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Proquest Dissertations The Impact of Stretch, Exercise and Drug Treatments on Structure, Function and Satellite Cell Activation in Aging Muscle by Jeffrey Robert Scott Leiter MSc A Thesis submitted to the Faculty of Graduate Studies of The University of Manitoba in partial fulfilment of the requirements of the degree of DOCTOR OF PHILOSOPHY (PhD) Department of Human Anatomy and Cell Science University of Manitoba Winnipeg, Manitoba COPYRIGHT © 2009 Library and Archives Bibliothdque et 1*1 Canada Archives Canada Published Heritage Direction du Branch Patrimoine de l'6dition 395 Wellington Street 395, rue Wellington Ottawa ON K1A0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votm reference ISBN: 978-0-494-64257-3 Our file Notre r6f6rence ISBN: 978-0-494-64257-3 NOTICE: AVIS: The author has granted a non- L'auteur a accorde une licence non exclusive exclusive license allowing Library and permettant a la Bibliothdque 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 telecommunication ou par Nnternet, preter, telecommunication or on the Internet, distribuer et vendre des theses partout dans le loan, distribute and sell theses monde, a des fins commerciales ou autres, sur worldwide, for commercial or non- support microforme, papier, electronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L'auteur conserve la propriete du droit d'auteur ownership and moral rights in this et des droits moraux qui protege cette these. Ni thesis. Neither the thesis nor la these ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent etre imprimes ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author's permission. In compliance with the Canadian Conformement a la loi canadienne sur la Privacy Act some supporting forms protection de la vie privee, quelques may have been removed from this formulaires secondaires ont ete enleves de thesis. cette these. 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. Canada THE UNIVERSITY OF MANITOBA FACULTY OF GRADUATE STUDIES COPYRIGHT PERMISSION The Impact of Stretch, Exercise and Drug Treatments on Structure, Function and Satellite Cell Activation in Aging Muscle BY Jeffrey Robert Scott Leiter A Thesis/Practicum submitted to the Faculty of Graduate Studies of The University of Manitoba in partial fulfillment of the requirement of the degree Of Doctor of Philosophy Jeffrey Robert Scott Leiter © 2009 Permission has been granted to the University of Manitoba Libraries to lend a copy of this thesis/practicum, to Library and Archives Canada (LAC) to lend a copy of this thesis/practicum, and to LAC's agent (UMI/ProQuest) to microfilm, sell copies and to publish an abstract of this thesis/practicum. This reproduction or copy of this thesis has been made available by authority of the copyright owner solely for the purpose of private study and research, and may only be reproduced and copied as permitted by copyright laws or with express written authorization from the copyright owner. TABLE OF CONTENTS ABSTRACT VII ACKNOWLEDGEMENTS IX List of Tables XI List of Figures XII CHAPTER 1 . INTRODUCTION 1 CHAPTER 2 . REVIEW OF LITERATURE 7 2.1 Skeletal Muscle 7 2.1a Structure 7 2.1b Function 13 2.1c Types of Contraction 23 2.Id Fiber Types 25 2.1e Fiber type transformation with loading and unloading 31 2. If Muscle Damage and Necrosis 34 2.1g Muscle Tissue Repair 35 2.1h Mechanisms of muscle hypertrophy 37 2.1i Atrophy and models of muscle atrophy 40 2.2 Satellite cells 43 2.2a Location 44 2.2b Satellite cell activation 45 2.2c Proliferation 46 2.2d Differentiation 47 2.2e Markers 49 I 2.2f Activation Stimuli 52 2.2g Activation Pathways 55 2.2h Changes with aging 57 2.3 Nitric Oxide 63 2.3a Nitric Oxide Synthase 64 2.3b NOS and stretch 66 2.3c NOS and exercise 67 2.4 Pharmacological Manipulation of Nitric Oxide 69 2.4a Nitric Oxide Donors 69 2.4b Nitric Oxide Synthase Inhibitors 71 2.5 Functional Measures 73 2.5a Voluntary wheel running 74 2.5b Treadmill Running 75 2.5c Grip Strength 76 2.6 Changes in Skeletal Muscle with Aging 78 2.6a Structural Changes 84 2.6b Functional Changes 86 2.6c Neuromuscular system 89 2.6d Cellular Changes 91 2.6e Age-related Sarcopenia 94 2.7. Significance 97 2.8. Tables and Figures 100 CHAPTER 3 . HYPOTHESIS AND AIMS 102 II 3.1. Hypothesis 102 3.2 Specific Aims: 102 CHAPTER 4 . THE EFFECTS OF AGE AND DRUG TREATMENTS ON SATELLITE CELL ACTIVATION IN CULTURED EDL MUSCLES OF NORMAL FEMALE MICE 104 4.1 Introduction 104 4.2 Methods 106 4.2a Experimental animals 106 4.2b Muscle isolation and