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Advances in the Fundamental Cryobiology of Mammalian Oocytes

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Advances in the Fundamental Cryobiology of Mammalian Oocytes ADVANCES IN THE FUNDAMENTAL CRYOBIOLOGY OF MAMMALIAN OOCYTES A Dissertation presented to the Faculty of the Graduate School at the University of Missouri-Columbia In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy by STEVEN FRANCIS MULLEN Dr. John K. Critser, Dissertation Supervisor MAY 2007 © Copyright by Steven Francis Mullen 2007 All Rights Reserved The undersigned, appointed by the dean of the Graduate School, have examined the dissertation entitled ADVANCES IN THE FUNDAMENTAL CRYOBIOLOGY OF MAMMALIAN OOCYTES presented by Steven Francis Mullen, a candidate for the degree of doctor of philosophy, and hereby certify that, in their opinion, it is worthy of acceptance. Professor John K. Critser Professor Yuksel Agca Professor Heide Schatten Professor Randall Prather Professor Edmund Rucker III My parents more than anyone else are responsible for who I have become. I would like to dedicate this work to my Mother Kathleen Marie (Bird) Mullen and my Father Timothy Jerome Mullen. ACKNOWLEDGEMENTS The work presented in this dissertation could not have been completed without the assistance and dedication of numerous individuals. First and foremost, I would like to thank Dr. John K. Critser for all of his support, kindness, understanding, and patience over the past 7 years. During this time John has taught me many things in relation to both science and life. He encouraged me in my pursuit of ideas, supported me in times of need and worry, and provided me with numerous opportunities that few individuals in my position are given. Equally important, John has taught me the true meaning of the word gentleman. John has helped me become the man I have always wanted to be. Dr. Yuksel Agca has been a great colleague, mentor, and friend during this time. I am particularly indebted to Yuksel for all of the practical laboratory skills he taught me during my first year as a student. I will cherish his friendship for my remaining days. Drs. Heide Schatten, Randall Prather, and Edmund Rucker III have become trusted colleagues and mentors. Dr. Schatten has encouraged me at every step of this process, provided me with valuable advice, and is always complimentary. Dr. Prather has been an influential outside advisor and I have come to better ii appreciate his role in this process. Dr. Rucker has always been available for consultation and advice. His presence at MU is missed. I would like to acknowledge Dr. Augustine Peter, professor and veterinary doctor at Purdue University. While Dr. Peter is no longer directly involved with my education, he was a cherished mentor and friend during my first 1.5 years as a student while studying at Purdue University. Augustine is also a true gentleman. He was extremely supportive and encouraging during those days, and his help in getting me started on this journey will always be remembered. I have encountered hundreds of wonderful people over the past years who provided me strength, companionship, encouragement, humility, and humor. I am particularly appreciative of all of those with whom I have worked directly and assisted me with the work presented here. I will apologize in advance for those who are not directly named. Labmates — I have had the pleasure of working with some of the kindest, funniest, and most respectable people I have ever encountered. They include: Sara Brown, Jun Liu, Erik Woods, Tracy Johnson, Mark Starr, Jenn Cornelius- Green, Janelle Lawrence, Hongsheng Men, Eric Walters, Lei Lei, Si Wei, Aric Krogstad, James Benson, Corinna Kashuba-Benson, Xu Han, Zeng Rong, Chongbei Zhao, Natalia Karasseva, Seth Schumacher, Aaron Buck, Andrea Sommer, Antonio Chaveiro (visiting student, The Netherlands). Special thanks iii goes to Mika Katayama for all of her support and encouragement during the later days. Fellow Students (non-Graduate) – I had the pleasure of mentoring 2 undergraduate students who participated in the Research in Engineering for Undergraduates program sponsored by the NSF. I would like to thank Alan Young and Amanda Corey for their dedication to the projects on which we worked during their time in our lab. I also had the pleasure of working with Matt Rosenbaum, who was at MU as a summer veterinary resident research fellow. Matt’s dedication is evident by his co-authorship on the manuscript that composes Chapter 5 of this dissertation. Juri Ota, an MS student and veterinary opthamology resident, has become a dear friend and colleague. Several veterinary students have become my friends and colleagues, and I would specifically like to acknowledge Anna Bruening, Michelle Belviy, Megan Baebler, Krissy Bussmann, Jessica Michel, Lindsey Vansandt, and Luise King for their friendship. Na