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An Investigation of the Stem Cell Potential of Skeletal Muscle Satellite Cells

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An Investigation of the Stem Cell Potential of Skeletal Muscle Satellite Cells An investigation of the stem cell potential of skeletal muscle satellite cells Charlotte Anne Collins Eastman Dental Institute University College London A thesis submitted to the University of London in fulfilment of the requirements for the degree of Doctor of Philosophy September 2004 UMI Number: U602529 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. Dissertation Publishing UMI U602529 Published by ProQuest LLC 2014. Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 Abstract Satellite cells are defined by their position beneath the basal lamina of myofibres, and are a source of new myonuclei in adult skeletal muscles. However, other phenotypes also contribute to muscle regeneration, and the relative importance of satellite cells is not known. This work aimed to analyse the stem cell potential of,satellite cells by formally investigating their contribution to muscle regeneration. Myofibres isolated from extensor digitorum longus, soleus, and tibialis anterior muscles were found to have respective means of 7, 22 and 10 associated satellite cells. When a single myofibre was grafted into an irradiated dystrophic mouse muscle, the associated satellite cells underwent extensive, stem cell-like proliferation, generating progeny which sometimes gave rise to a cluster of more than 100 new myofibres. Cluster size varied according to the muscle group from which the graft was derived, but was not proportional to satellite cell number. Primary myoblasts derived from equivalent muscle groups did not undergo such extensive proliferation, or show inter­ muscle variability, suggesting that stem cell activity is critically dependent on a component of the satellite cell niche. Single myofibres isolated from irradiated muscles were non-myogenic after grafting. Satellite cells associated with single myofibres were found to generate new satellite cells in engrafted muscles, demonstrating that satellite cell compartment is maintained by self-renewal. When single myofibre-engrafted muscles were damaged with myotoxin, graft-derived cells underwent rapid clonal expansion to regenerate compact clusters of donor- derived myofibres. The percentage of engrafted muscles containing identifiable donor-derived nuclei was increased after damage, showing that previously inactive cells had been recruited into an active myogenic program. Without experimentally- induced damage, frequency of muscle formation and cluster size were spontaneously augmented over time. These findings demonstrate that satellite cells have several stem cell-like qualities, and thus constitute a self-sufficient and sustainable source of regeneration in adult muscles. 2 Contents Title page 1 Abstract 2 Contents 3 List of figures 9 List of tables 14 List of abbreviations 16 Acknowledgements 20 Chapter 1: Introduction 1.1 General introduction 21 1.2 Structure and origin of skeletal muscle 23 1.21 The anatomy of adult skeletal muscle 23 1.22 Myofibres as syncitia 24 1.23 The developmental origin of skeletal muscle 25 1.24 Expression of MyHC isoforms in developing and adult muscles 28 1.3 Adult stem cells 30 1.31 Definition of a stem cell 30 1.32 Stem cells of adult tissues 30 1.33 Adult stem cell metaplasia 35 1.4 Regeneration of adult skeletal muscle 38 1.41 Evidence for the regenerative ability of adult muscle 38 1.42 The role of satellite cells in muscle regeneration 40 1.43 Evidence for resident MPC outside the satellite cell niche 44 1.44 The contribution of circulatory cells to adult muscle 46 1.45 The origin of postnatally-renewed satellite cells 48 1.5 Skeletal muscle myopathy 54 1.51 Myopathies involving the dystrophin-glycoprotein complex 54 1.52 DMD 56 1.53 Animal models of DMD 56 3 Myoblast transfer therapy 61 Gene therapy of DMD 64 Myotoxic agents 65 Use of myotoxic agents in the study of muscle regeneration 65 Notexin 66 Cardiotoxin 67 Bupivacaine 67 Barium chloride 68 Aims of study 69 Chapter 2: Materials and Methods Mouse strains 71 C57 Bl/lOScSn (C57 Bl/10) mouse 71 C57 Bl/lOScSn-mdjc nu/nu (mdx-nude) mouse 71 3F-nLacZ-2E transgenic mouse 71 Myf5nLacZ/+ mouse 72 Pax3GFP/+ mouse 72 //-2^-tsA58 mouse 72 Muscle cell culture protocols 73 Isolation and culture of single myofibres 73 Isolation and culture of primary myoblasts 76 Culture of conditionally immortal myoblast cell lines 77 Induction of differentiation 78 Cryopreservation of cells 79 Viral infection of cell cultures 79 LNPOZ retroviral vector 79 Infection