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Downloaded April 2015 For Distribution Agreement In presenting this thesis or dissertation as a partial fulfillment of the requirements for an advanced degree from Emory University, I hereby grant to Emory University and its agents the non-exclusive license to archive, make accessible, and display my thesis or dissertation in whole or in part in all forms of media, now or hereafter known, including display on the world wide web. I understand that I may select some access restrictions as part of the online submission of this thesis or dissertation. I retain all ownership rights to the copyright of the thesis or dissertation. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. Signature: _____________________________ ______________ Alicia Ann Cutler Date Analyses of aging and heterogeneity in nuclei of multinucleated skeletal muscle cells By Alicia Ann Cutler Doctor of Philosophy Graduate Division of Biological and Biomedical Science Biochemistry, Cell, and Developmental Biology ________________________________ ______________________________ Anita H. Corbett, Ph.D. Grace K. Pavlath, Ph.D. Advisor Advisor ________________________________ ______________________________ Winfield S. Sale, Ph.D. Maureen A. Powers, Ph.D. Committee Member Committee Member ________________________________ ______________________________ James Q. Zheng, Ph.D. Nicholas T. Seyfried, Ph.D. Committee Member Committee Member Accepted: _________________________________________ Lisa A. Tedesco, Ph.D. Dean of the James T. Laney School of Graduate Studies ___________________ Date Analyses of aging and heterogeneity in nuclei of multinucleated skeletal muscle cells By Alicia Cutler B. S. Brigham Young University, 2012 Advisors: Anita Corbett, Ph.D. and Grace Pavlath, Ph.D. An Abstract of A dissertation submitted to the Faculty of the James T. Laney School of Graduate Studies of Emory University In partial fulfillment of the requirements for the degree of Doctor of Philosophy In Biochemistry Cell and Developmental Biology 2017 Abstract Analyses of aging and heterogeneity in nuclei of multinucleated skeletal muscle cells By Alicia Cutler The primary cell type of skeletal muscle is the myofiber. Myofibers are multinucleated containing thousands of nuclei all sharing a single, common cytoplasm. Despite all nuclei sharing the same cytoplasm, individual nuclei differ in key characteristics. Although the nucleus is the major site of gene regulation, the muscle nucleus has been underexamined because of technical limitations including contamination with non-myofiber derived nuclei and inability to selectively analyze individual nuclei. In this dissertation, we overcome these difficulties and demonstrate that nuclei in a single myofiber differ in nuclear import as a potential mechanism for achieving variation in nuclear content and function among nuclei in a single cell. We also present an approach to selectively isolate myonuclei, the first detailed myonuclear proteome, and changes that occur in the myonuclear proteome with aging. This work reinforces the significance of variation among myonuclei and emphasizes the importance of examining nuclear activity on the level of individual nuclei. Additionally, we show that we have developed the technical approach needed to pursue myonuclear-specific studies. Together our findings lay the foundation for careful examination of the myonuclear proteome, transcriptome, and epigenome in response to muscle growth, regeneration, exercise, and disease. Analyses of aging and heterogeneity in nuclei of multinucleated skeletal muscle cells By Alicia A Cutler B.S., Brigham Young University, 2012 Advisors: Anita Corbett, Ph.D. and Grace Pavlath, Ph.D. A dissertation submitted to the Faculty of the James T. Laney School of Graduate Studies of Emory University In partial fulfillment of the requirements for the degree of Doctor of Philosophy In Biochemistry Cell and Developmental Biology 2017 Acknowledgements I gratefully acknowledge my two wonderful mentors: Grace Pavlath and Anita Corbett. Grace is an incredible role model with her unwavering professionalism, remarkable efficiency, and unfailing optimism. After meeting with her I always felt like I knew what the next step was and was excited to do it. Her faith in and optimistic support of my career has made all the difference in the course I have taken. Anita is a remarkable example of dedicated service to important causes in science; she readily makes room among her many time commitments and responsibilities for those things she cares deeply about. I am thankful for her investment in my development as a scientist. I was fortunate to have a dedicated thesis committee who provided valuable insights into the logic of my project and technical expertise that solved so many of my problems. Collaboration with them enabled me to develop specialized expertise that would otherwise have been infeasible. The friendship and comradery of my lab mates made coming to work a joy. I am profoundly grateful for their support and problem-solving insights during stressful times and for being the inspiration for some particularly brilliant musical parodies. I appreciate the example of my classmates; together we pushed each other to excellence. The support of my friends helped keep me sane and was a valuable reserve of knowledge on statistics, computer programming, and edible plants. Finally, I am grateful to my family for their support and encouragement. In particular, my parents, who instilled me with a love of science and a passion for learning, my inspirational Grandmother, my brother Chris, who was always available to bounce ideas off and lend a hand, and my sister Sarah for reading and correcting my papers. I thank the many people who contributed to my success. Table of Contents Chapter 1: Background and Significance ............................................................................1 Introduction ..................................................................................................................... 2 1.1 Skeletal muscle .......................................................................................................... 3 1.1.1 Myogenesis ......................................................................................................... 4 1.1.2 Aging Muscle ..................................................................................................... 6 1.2 Nucleocytoplasmic transport ..................................................................................... 8 1.2.1 Nuclear envelope ................................................................................................ 9 1.2.2 Nuclear pore complex ....................................................................................... 11 1.2.3 Nuclear transport receptors ............................................................................... 17 1.3 Multinucleated cells ................................................................................................ 20 1.3.1 Multinucleated single-celled organisms ........................................................... 21 1.3.2 Multinucleated cells in multicellular organisms ............................................... 23 1.4 Summary ................................................................................................................. 30 1.5 Figures ..................................................................................................................... 33 Chapter 2: Non-equivalence of nuclear import among nuclei in multinucleated skeletal muscle cells ........................................................................................................................38 2.1 Summary ................................................................................................................. 39 2.2 Introduction ............................................................................................................. 40 2.3 Results ..................................................................................................................... 44 2.3.1 Nuclear import varies among nuclei within single cultured multinucleated myotubes .................................................................................................................... 44 2.3.2 Independence of nuclear import pathways in cultured myotubes .................... 48 2.3.3 Variation in cNLS import among myofiber nuclei in situ ................................ 51 2.3.4 Nuclear import varies with muscle differentiation ........................................... 54 2.4 Discussion ............................................................................................................... 55 2.5 Methods ................................................................................................................... 66 2.6 Tables ...................................................................................................................... 75 2.7 Figures ..................................................................................................................... 76 Chapter 3: Biochemical isolation of myonuclei employed to define changes to the myonuclear proteome that occur with aging ......................................................................92 3.1 Summary ................................................................................................................. 93 3.2 Introduction ............................................................................................................
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