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The Parvovirus Minute Virus of Mice Modulates the Dna Damage Response

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The Parvovirus Minute Virus of Mice Modulates the Dna Damage Response THE PARVOVIRUS MINUTE VIRUS OF MICE MODULATES THE DNA DAMAGE RESPONSE TO FACILITATE VIRAL REPLICATION AND A PRE-MITOTIC CELL CYCLE BLOCK A Dissertation Presented to The Faculty of the Graduate School At the University of Missouri In Partial Fulfillment Of the Requirements for the Degree Doctor of Philosophy By MATTHEW S. FULLER David J. Pintel, Dissertation Supervisor May 2017 The undersigned, appointed by the dean of the Graduate School, have examined the Dissertation entitled THE PARVOVIRUS MINUTE VIRUS OF MICE MODULATES THE DNA DAMAGE RESPONSE TO FACILITATE VIRAL REPLICATION AND A PRE-MITOTIC CELL CYCLE BLOCK Presented by Matthew S. Fuller A candidate for the degree of Doctor of Philosophy And hereby certify that, in their opinion, it is worthy of acceptance. Dr. David J. Pintel Dr. Dongsheng Duan Dr. Mark Hannink Dr. Christian Lorson Dr. Stefanos Sarafianos ACKNOWLEDGEMENTS First and foremost I would like to thank David Pintel for graciously accepting me into his laboratory and patiently mentoring me for nearly six years. Hands down, without question, the single best choice I made during my entire tenure in graduate school occurred early on, when I decided to join your lab. Your patience and understanding afforded me the freedom to make and learn from my, at times quite plentiful, mistakes and to gain the confidence needed to become an independent thinker and scientist. Although demanding, and at times exceptionally challenging, your persistence and insistence of adhering to the highest standards of scientific rigor and intellectual discourse allows each of us to stand out in the scientific community and generate exceptional work and ideas. With your guidance, every member of your lab generates work that we can all be proud of. As I continue my journey into science, I will strive to always to hold myself to the same standards you would, for then I know I will be the type of thoughtful, exceptional scientist that you are. It has been my honor to work with you these past 6 years. Thank you. I would also like to thank each member of my dissertation committee: Dr. Dongsheng Duan, Dr. Mark Hannink, Dr. Chris Lorson and Dr. Stefan Sarafianos for helpful suggestions, support and kindness during this time. Each of you was always willing to listen and help when I needed it and always treated me with such kindness and respect. For that I am very grateful. I am also very grateful to Pintel Lab members, past and present, for providing camaraderie and support over the years. I would like to thank Loretta, Venkatesh, Rick, ii Lisa, Richard and Femi for welcoming me into the lab and helping me start off on the right foot. I would like to thank Yanming and Igor for their contributions to the lab and their friendship. Specifically, I would like to thank Richard for collaborating with me during my first few years and patiently helping me learn to do experiments the right way. I would also like to thank Femi for being a great lab mate and friend. I enjoyed being able to discuss politics and our science with you, traveling to conferences and just spending time hanging out in the lab. With the exception of Dave, you taught me more about how to execute and communicate great science than anyone else and for that I am truly grateful. I would like to thank Kinjal for pushing the boundaries of what I was capable of doing and thinking about in science. Your patient help with “new” techniques was absolutely critical for allowing me to reach my final destination. I am also thankful for your immediate friendship and fine appreciation of music from a certain animated household gentleman. Finally, I would like to thank Lisa for everything that you did for me and that you continue to do for members of our lab. Your kindness and patience are appreciated by each and every one of us who have had the fortune to work with you in this lab. Each time you were willing to harvest or add something to my cells was precious time you gave me to spend with my girls. Thank you. I would like to thank our friends from our pre-graduate school life that stuck with us and reminded us that there was a world outside of the walls of the LSC and lab 411. Matt Jones, Brittany and Lance Lines, and Erin Heitman: thank you for everything over the years. You all helped us remain sane during particularly difficult times. I would also like to thank my new friends in the LSC: Obi, Mary, Andrew, Kevin, Dandan, Kyle and iii Carolina, for immense help and laughter over the years. And thanks to the Hannink, Johnson, Lorson and Sarafianos labs for help with ideas, reagents and equipment over the years. I would like to thank my parents, John and Melinda Fuller, for fostering, at a very