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Design and Characterization of Photopolymerizable Semi DESIGN AND CHARACTERIZATION OF PHOTOPOLYMERIZABLE SEMI- INTERPENETRATING NETWORKS FOR IN VITRO CHONDROGENESIS OF HUMAN MESENCHYMAL STEM CELLS by AMANDA NICOLE BUXTON Submitted in partial fulfillment of the requirements For the degree of Doctor of Philosophy Dissertation Adviser: Dr. Brian Johnstone Department of Biomedical Engineering CASE WESTERN RESERVE UNIVERSITY August, 2007 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the thesis/dissertation of _____________Amanda N. Buxton______________________ candidate for the Doctor of Philosophy degree *. (signed)_____Roger Marchant______________ (chair of the committee) ________________Stuart Rowan____________________________ __________________Steve Eppell___________________________ __________________Brian Johnstone________________________ _______________Joseph Mansour___________________________ _______________Lloyd A. Culp_____________________________ (date) ___April 3, 2007____________________ *We also certify that written approval has been obtained for any proprietary material contained therein. TABLE OF CONTENTS List of Tables iii List of Figures iv Acknowledgements vii List of Abbreviations viii Glossary ix Abstract 1 Chapter One: Background & Significance 3 Structure & Function of Articular Cartilage 4 Formation of Cartilage 13 Articular Cartilage Pathology & Repair 17 Tissue Engineering Design Criteria 20 Cell Source 21 Scaffold Considerations 22 Addition of Bioactive Factors 25 Chapter Two: In Vitro Chondrogenesis in a Poly(ethylene glycol) Diacrylate (PEGDA) Scaffold – Preliminary Experiments 30 In Vitro Chondrogenesis in Pellet Culture 30 MSC Encapsulation in 20% (w:v) PEGDA (6 kDa) Hydrogels 34 Examination of the Photoinitiator 36 Formation of the Semi-Interpenetrating Network 38 Conclusions 42 i Chapter Three: Design and Characterization of Photopolymerizable Poly(ethylene glycol) Semi-Interpenetrating Networks for Chondrogenesis of Human Mesenchymal Stem Cells 44 Abstract 45 Introduction 46 Materials & Methods 49 Results 54 Discussion 67 Acknowledgements 72 Chapter Four: In Vitro Chondrogenesis of Human Mesenchymal Stem Cells in Hydrogels is Affected by Temporal Exposure to Chondrogenic Factors 73 Abstract 74 Introduction 75 Materials & Methods 76 Results 80 Discussion 89 Acknowledgements 94 Chapter Five: Conclusions & Future Work 95 Can Further Alterations Improve Matrix Elaboration? 104 What Type of Animal Model Should Be Explored? 110 Summary 111 Bibliography 112 ii LIST OF TABLES Chapter Three 3-1. Experimentally determined swelling ratios, Q, for PEGDA scaffolds fabricated with and without PEG. 57 3-2. Molecular weight between crosslinks, MC, and mesh size, ξ, calculated for PEGDA hydrogels. 58 iii LIST OF FIGURES Chapter One 1-1. Components of the extracellular matrix 7 1-2. Zonal architecture of adult articular cartilage 11 1-3. Endochondral ossification 15 Chapter Two 2-1. Toluidine blue stained histological sections and immunohistochemistry for collagen type II of human pellets after 1, 3, 6, 9, and 14 days of culture. 32 2-2. Immunohistochemistry for collagen types I, II, and X in day 1 and 14 pellets. 33 2-3. Chemical structure of PEGDA 35 2-4. Toluidine blue histological sections of 20% (w:v) PEGDA cell-seeded constructs. 37 2-5. Cellular viability of hMSCs subsequent to initiator and UV exposure, assessed through LDH activity. 39 2-6. Idealized and simplified depiction of an interpenetrating network. 40 2-7. Toluidine blue stained histological sections at 3 and 6 weeks. 43 Chapter Three 3-1. Extracellular matrix content of PEGDA (6 kDa) hydrogels polymerized with increasing concentrations of initiator. 56 3-2. Extracellular matrix content of constructs fabricated with the addition of PEG to PEGDA (6 kDa) at a PEGDA:PEG ratio of 2:1. 60 3-3. Extracellular matrix content of PEGDA (6 kDa) hydrogels iv constructed at varying ratios of PEGDA:PEG. 62 3-4. Proteoglycan distribution in PEGDA (6 kDa) constructs fabricated with PEG at different ratios. 63 3-5. Extracellular matrix content of networks constructed with increased PEGDA molecular weight and PEG (88 kDa) at varying PEGDA:PEG ratios. 64 3-6. Proteoglycan distribution in higher molecular weight PEGDA constructs fabricated with PEG (88 kDa). 66 Chapter Four 4-1. Comparison of extracellular matrix content at 6 weeks in constructs fabricated at different initial seeding densities. 81 4-2. Proteoglycan distribution of constructs made with different initial cell seeding density. 82 4-3. Extracellular matrix content of hydrogels fabricated with hMSCs pretreated in monolayer culture with defined chondrogenic medium. 84 4-4. Extracellular matrix content of hMSC-seeded scaffolds subjected to TGF-β1 withdrawal from defined chondrogenic medium. 