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Characterising the Role of Articular Cartilage Progenitor Cells in Osteoarthritis

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Characterising the Role of Articular Cartilage Progenitor Cells in Osteoarthritis Characterising the role of Articular Cartilage Progenitor Cells in Osteoarthritis Adam Esa (MB BCh) Thesis submitted for the award of PhD, June 2015 i DECLARATION This work has not been submitted in substance for any other degree or award at this or any other university or place of learning, nor is being submitted concurrently in candidature for any degree or other award. Signed ………………………………………… (candidate) Date ………………………… STATEMENT 1 This thesis is being submitted in partial fulfillment of the requirements for the degree of …………………………(insert MCh, MD, MPhil, PhD etc, as appropriate) Signed ………………………………………… (candidate) Date ………………………… STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by explicit references. The views expressed are my own. Signed ………………………………………… (candidate) Date ………………………… STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available online in the University’s Open Access repository and for inter-library loan, and for the title and summary to be made available to outside organisations. Signed ………………………………………… (candidate) Date ………………………… STATEMENT 4: PREVIOUSLY APPROVED BAR ON ACCESS I hereby give consent for my thesis, if accepted, to be available online in the University’s Open Access repository and for inter-library loans after expiry of a bar on access previously approved by the Academic Standards & Quality Committee. Signed ……………………………………… (candidate) Date ……………………… ii Acknowledgments Bismillah Al-Rahman Al-Rahim. First of all, I would like to thank my supervisors Dr Clare Hughes and Prof Charlie Archer. Thanks to both of you for giving me this opportunity to study under your guidance. A special thanks to Clare for all the amazing supervision you provided me over the last 4 years. Also thanks to Professor Bruce Caterson for being an excellent exemplar of dedication to one’s profession. I have learnt from you the highest work ethics and hope to follow it for the rest of my professional life. I would like to thank my colleagues in Caterson, Duance, Mason, Archer and Blain’s research groups. I have learnt a lot from you all during my PhD. A special thanks to my friend and mentor Dr Ahmed Ali for sharing with me this journey and often working together over many weekends and encouragements from the first day. Thank you to Drs Lawrence Glennon-Alty and Shane Wainwright for their encouragement. I would like to thank my collaborators, Dr Ken Ewan for the assistant with the reporter assay work and Dr Gareth Willis for his assistance with the angiogenesis work. I was also lucky to have two talented undergraduate students to supervise namely Amo Sahota and Rob Aldridge, who were a pleasure to teach. I would like to thank my clinical mentors during the years especially Professor Ashraf Rasheed for the amazing training I had and for allowing me to pursue a PhD study. Last, I would like to thank my parents, siblings, Ismahan, Amira and my wife Hanna and the children for helping me. Thank you Hanna, this journey would not have happened without you! Sorry for neglecting my duties over the last few years and sorry for what to come! This PhD study was kindly funded by the Medical Research Council. iii Abstract: Osteoarthritis (OA) is a chronic and highly prevalent degenerative disease of the synovial joint leading to cartilage destruction and bone remodelling. The current management of end-stage OA is joint replacement, however, this procedure is not suitable for a subset of patients hence there is a growing need for alternative treatments and technologies to address this limitation. One such approach to this problem is the application of cell-based therapies that regenerate areas of damaged cartilage. Recently discovered articular cartilage progenitor cells (CPC) have been hallmarked as a potential cell source for repair and/or regeneration of damaged articular cartilage. Initial focus was on the characterisation of human CPC isolated from healthy donors and compared with OA derived CPC and patient matched OA Bone Marrow Mesenchymal Stem Cells (BM-MSCs). Comparison of all cell types showed similar morphology and proliferative capacity. In addition, all cell types isolated showed positive expression of the putative mesenchymal stem cell makers; CD-90, CD-105 and CD-166 while lacking expression of CD-34. All cell types investigated showed successful osteogenic, chondrogenic and adipogenic differentiation, hence providing evidence of the mesenchymal stem cell properties of isolated CPC. A gene profiler array was used to identify the expression of Wnt pathway genes from RNA isolated from CPC cell lines originating from healthy and OA cartilage. Interestingly, the expression