early age, the desire to learn and the resources to do so. You both instilled in me the importance of a strong work ethic, which perhaps I take overboard at times, but has been essential in my journey to here. Even though we didn’t have a lot at times, you always made sure I had what I needed to excel at whatever I was doing. I would not be where I am without you. I would also like to thank my brothers John Jr. (JJ) and Michael Fuller for camaraderie and laughs over the years. And specifically to JJ for helping me and my family at some of our most difficult points. I would also like to thank my in-laws: Rick, Debbie, Chip and Jacquie. Rick and Debbie, you have been unbelievably supportive in innumerable ways. You have made this difficult journey much easier. Rick, thank you for teaching me, with an incredible amount of patience, how to fix cars and appliances and undertake household repairs. Debbie, thank you for always being willing to drive to Columbia to help Cathy with work and enabling us to do things with our children. Chip and Jacquie, thank you for all the support over the years. The most important people I must thank are my girls, who patiently await my late arrival every night. To Talitha, my first born, who has unwearyingly traveled to the lab countless times, missed me at meals and late nights of work, and grown up thinking all dads go to work seven days a week, thank you for being patient with me during this iv time. And thank you for being such an intelligent, thoughtful young girl. You have made this process so much more enjoyable and continue to give me motivation during tough times. To Hazel, you brighten even the darkest days by meeting me at the door every night with a grin and a toy. Thank you for being so sweet and innocent. And finally, to my strong, beautiful and unwaveringly supportive wife, Cathy, thank you for everything you have done for me and our family during this time. I couldn’t have undertaken this journey if you hadn’t supported my poorly timed decision to leave a good job while we had an infant. Your support and absolute belief in my abilities has given me the strength I needed to succeed. This simply would not have been possible without you. And finally, I would like to thank God, for creating a universe filled with such inherent beauty that we cannot help but investigate the mysteries held within. v TABLE OF CONTENTS Acknowledgements …………………………………………………………………………………………………….…ii Table of Figures …………………………………………………………………………………………………………..viii Abstract …………………………………………………………………………………………………………………………x 1 Introduction …………………………………………………………………………………………………………1 1.1 Parvoviruses ..………………………………………………………………………………………………………1 1.2 Minute virus of mice …………………………………………………………………………………………...9 1.3 DNA Damage and repair …………………………………………………………………………………...23 1.4 Parvoviruses and the DNA damage response ………………………………………………….…43 1.5 Cell cycle control and regulation ……………………………………………………………………....53 2 Efficient parvovirus replication requires CRL4Cdt2-targeted depletion of p21 to prevent its inhibitory interaction with PCNA 2.1 Introduction ………………………………………………………………………………………………….…74 2.2 Results ………………………………………………………………………………………………………….….76 2.3 Discussion ………………………………………………………………………………………………………..93 2.4 Materials and Methods ……………………………………………………………………………………97 2.5 Supporting Information ………………………………………………………………………………….101 3 Minute virus of mice inhibits transcription of the cyclin B1 gene during infection 3.1 Introduction …………………………………………………………………………………………………..114 3.2 Materials and Methods ………………………………………………………………………………….117 3.3 Results ……………………………………………………………………………………………………………121 3.4 Discussion ………………………………………………………………………………………………………138 vi 3.5 Supplemental Material …………………………………………………………………………………..142 4 Minute virus of mice relocalizes the RNA-binding protein HuR during infection 4.1 Introduction …………………………………………………………………………………………………..148 4.2 Materials and Methods ………………………………………………………………………………….151 4.3 Results ……………………………………………………………………………………………………………155 4.4 Discussion ………………………………………………………………………………………………………171 5 Overall summary ……………………………………………………………………………………………..175 Bibliography ………………………………………………………………………………………………………………178 Vita ……………………………………………………………………………………………………………………………210 vii TABLE OF FIGURES Figure 1-1: Phylogenetic tree of the genera within the Family Parvoviridae ……….…………3 Figure 1-2: Rolling Hairpin Replication …………………………………………………………………………..6 Figure 1-3: Transcriptional Map of MVM ……………………………………………………………………..11 Figure 1-4: Functional domains of MVM NS1 and NS2 …………………………………………………18 Figure 1-5: General overview of DNA damage, DDR signaling and potential outcomes .25 Figure 1-6: Schematic of double-stranded break repair and repair of single-stranded DNA after processed DSB …………………………………………………………………………………29 Figure 1-7: – Summary of viral interactions with the DDR ……………………………………………36 Figure
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