of satellite-derived cells with LNPOZ retroviral vector 80 GFP lentiviral vector 81 Infection of isolated myofibres with GFP lentiviral vector 82 Assays of cell behaviour 83 BrdU assay for DNA synthesis 83 Myoblast differentiation assay (fusion index) 83 4 2.5 Animal protocols 83 2.51 Host mice for cell grafting experiments 83 2.52 Anaesthesia and analgesia 84 2.53 Ablation of the satellite cell compartment by local irradiation 84 2.54 Grafting of myoblasts into mouse muscles 84 2.55 Grafting of single myofibres into mouse muscles 85 2.56 Model of acute muscle damage 85 2.6 Tissue preparation for histological analyses 85 2.61 Removal and storage of muscles 85 2.62 Preparation of cryosections 86 2.7 Staining of cells and tissue sections 86 2.71 Fixation methods 86 2.72 Primary antibodies for protein immunochemistry 87 2.73 Antibodies for secondary detection 88 2.74 Immunocytochemistry of cell cultures 88 2.75 Immunocytochemistry of single myofibres 89 2.76 Immunohistochemistry of muscle tissue sections 89 2.77 X-gal staining for localisation of P-gal activity 89 2.78 Haematoxylin and eosin staining 90 2.79 Microscopy and image capture 91 Chapter 3: The myogenic potential of satellite cell grafts 3.1 Background and aim of study 92 3.11 Background to work 92 3.12 Aims of work 94 3.13 Note on genetic markers of grafted cells 94 3.2 Grafts of immortalised satellite cell-derived MPC 95 3.21 Aim 95 3.22 Preparation of a LacZ satellite cell-derived cell line 95 3.23 Muscle formation by different numbers of MPC 96 3.3 Grafts of primary MPC isolated from different muscles 102 3.21 Aim 102 5 Preparation of cell isolates from 3F-nLacZ-2E muscles 102 The myogenic potential of MPC isolated from different muscles 104 Grafts of single myofibres derived from adult muscles 108 Aim 108 Counts of Pax7+ satellite cells associated with single myofibres 108 Preparation and grafting of single myofibres 113 The myogenic potential of EDL single myofibre grafts 114 The myogenic potential of soleus single myofibre grafts 117 The myogenic potential of TA single myofibre grafts 120 Summary: comparison of the myogenic potential of satellite cells derived from different adult muscles 122 Fibre types formed by single myofibre grafts 126 The myogenic potential of EDL single myofibres in long-term grafts 129 Grafts of single myofibres derived from juvenile muscles 133 Aim 133 The myogenic potential of single myofibres derived from juvenile muscles 133 Investigation of the radiation-sensitivity of satellite cells 138 Aim 138 Cells emanating from irradiated single myofibres in culture 138 The myogenic potential of irradiated EDL single myofibres 140 The myogenic potential of irradiated and non-irradiated single myofibres in notexin-damaged sites 140 The myogenic potential of primary MPC isolated from irradiated muscles 143 Comments on results 147 Chapter 4: The potential of satellite cells to self-renew Background and aim of study 150 Background to work 150 Aims of work 151 Note on genetic markers of graft-derived satellite cells 152 6 4.2 The ability of a satellite cell-derived clone to generate new satellite cells 154 4.21 Aim 154 4.22 Preparation of a Myf5nLacZ satellite cell-derived cell line 154 4.23 The potential of immortalised satellite cell-derived Myf5nlacZ myoblasts to give rise to satellite cells 156 4.3 The ability of satellite cells to generate new satellite cells 164 4.31 Aim 164 4.32 Generation of reserve populations from satellite cells in culture 164 4.33 The potential of grafts of Myf5nLacZ/+ single myofibres to give rise to satellite cells 168 4.4 Formation of MPC by single myofibre grafts 177 4.41 Aim 177 4.42 Experiment plan 177 4.43 Grafts of GFP lentivirus-labelled H-21^-tsA58 single myofibres 180 4.5 The contribution of Pax3-GFP+ cells to satellite cells 186 4.51 Background and aim 186 4.52 Identification of satellite cells derived from grafts of Pax3+ cells 186 4.6 Comments on results 191 Chapter 5: The response of satellite cells to damage 5.1 Background and aim of study 195 5.11 B ackground to work 195 5.12 Aims of work 196 5.13 Note on identification of regenerate graft products 196 5.2 The response of grafted satellite cells to damage 197 5.21 Aim 197 5.22 The effect of notexin on control Myf5nLacZ/+ muscles 197 5.23 The effect of notexin on Myf5nLacZ/+ EDL single myofibre grafts 200 5.24 The effect of notexin on Myf5nLacZ/+ soleus single myofibre grafts 204 5.25 The effect of notexin on Myf5nLacZ/+ TA single myofibre grafts 208 5.26 The response of graft-derived cells to repeated bouts of damage 212 7 5.27 Summary: comparison of the response of single myofibre grafts to damage
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