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Martins Thesis University of Alberta Satellite Cell Involvement in Activity-Induced Skeletal Muscle Adaptations by Karen Janet Bernice Martins (Nee: Martinuk) A thesis submitted to the Faculty of Graduate Studies and Research in partial fulfillment of the requirements for the degree of Doctor of Philosophy Faculty of Physical Education and Recreation ©Karen Janet Bernice Martins (Nee: Martinuk) Fall 2009 Edmonton, Alberta Permission is hereby granted to the University of Alberta Libraries to reproduce single copies of this thesis and to lend or sell such copies for private, scholarly or scientific research purposes only. Where the thesis is converted to, or otherwise made available in digital form, the University of Alberta will advise potential users of the thesis of these terms. The author reserves all other publication and other rights in association with the copyright in the thesis and, except as herein before provided, neither the thesis nor any substantial portion thereof may be printed or otherwise reproduced in any material form whatsoever without the author's prior written permission. Library and Archives Bibliothèque et Canada Archives Canada Published Heritage Direction du Branch Patrimoine de l’édition 395 Wellington Street 395, rue Wellington Ottawa ON K1A 0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre référence ISBN: 978-0-494-53993-4 Our file Notre référence ISBN: 978-0-494-53993-4 NOTICE: AVIS: The author has granted a non- L’auteur a accordé une licence non exclusive exclusive license allowing Library and permettant à la Bibliothèque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par télécommunication ou par l’Internet, prêter, telecommunication or on the Internet, distribuer et vendre des thèses partout dans le loan, distribute and sell theses monde, à des fins commerciales ou autres, sur worldwide, for commercial or non- support microforme, papier, électronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L’auteur conserve la propriété du droit d’auteur ownership and moral rights in this et des droits moraux qui protège cette thèse. Ni thesis. Neither the thesis nor la thèse ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent être imprimés ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author’s permission. In compliance with the Canadian Conformément à la loi canadienne sur la Privacy Act some supporting forms protection de la vie privée, quelques may have been removed from this formulaires secondaires ont été enlevés de thesis. cette thèse. While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n’y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. Examining Committee Charles Putman, Physical Education and Recreation Walter Dixon, Agricultural, Food and Nutritional Science George Foxcroft, Agricultural, Food and Nutritional Science Daniel Syrotuik, Physical Education and Recreation Karyn Esser, Physiology, University of Kentucky ABSTRACT Skeletal muscle is a heterogeneous, multinucleated, post-mitotic tissue that contains many functionally diverse fibre types that are capable of adjusting their phenotypic properties in response to altered contractile demands. This plasticity, or adaptability of skeletal muscle is largely dictated by variations in motoneuron firing patterns. For example, in response to increased tonic firing of slow motoneurons, which occurs during bouts of endurance training or chronic low-frequency stimulation (CLFS), skeletal muscle adapts by transforming from a faster to a slower phenotypic profile. CLFS is an animal model of endurance training that induces fast-to-slow fibre type transformations in the absence of fibre injury in the rat. The underlying signaling mechanisms regulating this fast-to- slow fibre type transformation, however, remain to be fully elucidated. It has been suggested that myogenic stem cells, termed satellite cells, may regulate and/or facilitate this transformational process. Therefore, the signaling mechanisms involved in CLFS-induced satellite cell activation as well as the role satellite cells may play in CLFS-induced skeletal muscle adaptation were investigated in rat. A pharmacological inhibitor of nitric oxide (NO) synthase, Nω-nitro-L-arginine methyl ester, was used to investigate CLFS-induced satellite cell activation in the absence of endogenous NO production. Results suggest that NO is required for early CLFS-induced satellite cell activation, but a yet-to-be defined pathway exists that is able to fully compensate in the absence of prolonged NO production. A novel method of satellite cell ablation (i.e. weekly focal γ -irradiation application) was used to investigate CLFS-induced skeletal muscle adaptation in the absence of a viable satellite cell population. Myosin heavy chain (MHC), an important structural and regulatory protein component of the contractile apparatus, was used as a cellular marker of the adaptive response to CLFS. It was demonstrated that satellite cell activity may be involved in early fast-to-slow MHC-based transformations to occur at the protein level without delay in the fast fibre population, and may also play an obligatory role in the final transformation from fast type IIA to slow type I fibres. Interestingly, additional results show that NO appears to be a key mediator of MHC isoform gene expression during CLFS-induced fast-to-slow fibre type transformations. ACKNOWLEDGEMENTS I would like to express sincere gratitude to my supervisor, Dr. Charles T. Putman for his exceptional academic mentorship and guidance. I am also truly grateful to my current and former committee members, Dr. Walter Dixon, Dr. George Foxcroft and Dr. Tessa Gordon, for their support and advice. Additionally, I would like to thank Dr. John Dunn for catalyzing the expansion of my academic knowledge. Thank you to Zoltan Kenwall, Dr. Gordon Murdoch, Joan Turchinsky, Neil Tyreman, and particularly Ian MacLean and Jean Pearcy for their gracious assistance, guidance and invaluable technical expertise and support in the laboratory. Of course, I cannot forget the assistance of Mark Burquest, Vanessa Carlson, Carolyn Crowell, Max Levine and Pam McDonald, all of whom spent countless hours in the laboratory and staring into microscopes on my behalf. Many thanks to my fellow colleagues both past and present, Victoria Cook, Dr. Maria Gallo, Dr. Luke Harris and Yang Shu for their practical help, advice and above all else, camaraderie. I would also like to thank the Gang for morning coffee, lab lunches and high-five Fridays, which provided unforgettable memories and much appreciated levity. Numerous friends outside of academia have helped to keep life in perspective for me. Particular thanks to Bobbi Barbarich, Daryl Lehocky and Shane Mortemore. Finally, thank you to my Husband for everything, but especially for teaching me balance, to my loving Mom and Dad for supporting their daughter, the proverbial student, to my Brother who is travelling a similar path, and to my entire family for their unconditional love and encouragement - always. Research support was provided by the Alberta Agricultural Research Institute, the Alberta Heritage Foundation of Medical Research (AHFMR), the Canadian Institutes of Health Research and the Natural Sciences and Engineering Research Council (NSERC). My scholarship funding support was provided by AHFMR, NSERC and the University of Alberta. Cheers to science! TABLE OF CONTENTS CHAPTER ONE: INTRODUCTION................................................................. 1 1.1 INTRODUCTION ....................................................................................... 1 1.2 REFERENCES............................................................................................. 5 CHAPTER TWO: LITERATURE REVIEW.................................................... 6 2.1 ADULT SKELETAL MUSCLE................................................................. 6 2.1.1 Diversity .................................................................................................. 6 2.1.2.1 Chronic Low-Frequency Stimulation................................................ 9 2.2 SATELLITE CELLS................................................................................. 12 2.2.1 Satellite Cell Function.......................................................................... 13 2.2.1.1 Muscle Development....................................................................... 13 2.2.1.2 Stem Cells ....................................................................................... 15 2.2.1.3 Muscle Regeneration ...................................................................... 17 2.2.1.4 Muscle Hypertrophy ....................................................................... 18 2.2.1.5 Fast-to-Slow Fibre Type Transformations ..................................... 21 2.2.2 Satellite Cell Activation ....................................................................... 22 2.2.2.1 Nitric Oxide..................................................................................... 22 2.2.2.2 Hepatocyte Growth Factor ............................................................. 24 2.2.2.3 Nitric Oxide-Dependent Satellite Cell Activation..........................
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