86 4-5. Extracellular matrix content of hydrogels subjected to dexamethasone withdrawal from defined chondrogenic medium. 88 Chapter Five 5-1. Immunohistochemistry for collagen types II and X of hMSC-seeded PEGDA:PEG networks cultured in defined chondrogenic medium that was subjected to removal of DEX or TGF-β1. 102 v 5-2. Immunohistochemistry for collagen types II and X of hMSC-seeded constructs cultured for 6 weeks in defined chondrogenic medium lacking or containing dexamethasone. 103 5-3. Extracellular matrix content of PEGDA scaffolds fabricated with or without tethered RGD. 106 5-4. Toluidine blue histological sections of hMSC-seeded constructs encapsulated in PEGDA polymer scaffolds with and without tethered RGD. 108 vi ACKNOWLEDGEMENTS Any degree is an undertaking. While the efforts that merit the achievement must be those of the student, they are not attained without support. The student, in fact, is supported by an extensive social network – family, friends, peers, and faculty all aid in the endeavor. This holds true in my experience and has been the case for everyone I have met in my graduate work, without exception. To those who have invested countless hours teaching, training, listening, encouraging, and loving me – I am eternally grateful. You know who you are: my committee, my academic and research advisors, my current and previous lab- mates, my family and friends. Thank you so very much. vii LIST OF ABBREVIATIONS MSC: Mesenchymal Stem Cell PEG: Poly(ethylene glycol) PEGDA: Poly(ethylene glycol) Diacrylate ECM: Extracellular Matrix CS: Chondroitin Sulfate (chains) KS: Keratan Sulfate (chains) SLRPs: Small Leucine-Rich Proteoglycans COMP: Cartilage Oligomeric Matrix Protein OA: Osteoarthritis DMEM: Dulbecco’s Modified Eagles Medium FBS: Fetal Bovine Serum PBS: Phosphate Buffered Saline FGF: Fibroblast Growth Factor TGF-β: Transforming Growth Factor-β GC: Glucocorticosteroid DEX: Dexamethasone BMPs: Bone Morphogenic Proteins LAP: Latency Associated Peptide LTBP: Latent TGF-β Binding Proteins LLC: Large Latency Complex TβRI & II: TGF-β Receptors I & II viii GLOSSARY Hydrogels: insoluble polymer networks that are composed of water-soluble polymers, which are made insoluble by addition of a crosslinking component. Semi-Interpenetrating Network: a hydrogel that employs two polymer components. Networks may be classified as covalent or non-covalent, depending on whether both polymers form covalent crosslinks. A non-covalent form is employed in this study, which uses the secondary (nonbinding) component to add stability, increase mass transport, and leave space for extracellular matrix elaboration. Fibrillation: a process by which degradation of PGs and collagens occurs. Osteochondritis Dessicans: a disorder leads to fracture through the subchondral bone and partial or complete separation of a fragment of the articular surface. Osteoarthritis: the most common joint disease, caused by joint degeneration. This process involves the progressive loss of articular cartilage, followed by attempted repair of cartilage, remodeling and sclerosis of subchondral bone, and in many instances the formation of subchondral bone cysts and marginal osteophytes. Crepitis: catching, grating, or grinding sensations during movement. Endochondral Ossification: one of the two processes by which bone is formed. In this case, bone development occurs through a transitional cartilage element. Chondrogenesis: the process by which cartilage is formed. Mesenchymal stem cells differentiate to become chondrocytes, which then synthesize all of the proteins and carbohydrates required to form the intricate extracellular matrix of which cartilage is comprised. ix Design and Characterization of Photopolymerizable Semi-Interpenetrating Networks for In Vitro Chondrogenesis of Human Mesenchymal Stem Cells ABSTRACT by AMANDA NICOLE BUXTON Cartilage is formed through the process of chondrogenesis, in which mesenchymal stem cells (MSCs) differentiate to become chondrocytes. Chondrocytes then synthesize all of the components of the intricate extracellular matrix (ECM) of which cartilage is comprised. Articular cartilage has a very poor reparative ability and extracellular matrix degradation leads to the eventual destruction of the tissue. Tissue engineering presents a possible avenue for its repair and regeneration. Because hydrogels are mimetic of the native, 3-dimensional, water-swollen environment in which chondrocytes exist, they have been the focus of much research in terms of cartilage tissue engineering, but success has been limited. This thesis describes the design and characterization of poly(ethylene diacrylate) (PEGDA) and poly(ethylene) (PEG)-based semi-interpenetrating networks that facilitated the formation of cartilage by human MSCs. Alterations in the molecular
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