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Folliculogenesis and Fertilization in the Domestic Dog: Application to Biomedical Research, Medicine, and Conservation

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Folliculogenesis and Fertilization in the Domestic Dog: Application to Biomedical Research, Medicine, and Conservation FOLLICULOGENESIS AND FERTILIZATION IN THE DOMESTIC DOG: APPLICATION TO BIOMEDICAL RESEARCH, MEDICINE, AND CONSERVATION A Dissertation Presented to the Faculty of the Graduate School of Cornell University in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy By Jennifer Beth Nagashima August 2015 © Jennifer Beth Nagashima FOLLICULOGENESIS AND FERTILIZATION IN THE DOMESTIC DOG: APPLICATIONS TO BIOMEDICAL RESEARCH, MEDICINE, AND CONSERVATION Jennifer Beth Nagashima, Ph.D. Cornell University 2015 Understanding of reproductive biology in canids, including the domestic dog, is surprisingly limited. This includes the regulators of ovarian follicle development, and mechanisms of anestrus termination, fertilization and embryo development. In turn, this lack of understanding has limited our ability to develop assisted reproductive technologies (ART) for endangered canid conservation efforts. ART of interest include in vitro follicle culture for maternal genome rescue, estrus induction protocols, and in vitro fertilization (IVF). Here, we describe: 1) Studies evaluating the stage-specific requirements for follicle stimulating hormone (FSH), luteinizing hormone (LH), and activin on domestic dog follicle development in vitro. We demonstrate the beneficial effects of FSH and activin on growth, and activin on antrum expansion and oocyte health in short term culture. 2) Evaluation of serum collected during the anestrus to estrus transition revealing a significant increase in anti-Müllerian hormone (AMH) during proestrus, likely originating from increased numbers of antral follicles during this time. 3) The birth of the first live puppies from IVF embryos utilizing in vivo matured oocytes. Further, consistently high rates of embryo production are obtained using the described system, with no effect of progesterone supplementation to embryo culture media. Improved knowledge of the drivers of follicle development inform understanding of the resumption of estrus cyclicity, which in turn is needed to explore mechanisms of oocyte maturation prior to fertilization. In vitro fertilization is also required to assess the developmental capacity of oocytes grown from cultured follicles. Thus, these combined discoveries represent significant advancements in the understanding of canid reproductive biology and potential application to development of ART for the management of biomedical research colonies and for endangered canid conservation. P a g e | iii BIOGRAPHICAL SKETCH Jennifer Nagashima was born in Chigasaki, Japan but grew up in southern California. As a middle school student she became interested in endangered animal conservation, which she pursued through volunteer education and animal enrichment work at her local zoo. Following completion of an International Baccalaureate Diploma programme in high school, she attended Cornell University, receiving her B.S. in animal science with a minor in education in 2009. She then completed two internships with the Smithsonian Conservation Biology Institute (SCBI), researching African lion reproductive endocrinology and domestic dog ovarian follicle culture. Her experiences at SCBI introduced her to the world of reproductive research for animal conservation, which became a passion she pursued as the inaugural student of the Cornell-Smithsonian Joint Graduate Training Program (JGTP). Under the dual guidance of Dr. Alexander Travis at the Baker Institute for Animal Health at Cornell University and Dr. Nucharin Songsasen at SCBI, she began a Ph.D. program in the field of Zoology and Wildlife Conservation studying reproduction in domestic dogs for application to endangered canid conservation efforts. Upon completion of her Ph.D., Jennifer Nagashima will continue her research career as a Smithsonian Institution Postdoctoral Fellow in Front Royal, VA. P a g e | iv ACKNOWLEDGEMENTS I have been so fortunate to learn from the expertise of two wonderful mentors, Drs. Nucharin Songsasen and Alexander Travis. Nuch - thank you for introducing me to the joy of science and teaching me how to ask the right questions. My internship with you truly was what inspired me to pursue this career path, and I am so glad I did. Alex - thank you for motivating me to be the best scientist I can be. You have been a wealth of support and advice, both in science and navigating the science world, and I am incredibly lucky to have you as a mentor. Thanks also to my wonderful committee members, Drs. Ned Place and George Kollias, I appreciate your expert insight and continued guidance. To my fellow lab-mates, past and present, you make coming to work not like coming to