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The Metabolism of Androstenone and Other Steroid Hormone Conjugates in Relation to Boar Taint

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The Metabolism of Androstenone and Other Steroid Hormone Conjugates in Relation to Boar Taint The Metabolism of Androstenone and Other Steroid Hormone Conjugates in Relation to Boar Taint by Heidi M. Laderoute A Thesis presented to The University of Guelph In partial fulfillment of requirements for the degree of Master of Science in Animal and Poultry Science with Toxicology Guelph, Ontario, Canada © Heidi M. Laderoute, April, 2015 ABSTRACT THE METABOLISM OF ANDROSTENONE AND OTHER STEROID HORMONE CONJUGATES IN RELATION TO BOAR TAINT Heidi M. Laderoute Advisor: University of Guelph, 2015 Dr. E.J. Squires Increased public interest in the welfare of pigs reared for pork production has led to an increased effort in finding new approaches for controlling the unpleasant odour and flavour from heated pork products known as boar taint. Therefore, this study investigated the metabolism of androstenone and the enzymes involved in its sulfoconjugation in order to further understand the pathways and genes involved in the development of this meat quality defect. Leydig cells that were incubated with androstenone produced 3-keto- sulfoxy-androstenone, providing direct evidence, for the first time, that sulfoconjugation of this steroid does occur in the boar. In addition, human embryonic kidney cells that were overexpressed with porcine sulfotransferase (SULT) enzymes showed that SULT2A1, but not SULT2B1, was responsible for sulfoconjugating androstenone. These findings emphasize the importance of conjugation in steroid metabolism and its relevance to boar taint is discussed. ACKNOWLEDGEMENTS I would like to gratefully and sincerely thank my advisor, Dr. E. James Squires, for providing me with the opportunity to be a graduate student and for introducing me to the world of boar taint. This project would not have been possible without your guidance, encouragement, and patience over the last few years. I would also like to thank Dr. James Raeside and Dr. John Cant for serving on my committee and taking the time to provide me with valuable advice, information, and support on numerous aspects of my project. I am very grateful to Yanping Lou for her technical expertise and friendship. I wouldn’t have finished my studies without her ability to troubleshoot and keep the HPLC ‘Frankenstein monster’ alive. I am also grateful to Heather Christie for the time she spent assisting with early morning Leydig cell isolations and for her advice on different experimental approaches. I would also like to thank Dr. Dyanne Brewer from the Mass Spectrometry Facility at the University of Guelph for her help with sample analysis and interpretation. My thanks and appreciation also goes to my friends and colleagues in the Department of Animal and Poultry Science. To Dr. Matthew Gray, thank you for your patience in answering my many questions, for helping to isolate hepatocytes, and for teaching me how to run a Western blot. To my lab mates, both past and present, thank you for the well-needed distractions and for reminding me that it was okay to take breaks. Finally, thank you to my family and my amazing husband Chris. Your love and support were vital in keeping me sane throughout the writing process. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS ........................................................................................... III TABLE OF CONTENTS ............................................................................................... IV LIST OF FIGURES ...................................................................................................... VII LIST OF TABLES .......................................................................................................... IX LIST OF ABBREVIATIONS ......................................................................................... X CHAPTER 1: LITERATURE REVIEW ....................................................................... 1 1.1 INTRODUCTION ........................................................................................................... 1 1.2 ANDROSTENONE BIOSYNTHESIS ................................................................................. 4 1.2.1 Steroidogenesis ................................................................................................... 4 1.2.2 Biological Function ............................................................................................ 8 1.2.3 Accumulation in Adipose Tissue ....................................................................... 10 1.3 ANDROSTENONE METABOLISM ................................................................................ 11 1.3.1 Phase I Metabolism .......................................................................................... 11 1.3.2 Phase II Metabolism ......................................................................................... 13 1.3.2.1 Sulfoconjugation ........................................................................................ 13 1.3.2.2 Glucuronidation ......................................................................................... 20 1.3.3 Enterohepatic Circulation ................................................................................ 24 1.4 CONTROLLING BOAR TAINT ..................................................................................... 25 1.4.1 Early Slaughter ................................................................................................. 25 1.4.2 Sperm Sorting ................................................................................................... 26 1.4.3 Immunocastration ............................................................................................. 27 1.4.4 Genetic Selection .............................................................................................. 28 iv CHAPTER 2: HYPOTHESIS AND RESEARCH OBJECTIVES ............................ 30 2.1 HYPOTHESIS ............................................................................................................. 30 2.2 RESEARCH OBJECTIVES ............................................................................................ 30 CHAPTER 3: METABOLISM OF ANDROSTENONE IN PRIMARY CULTURED PORCINE LEYDIG CELLS AND HEPATOCYTES ............................................. 32 3.1 ABSTRACT ................................................................................................................ 32 3.2 INTRODUCTION ......................................................................................................... 33 3.3 MATERIALS AND METHODS ...................................................................................... 35 3.3.1 Reagents ........................................................................................................... 35 3.3.2 Research Animals ............................................................................................. 35 3.3.3 Leydig cell isolation ......................................................................................... 35 3.3.4 Hepatocyte isolation ......................................................................................... 36 3.3.5 Biosynthesis studies .......................................................................................... 37 3.3.6 High-Performance Liquid Chromatography (HPLC) ...................................... 37 3.3.7 Steroid Conjugate Analyses .............................................................................. 38 3.3.8 Mass Spectrometry ........................................................................................... 39 3.3.9 Data Analysis .................................................................................................... 40 3.4 RESULTS ................................................................................................................... 40 3.5 DISCUSSION .............................................................................................................. 49 CHAPTER 4: THE SULFOCONJUGATION OF ANDROSTENONE AND DEHYDROEPIANDROSTERONE BY HUMAN AND PORCINE SULT2A1 AND SULT2B1 ENZYMES ....................................................................................... 56 4.1 ABSTRACT ................................................................................................................ 56 v 4.2 INTRODUCTION ......................................................................................................... 57 4.3 MATERIALS AND METHODS ...................................................................................... 59 4.3.1 Materials ........................................................................................................... 59 4.3.2 Plasmid Constructs ........................................................................................... 60 4.3.3 Cell Culture Transfection and Enzyme Expression .......................................... 61 4.3.4 HPLC ................................................................................................................ 62 4.3.5 Steroid Conjugate Analyses .............................................................................. 63 4.3.6 Western Blot Analysis ....................................................................................... 63 4.3.7 Data Analysis .................................................................................................... 64 4.4 RESULTS ................................................................................................................... 65 4.5 DISCUSSION .............................................................................................................. 77 CHAPTER 5: GENERAL
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