued) Page Results .................................................................................................... 59 Discussion .............................................................................................. 64 Acknowledgements ................................................................................ 68 References .............................................................................................. 68 4. GENOME-WIDE ASSOCIATION STUDIES FOR MULTIPLE DISEASES OF THE GERMAN SHEPHERD DOG ......................................................................................... 71 Abstract .................................................................................................. 75 Introduction ............................................................................................ 75 Materials and Methods ........................................................................... 79 Results .................................................................................................... 82 Discussion .............................................................................................. 88 Acknowledgements ................................................................................ 93 References .............................................................................................. 93 5. CONCLUSIONS, FUTURE DIRECTIONS, AND APPLICATIONS ........................................................................................... 99 A COLQ Missense Mutation in Labrador Retrievers Having Congenital Myasthenic Syndrome ................................ 99 A CHRNE frameshift mutation causes congenital myasthenic syndrome in Jack Russell Terriers ........................ 101 Genome-wide association studies for multiple diseases of the German Shepherd Dog .................................................. 102 Final Thoughts ..................................................................................... 103 References
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