pinning 107 4.2c Drug treatments 108 4.2d Stretching of EDL muscles 109 4.2e Tissue homogenization and DNA assay 110 4.2e. Statistical analysis Ill 4.3 Results Ill 4.3a Effects of age on satellite cell activation Ill 4.3b Stretch-activation of satellite cells Ill 4.3c Drug Treatments 112 4.4 Discussion 113 4.5 Tables and Figures 118 CHAPTER 5 . AGE-RELATED CHANGES IN STRUCTURE, FUNCTION, GENE EXPRESSION AND SATELLITE CELL ACTIVATION 125 5.1 Introduction 125 5.2 Methods 126 III 5.2a Animals 126 5.2b Body Mass 127 5.2c Grip Strength 127 5.2d Muscle Isolation 128 5.2e Muscle Fiber CSA 129 5. If In Situ Hybridization 129 5.2 g Westerns Blotting Experiments for NOS-I, myostatin, and Myf5 130 5.2h Data Analysis 132 5.3 Results 133 5.3a Body Mass 133 5.3b Muscle Mass 133 5.3c Grip Strength 133 5.3d Muscle Fiber CSA 134 5.3e Number and distribution of Satellite Cells 135 5.3f Satellite Cell Activation 135 5.3g NOS-I, myostatin, and Myf5 Protein Content 136 5.4 Discussion 136 5.5 Tables and Figures 142 CHAPTER 6 . MUSCLE-SPECIFIC CHANGES IN SATELLITE CELL ACTIVATION AND GENE EXPRESSION AFTER VOLUNTARY WHEEL RUNNING IN NORMAL ADULT MICE 150 6.1 Introduction 150 6.2 Materials 152 IV 6.2a Animals and Exercise 152 6.2b Training Schedule 153 6.2c Voluntary Exercise 153 6.2d Grip Strength 154 6.2e Tissue Collection 155 6.2f Muscle Cross Sectional Area 155 6.2g Satellite Cell Activation 156 6.2h Western Blot analysis for NOS-I, MyoD and myostatin 157 6.2i Data Analysis 158 6.3 Results 158 6.3a Body Mass 158 6.3b Voluntary Exercise 159 6.3c Grip Strength 159 6.3d Muscle Fiber Cross Sectional Area 160 6.3e Satellite Cell Activation 160 6.3f NOS-I 161 6.3g MyoD 161 6.3h Myostatin 162 6.4 Discussion 162 CHAPTER 7 . DISCUSSION 179 7.1 Mechanical and chemical activation of satellite cells is perturbed in skeletal muscle from normal aged mice 179 7.2 Changes in the structure and function of normal skeletal muscle with age 182 V 7.3 Exercise-induced satellite cell activation, NOS-I expression, and myostatin regulation are muscle-dependent and age-specific 184 7.4 Limitations and strengths 190 7.4a Limitations 190 7.4b Strengths 192 7.5 Conclusion 194 7.6 Future Directions 208 CHAPTER 8 . REFERENCES 213 VI ABSTRACT Age-related muscle atrophy and the importance of satellite cells in muscle maintenance, growth and repair led us to examine the effects of mechanical stretch, nitric oxide (NO), and age on satellite cell (SC) activation and gene expression in normal young and old mice. Baseline variables (body mass, muscle mass, fiber cross-sectional area (CSA), muscle strength, SC population, stretch activation and gene expression) were obtained from normal C57BL/6 mice at 3-, 8-, 12- and 18-months-of-age. Activation was assayed by 3H-thymidine incorporation into extensor digitorum longus (EDL) muscles isolated for culture. In a second experiment, muscle from 8- and 18-month-old mice was treated with one or more of: stretch; NO-donors (L-Arginine (LA), isosorbide dinitrate (ISDN)) and; N0)-nitro-L-Arginine methyl ester (LN). EDL muscles from 6-month-old mice required a greater stretch stimulus (20% vs. 10% length increase) than EDL from younger mice to increase SC activation. Stretch did not increase SC activation in mice older than 6 months-of-age. NO supplementation from an exogenous source (ISDN) increased SC activation by stretch in 8- but not 18-mo-old EDLs. In a third experiment, 8- and 18-month-old mice were subjected to 3 weeks of voluntary wheel running, or not. The EDL, tibialis anterior (TA), gastrocnemius (GAST) and quadriceps (QUAD) muscles were selected for analysis following sacrifice. The QUAD muscle from 8-month-old mice was the only muscle that demonstrated an exercise-induced increase in SC activation, elevated expression of neuronal nitric oxide synthase (NOS-I) and downregulation of myostatin, a gene that inhibits muscle growth. These results suggest mechanical stimulation of satellite cells and regulation of gene expression that controls muscle growth in voluntary contractile tissue is muscle-specific and age-dependent. VII Perturbed sensitivity to mechanical stimulation and NO in muscle from 18-mo-old mice, in culture and in vivo, may partly explain loss of muscle mass, fiber CSA, relative grip strength and SC pool size with age. Similar to dystrophic muscle, a disrupted dystrophin- glycoprotein complex and subsequent alteration in NO availability may affect the ability of native satellite cells to maintain or effectively regenerate aged muscle.
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