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University of Florida Thesis Or Dissertation Formatting THE ROLE OF OTARINE HERPESVIRUS 1 IN CALIFORNIA SEA LION (ZALOPHUS CALIFORNIANUS) UROGENITAL CARCINOMA . By ALISSA C. DEMING A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2018 © 2018 Alissa C. Deming To my family ACKNOWLEDGMENTS I thank my parents for always supporting my educational endeavors and instilling in me a love, respect and curiosity of nature which has driven me along my path. I want to thank my mother, father, brother, sister-in-law, nanny, aunt, cousin and friends for encouraging me to follow my dreams. I also thank my primary advisors, James Wellehan and Frances Gulland, for their constant support throughout my career. Particular thanks go to Katie Colegrove for her constant support through this process. I am additionally grateful to the members of my committee: Rowan Milner, Rolf Renne, and Nancy Denslow, for their invaluable support and advice. Also, I want to thank Linda Archer and April Childress for their fearless leadership in the lab. I am also thankful to my friends and coworkers including Ashley Barratclough, Cara Field, Padraig Duignan, Christine Fontaine, Barbie Halaska, Tenaya Norris, Sophie Whoriskey, Sophie Guarasci, Jennifer Luff, Galaxia Cortes, and Jessica Jacobs for their personal and academic support. I am also indebted to The Marine Mammal Center (TMMC) for awarding me the Geoffrey Hughes Veterinary Research Fellowship, which provided financial support for my PhD research, without which this project would have never been possible. A huge thanks to all the incredible volunteers, veterinary technicians, research biologists, and staff that make the rehabilitation and research that is done at The Marine Mammal Center possible. And most importantly, a special thanks to all the California sea lions with and without cancer that made this study possible- even in your death you shed light. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 7 LIST OF FIGURES .......................................................................................................... 8 LIST OF ABBREVIATIONS ........................................................................................... 10 ABSTRACT ................................................................................................................... 12 CHAPTER 1 SEA LIONS, CANCER, AND VIRUSES.................................................................. 14 Urogenital Carcinoma in California Sea Lions ........................................................ 14 Cancer .................................................................................................................... 18 Oncogenic Viruses .................................................................................................. 20 Herpesviruses ......................................................................................................... 22 Latently Expressed Viral Proteins: LANA/EBNA1 and vFLIP ........................... 25 Host-derived Viral Genes: vBCL2 and vCDK4 ................................................. 26 Endogenous Viral Elements ............................................................................. 27 2 PREVALENCE OF UROGENITAL CARCINOMA IN STRANDED CALIFORNIA SEA LIONS (ZALOPHUS CALIFORNIANUS) FROM 2005-2015 ........................... 32 Background ............................................................................................................. 32 Materials and Methods............................................................................................ 33 Retrospective Data Collection .......................................................................... 33 Statistics ........................................................................................................... 34 Results .................................................................................................................... 34 Prevalence of Urogenital Carcinoma ................................................................ 34 Urogenital Carcinoma in Adults versus Subadults and Juviniles ...................... 34 Histologic Evaluation ........................................................................................ 35 Metastatic Lesions in Urogenital Carcinoma .................................................... 35 Temporal Trends in Prevalence of Urogenital Carcinoma ................................ 36 Discussion .............................................................................................................. 36 3 OTARINE HERPESVIRUS 1 GENOME AND ONCOGENES ................................. 43 Background ............................................................................................................. 43 Materials and Methods............................................................................................ 44 Sample Collection ............................................................................................ 44 DNA Extraction and PCR Screening ................................................................ 45 OtHV1 and OtHV4 qPCR for Viral Load Assessment ....................................... 46 5 OtHV1 Genome Sequencing ............................................................................ 48 OtHV4 Genome Sequencing ............................................................................ 50 Bioinformatics and De Novo Assemblies .......................................................... 51 Gene Comparisons: Percent Identity and Differences of Select Genes ........... 52 Phylogenic Analysis ......................................................................................... 52 Results .................................................................................................................... 54 Histological Classification ................................................................................. 54 PCR and qPCR Results ................................................................................... 54 OtHV1 Genome Assembly ............................................................................... 55 OtHV4 Genome Assembly ............................................................................... 56 OtHV1 and OtHV4 Annotation and Genome Comparison ................................ 58 OtHV1 and OtHV4 Percent Identity and Distance Comparisons ...................... 61 OtHV1 and OtHV4 Represent New Oceanic Gammaherpesvirus Genus ........ 62 Discussion .............................................................................................................. 62 4 OTHV1 GENE EXPRESSION IN UROGENITAL CARCINOMA ............................. 77 Background ............................................................................................................. 77 Materials and Methods............................................................................................ 81 Cases and Tissue Preparation ......................................................................... 81 Basescope in situ Hybridization ...................................................................... 83 Image Analysis ................................................................................................. 85 Data Analysis ................................................................................................... 86 Results .................................................................................................................... 86 Gross Findings ................................................................................................. 86 Histological Classification ................................................................................. 87 OtHV1 Gene Expression in Sea Lion Urogenital Carcinoma ............................ 88 Discussion .............................................................................................................. 90 5 CONCLUSION ...................................................................................................... 105 LIST OF REFERENCES ............................................................................................. 107 BIOGRAPHICAL SKETCH .......................................................................................... 116 6 LIST OF TABLES Table page 2-1 Prevalence of urogenital carcinoma in California sea lions (Zalophus californianus) of different age and sex classes ................................................... 38 2-2 Non-urogenital carcinoma cancer in California sea lions (Zalophus californianus) ...................................................................................................... 39 2-3 Number and prevalence of various stages of urogenital carcinoma diagnosed histologically in juvenile, subadult and adult California sea lions ........................ 40 3-1 Herpesvirus species list for concatenated phylogenetic tree. ............................. 66 3-2 Herpesvirus gene list for concatenated phylogenetic tree. ................................. 67 4-1 Normal cervical or vaginal cases from California sea lions ................................. 96 4-2 Urogenital carcinoma cases from California sea lions ........................................ 97 4-3 Basescope custom probes targeting
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