Yang, Amber Taufen, and Rebecca Rivas were undergraduate students who became my friends during my time as a graduate student and I appreciate them for this. Graduate Students — Deborah Nell Shelley, Dongyan Feng, Gabe Hosu, Mami Iramajiri, Scott Rector, Jessica Taylor, Tiffany Romain, Yi Zhuang, Cindy Bracken, Denise Bouvrette, Ferril Rose, Liliana Salinas-Flores, Lin Zhang, iv Sriganesh Talatam, and Kristin Whitworth are just a few of the Graduate Students who have befriended me during this time. James Orr (University of Kansas) and Holly Bender (Iowa State University) were my two off-campus faculty mentors while I was a fellow in the Preparing Future Faculty program, and their time and attention during my visit to their campus is sincerely appreciated. Faculty and Research Fellows – I have had the distinct pleasure of interacting with numerous excellent professors at Purdue, MU, and other universities. I would like to thank the following individuals for their support and encouragement: Lela Riley, Robert Livingston, Earl Steffen, Elizabeth Bryda, Cindy Besch- Williford, Craig Franklin, Beth Bauer, Timothy Evans, Elizabeth Giuliano, Elizabeth Critser, James Graham, Teresa Woodruff, Serean Adams, Zi-Jiang Chen, Li Yuan, Li Mei, Peter Sutovsky, John Green, James Schadt, Eileen Hasser, Marc Hamilton, Mark Ellersieck, Gary Solbrekken, Gabor Forgacs, Catherine Vogelweid, Gary Johnson, Pam Benoit, Ibitola Pearce, and Barbara Townsend. Venkataseshu Ganjam and Matt Lucy are two faculty members outside of our department that I would like to specifically acknowledge for the generous support and assistance they have given me over the past several years. v Staff – None of this work could have been completed without the diligence and kindness of staff members of the various institutions of which I have been affiliated. I would like to thank Laura Oxford for everything she did for me while I was at Purdue. Rose Mayfield has gone out of her way so many times for me, that I have lost count. Patricia Parry has been most generous with her time and friendship. Anne Chegwidden and Darlene Ward from the Veterinary Pathobiology office, and Nancy Wawrzyniak from the Dean’s office have been so very kind and helpful to me, and are three of the nicest ladies I know. Laura Buck, Ed Parker, and Trenton Boyd from the Veterinary Medicine Library have assisted me greatly during the years, and their time and effort is greatly appreciated. Don Conner and Howard Wilson have provided excellent artistic services for me and their contribution to my work is appreciated. Collaborators – Members of the Atlanta Center for Reproductive Medicine, and in particular, Chad Johnson, Claudia Jenkins, and Dianne (Broermann) Hurney are graciously acknowledged for their assistance and support on our collaborative project, the results of which are described in Chapter 3. I would like to thank all of the members of the Reproductive Medical Center of Shandong Provincial Hospital, Shandong University, for their hospitality and friendship during my time in Jinan, China. The assistance of the following individuals on the project undertaken at that time, the results of which are described in Chapter 6: Jing-Mei Hu, Shui-Ying Ma, Shan Liu, Na Zhang, Hui-Jun vi Yang, and Wan-Xia Zhong. Special thanks go to Jun-Hao Yan and Wang Lihong. I would particularly like to thank Li Mei and Li Yuan for everything they did to make that project a success, and Chen Xin for her friendship and assistance with English translation. Most importantly, I would like to thank Zi-Jiang Chen for her wonderful hospitality and support for that project. My trip to China is one of the most memorable experiences of my life. vii TABLE OF CONTENTS ACKNOWLEDGEMENTS………………………………………………………………ii LIST OF ILLUSTRATIONS ………………..………………………………………....xv LIST OF TABLES…………………………………………………………………….xviii ABSTRACT…………………………………………………………………….………xix Chapter 1. INTRODUCTION…………………………………………………..1 Outline of the Study……………………………………………………..1 The Science of Cryobiology……………………………………………2 Introduction………………………………………………………2 Anatomy of Cryopreservation………………………………….3 The Effects of Water Precipitation (as ice) During Cooling…4 Ice Nucleation, Crystallization, Vitrification, and Devitrification………………………………………………...4 Solute Concentration as a Result of Ice Crystallization, the Associated Osmotic Effects, and Cell Death at Supra- optimal Cooling Rates………...…………………………….8 Cell Death at Sub-optimal Cooling Rates and the Role of Cryoprotectants in Mitigating Cell Damage……………..16 Cryoprotectants: Beneficial Effects…………………………..18 Cryoprotectants: Detrimental Effects………………………..24 Cell Death at Sub-optimal Cooling Rates (continued)….....31 Chilling Injury / Cold Shock…………………..………………36 Vitrification as an Alternative to Equilibrium Freezing……..40 Mammalian Oocyte Development: General and Comparative Aspects……………………………………………………………44
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