work. At Cornell, I’d like to thank Dr. Chinatsu Mukai for her friendship, as well as for passing on so much of her sperm capacitation and microscope knowledge. Dr. Atsushi Asano, thank you for all your training. Jacque Nelson-Harrington, you have been my rock during the ups and downs here, both in research and life. Also, to quote James, thank you so much for all the ordering. James Lata and Lauren Wu, as well as Kristen Beck, Jeremy Allen, and Lara Mouttham, thank you for being my graduate school community. Dr. Roy Cohen, I’ll miss your innovative ideas in lab meeting (and delicious desserts). Chip Thompson, glassware is my favorite part of Baker, as all the students I’ve worked with here will attest. Thank you to Sue Williams for answering every random question I’ve had, and for the happy greetings every day. Big thank you’s to Skylar Sylvester for bearing with me on every aspect of the projects here for 3+ years, the dog project would not be where it is today without you, and Zack Dvornicky-Raymond for your assistance and for bringing renewed enthusiasm to routine experiments. Thanks to Gail Huckins, Jennifer Yordy, and Victoria Williams for all your help, especially during chaotic times. To all those who have assisted us with their expertise over the years, including Dr. Vicki Meyers-Wallen for teaching me P a g e | v dog colony management, Dr. Soon Hon Cheong for neonatal dog advice, and Drs. James Flanders and Colleen Lambo for their surgical skills, thank you so much. None of the work at Cornell would have been possible without the animal care staff at the Baker Institute. Jackie Wright, Kevin Draiss, Julie Reynolds and particularly Shannon Kellogg, thank you for taking such wonderful care of the dogs and being so generous with your time to help with various sample collections. No amount of cookies could thank you enough! I am also eternally thankful for the CARE veterinarians - I was definitely not the easiest person to work with, considering the short notice for scheduling spays with the IVF project. Drs. Mary Martin, Bryant Blank, Bhupinder Singh, Todd Pavek, Wendy Williams, Elizabeth Moore, Amy Rizzo, Balu Reddyjarugu, Rohit Jajoria, Kate Breyer, and Beth Noe, I appreciate all your help. And a big thank you to Cherie Brown and Scott Soprano! Luce Guanzini, thank you also for finding lovely homes for our 50+ beagles over the past few years. It is so great to see photos of their smiling faces after they leave us. To my co-workers at SCBI, I first want to thank the incredible research scientists, particularly Dr. David Wildt and Dr. Buddha Pukazhenthi for their advice, encouragement, and guidance over the years. Thanks also to Drs. Janine Brown, Adrienne Crosier, and Pierre Comizzoli. I’d like to extend a huge thanks to my friend Dr. Mayako Fujihara. It has been a joy to learn from you and to work alongside you all these years. My fellow ducklings, Megan Brown, Amy Johnson, Marieke Koester, Stacie Castelda, Lauren Reiter, Gift Thongkittidilok, and Lauren Henson, it has been a pleasure. I’d also like to thank visiting students and interns who have brought such great variety of ideas and interests to the lab: Michelle Brazil Serafim, Tathiana Ferguson Motheo, and Caitlin McDonough. Several veterinary clinics in the Shenandoah Valley and New York were kind enough to donate ovaries from routine ovariohysterectomies to these projects, including Royal Oak Animal Clinic, Cedarville Veterinary Clinic, Warren Country Veterinary Clinic, Newtown Veterinary Clinic, Animal Medical Center of Stephen’s City, Stephen’s City Animal Hospital, and Anicira Veterinary P a g e | vi Center in Virginia, and Shelter Outreach Services in central New York. Special thanks to Jennifer Whittaker at SOS for letting me know whenever it was a good day for ovaries. I would like to thank the friends and family who have been the best support system a graduate student could ask for. Thank you mom, dad, and Erica for putting up with me trying to explain my project woes over the phone. Drs. Jennifer Cassano, Diana Koester, and Judy Fry, as well as Alisa Steinklein and Skylar, you have been the best roommates in the world. Trenton Caudill, I can’t thank you enough for your unfaltering support, and for bearing with so many 3 am checks this year. Finally, thank you to all the dogs out there who contributed their ovaries to this project. It really wouldn’t have been possible without your donations! P a g e | vii TABLE OF CONTENTS Biographical Sketch ................................................................................................................... iii Acknowledgements .................................................................................................................... iv Table of Contents ...................................................................................................................... vii Chapter One: Introduction and Literature
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