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Marvel Umbc 0434D 12055.Pdf APPROVAL SHEET Title of Dissertation: The Roles of Gonadotropin-releasing Hormone 2 (Gnrh2) in Feeding and Reproduction in Zebrafish: A Potential Mediator of These Interlinked Processes Name of Candidate: Miranda Marvel Doctor of Philosophy, 2019 Dissertation and Abstract Approved: _________________________________ Dr. Yonathan Zohar Professor and Chair Department of Marine Biotechnology Date Approved: ___________________ ABSTRACT Title of Document: THE ROLES OF GONADOTROPIN- RELEASING HORMONE 2 (GNRH2) IN FEEDING AND REPRODUCTION IN ZEBRAFISH: A POTENTIAL MEDIATOR OF THESE INTERLINKED PROCESSES Miranda M. Marvel, Doctor of Philosophy, 2019 Directed By: Professor and Chair, Yonathan Zohar, Ph.D., Department of Marine Biotechnology Gonadotropin-releasing hormone (GNRH) is the neuropeptide in vertebrates most well-known for controlling reproduction and stimulating the gonadotropins, luteinizing hormone (LH) and follicle-stimulating hormone (FSH), from the pituitary. The gonadotropins circulate to the gonads and stimulate steroidogenesis and gametogenesis. There are three forms of GNRH, named for their location and function in the brain. GNRH1 is known to be the main hypophysiotropic isoform regulating gonadotropin release. GNRH2 is found in the midbrain and, despite being the most evolutionarily conserved and ubiquitous, is the least studied form among the three, most likely due to the absence of GNRH2 protein in common murine research models. Zebrafish, another common vertebrate model for genetic manipulation and biological studies, possesses Gnrh2 and is therefore an ideal organism to study this neuropeptide. Through a combination of gene knockout/knockdown, neuroanatomical imaging, and functional assays, the roles of Gnrh2 in zebrafish were comprehensively explored. Gnrh2 knockout (gnrh2-/-) zebrafish demonstrated decreased lhb expression, compromised oocyte quality, increased feeding and growth, and, most strikingly, major inhibition of spawning and oocyte maturation after long-term fasting. Neuroanatomical assays confirmed that Gnrh2 projected more neurons to gonadotropes under fasting conditions, whereas Gnrh3 was inhibited. Interestingly, Gnrh2 was unable to compensate for Gnrh3 loss, as double knockout (gnrh2-/-;gnrh3-/-) zebrafish displayed normal reproduction. Through transcriptomics and qPCR, novel differentially expressed reproductive factors were discovered in knockout zebrafish, with potential reproductive regulatory roles. Additionally, examination of Gnrh2 neuronal projections identified fibers innervating melatonin cells, neurons of the feeding factor, Agouti-related peptide 1 (Agrp1), and neurons of the reproduction regulator, Gonadotropin-inhibitory hormone (Gnih). Gnrh2 was also able to modulate gnih and agrp1 expression. Additionally, a previously unstudied population of Gnrh2 was identified in the olfactory region and multiple experiments implicated these neurons in transducing pheromonal cues, and thus affecting reproductive behavior. Overall, Gnrh2 most likely has roles in stimulating lhb expression, maintaining oocyte quality, transducing pheromonal cues, and reducing feeding behavior through the modulation of agrp1 and potentially melatonin. Under fasting conditions, Gnrh2 exhibits plasticity to become the main hypophysiotropic stimulator of gonadotropin secretion. Gnrh2 therefore appears to be an important upstream factor mediating feeding and reproductive processes in vertebrates. THE ROLES OF GONADOTROPIN-RELEASING HORMONE 2 (GNRH2) IN FEEDING AND REPRODUCTION IN ZEBRAFISH: A POTENTIAL MEDIATOR OF THESE INTERLINKED PROCESSES By Miranda Marvel Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, Baltimore County in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2019 Advisory Committee: Professor Yonathan Zohar, Ph.D., Chair Associate Professor Shaojun “Jim” Du, Ph.D. Professor and Chair Margaret McCarthy, Ph.D. Associate Professor Sheng Bi, Ph.D. Assistant Professor Edward Orlando, Ph.D. © Copyright by Miranda Marvel 2019 Dedication This dissertation is dedicated to my grandfather, Robert L. Marvel, who instilled in me a love for the environment and critters of the Chesapeake Bay, which motivated me to pursue a career in environmental sciences, and whom unfortunately passed away before his time in the midst of my graduate studies. I also dedicate this work to my biology teachers and professors, whose passion for science motivated me to continue a path in this field ii Acknowledgements I would like to recognize my colleagues, friends, and family of whom this dissertation would not have been possible without. First and foremost, I would like to thank my advisor, Dr. Yonathan Zohar, who believed in me from the start and hasn’t stopped