of Dkk-1 was observed to have the highest up-regulation in OA-derived CPC. The role of Dkk-1 was further studied in a number of CPC and chondrocyte cell lines from healthy and OA cartilage. It was found that normal CPC cell lines showed homogenously low expression and secretion of Dkk-1, however, OA- derived CPC cell lines exhibited a heterogeneous expression and secretion of Dkk-1. In a pellet culture model of chondrogenic differentiation, CPC cell lines secreting high levels of Dkk-1 failed to undergo chondrogenic differentiation, measured by diminished expression of chondrogenic differentiation markers, Type II collagen, ACAN and Sox-9 at both molecular and protein levels. Immunolocalisation of Dkk-1 in OA osteochondral plugs showed peri-cellular expression in chondrocytes located in all zones and around migratory endothelial cells iv invading articular cartilage where there was a quantifiable increase of blood vessel invasion. This later observation was further studied through a series of experiments to investigate the role of Dkk-1 in relation to endothelial cell migration and angiogenesis using an in vitro model of angiogenesis and migration/invasion assays. A novel finding emerged from these studies, which provides evidence for a pro- angiogenic and pro-migratory role of Dkk-1 and to a lesser extent Dkk-2 in human endothelial cell lines. A novel in vitro Transwell co-culture model was developed to study the interaction between chondrocytes and endothelial cells mimicking the osteochondral interface. A novel finding from these studies included the observation that normal or OA-derived chondrocytes appeared to induce an endothelial to mesenchymal transformation (EndMT) of the co-culture endothelial cells. This was assessed by a loss of the endothelial cobble stone morphology and a down-regulation of key factors implicated in endothelial cell phenotype, including VE-cadherin, Tie-2, e-NOS, PDGF-AA and PECAM-1. As endothelial cells lost their phenotype they adopted a spindle morphology and expressed mesenchymal cell markers including: Lumican, Snail, α- SMA, Vimentin and MMPs. Interestingly, this was also associated with an increase in Dkk-1 expression. To confirm a role for Dkk-1 in this process endothelial cells were cultured in the presence of Dkk-1 and were found to undergo EndMT when compared to the control. In summary, this thesis has uncovered several interesting differences in CPC phenotype. In addition, my results suggest that Dkk-1 has potential as a biomarker of OA pathology. This thesis highlights further the complex role of the Wnt Pathway and in particular Dkk-1 may play a role in the pathogenesis of osteoarthritis. v Contents Acknowledgments .................................................................................................. iii CHAPTER 1: GENERAL INTRODUCTION. .................................................................. 1 1.1 Synovial joint. ................................................................................................ 1 1.1.1 Adult Articular Joint Anatomy................................................................................2 1.1.2 Articular cartilage: Structure and Morphology. .......................................................3 1.1.3 Chondrocytes. ......................................................................................................3 1.1.4 Zones of articular cartilage. ..................................................................................4 1.1.5 Regions of extracellular matrix within articular cartilage. ........................................7 1.2 Subchondral bone. ......................................................................................... 7 1.2.1. Structure and Composition. .................................................................................7 1.2.2 Bone turnover and metabolism .............................................................................9 1.2.3. Osteoblasts. ...................................................................................................... 10 1.2.4. Osteocytes. ....................................................................................................... 11 1.2.5. Osteoclast. ........................................................................................................ 12 1.3 Extracellular Matrix Molecules of cartilage. ................................................. 13 1.3.1 Collagens. .......................................................................................................... 13 1.3.2 Proteoglycans. ................................................................................................... 15 1.4. Maturation of articular cartilage and the skeletal system. .......................... 18 1.5 Pathophysiology of OA. ...............................................................................
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