supporting me since. He has given me all of the advice, help, and resources that I needed to conduct a thorough research project in his lab, but also allowed me the freedom and supported my independence in coming up with my own experiments and following whichever paths of investigation I wanted to pursue. I would like to thank the members of my committee, Dr. Du, Dr. McCarthy, Dr. Orlando, and Dr. Bi for their advice and guidance in improving my research and studies. I am thankful to Dr. Berta-Levavi Sivan and her graduate student, Lian Hollander-Cohen, who hosted me in their lab for three months and mentored me in confocal microscopy, ELISA’s, and many experimental procedures, as well as Dr. Yoav Gothilf who hosted me for a very busy but productive week in his lab, and thanks to Dr. Laura Gabriela Nisembaum for conducting the HPLC analysis for melatonin measurements. I also want to thank my mentor, Dr. Nilli Zmora, who has been there as a constant source of information, guidance, and support from the beginning to the end of my dissertation. She has given me integral advice and encouragement on all things ranging from experimental assays to writing guidance and has been a crucial mentor and friend, helping me grow as a researcher and a person. I express my gratitude to Dr. Ten-Tsao Wong, who advised me on all things zebrafish- related, and mentored me in conducting many experiments, as well as always being there for me when I needed advice or suggestions, frequently and willingly taking hours out of his day to help and mentor me. I also want to express my thanks to my former fellow iii graduate student in the Zohar lab, Dr. Olivia Smith Spicer, who helped to mentor and train me in the beginning of my studies, and was always there for any questions that I needed answered about experiments, fish, or student-related issues. She was also a great friend and conference partner, and I will always value her patience, support, and mentorship while we were students together. I want to thank Mr. John Stubblefield, Ms. Teressa Freeman, and Ms. Mildred Homa for all of their help with lab management and administrative matters, keeping me and the lab on track with logistical issues. I also want to thank Ms. Sakura Tanaka, a fellow graduate student in the Zohar lab, for her help and advice with conducting experiments and feeding fish, and her friendship and support as we navigated our graduate studies together. Her friendship, along with that of the other graduate students at the Institute of Marine and Environmental Technology, was essential in keeping me sane and motivated to finish my studies. I want to thank Ms. Sabeena Nazar from the BAS Lab for her advice and help with sequencing and thank the ARC staff who kept the zebrafish facility running and continually improving, making sure our research animals were happy and healthy. I would like to also thank my family and friends who supported me and cheered me on throughout this journey. Finally, I would like to thank my significant other, Shaun Miller, who was by my side for the entirety of my graduate studies, and put up with the long hours of classwork, lab work, and writing. His love and support motivated me to get through all the obstacles and to conduct the best work that I could achieve. iv TABLE OF CONTENTS Chapter 1: Introduction………………………………………………………………….1 1.1. Neuroendocrine control of reproduction………………………………1 Overview…………………………………………………………..1 1.2. Neuroendocrine control of feeding……………………………………4 Overview…………………………………………………………4 Feedback between feeding and reproductive systems…………….5 1.3. Gonadotropin-releasing hormone family……………………………...7 Discovery………………………………………………………….7 Distribution and variance amongst species………………………..7 Multiplicity of isoforms……………………………………………8 Roles of Gnrh1 in mammals……………………………………...10 Roles of Gnrh1 in teleosts………………………………………...11 Roles of Gnrh3 in teleosts………………………………………...12 1.4. Gonadotropin-releasing hormone 2 (Gnrh2) ………………………..14 Discovery………………………………………………………...14 Previous research on potential roles in reproduction……………..15 Previous research on potential roles in feeding…………………...16 Previous research on non-canonical roles in other systems………17 1.6 Zebrafish as a model organism for studying Gnrh2………………….19 1.7 Hypotheses and objectives……………………………………………21 Chapter 2: Studying the Roles of Gnrh2 in Reproduction……………………………24 Abstract………………………………………………………………………..…24 Introduction………………………………………………………………………25 Methods…………………………………………………………………………..28 Results……………………………………………………………………………39 Discussion………………………………………………………………………..52 Chapter 3: Investigating the Roles of Gnrh2 in Feeding and Growth………………..63 Abstract…………………………………………………………………………..63 Introduction………………………………………………………………………64 Methods…………………………………………………………………………..66
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