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DEVELOPMENT of a REGENERATIVE MEDICINE STRATEGY for the TREATMENT of DUCHENNE MUSCULAR DYSTROPHY by Kenneth Michael Estrellas A

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DEVELOPMENT of a REGENERATIVE MEDICINE STRATEGY for the TREATMENT of DUCHENNE MUSCULAR DYSTROPHY by Kenneth Michael Estrellas A DEVELOPMENT OF A REGENERATIVE MEDICINE STRATEGY FOR THE TREATMENT OF DUCHENNE MUSCULAR DYSTROPHY by Kenneth Michael Estrellas A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland March 2017 © 2017 Kenneth Michael Estrellas All Rights Reserved Abstract Despite decades of work, Duchenne Muscular Dystrophy (DMD) remains a deadly disease with no cure. Recent advances in stem cell biology, immunology, and bioengineering suggest an interdisciplinary approach to the treatment of DMD. Towards this end, we created a multifunctional hydrogel composed of hyaluronic acid and skeletal muscle extracellular matrix that is cytocompatible, injectable, and biodegradable. The hydrogel facilitates the controlled release of myostatin inhibitors in vitro and increases their bioactivity in vivo. The hydrogel also promotes macrophage polarization towards CD206 expression, elevates anti-inflammatory cytokine levels, and co-injection of hydrogel with myostatin inhibitor yields a significant increase in Foxp3+ regulatory T cells. Finally, human embryonic stem cell derived myoblasts transplanted with the hydrogel demonstrated greater survival at 7-10 days post-injection, and increased engraftment after 4 months in immunodeficient dystrophic mice. Overall, this study represents a promising advance in regenerative medicine therapies for DMD. Advisors / Thesis Readers Jennifer Elisseeff, Ph.D. Department of Biomedical Engineering, Johns Hopkins University Kathryn Wagner, M.D. Ph.D. Departments of Neurology and Neuroscience, Johns Hopkins University School of Medicine ii Acknowledgements To Kathryn and Jennifer, for your guidance, mentorship, insight, and patience. To Kaitlyn for introducing me to the world of immunology, Matt and Liam for helping me analyze endless FACS samples, Shoumyo for helping with rheology, and everyone else in the Elisseeff lab for being awesome. To Lindsay, for being the best undergraduate mentee a grad student could ever ask for. To Tracy and Naili for teaching me how to cryosection and harvest muscle, to Jyothi for correcting me, and everyone else in the Wagner lab for being awesome. To Colleen, Leslie, Rajini, Bob, and everyone else in the CMM program for giving me the opportunity to train at such an amazing place. To my CMM Class of 2011, and everyone I’ve met at Hopkins, it’s been a wonderful journey. To all those still in the process – you’ll get there soon! To Edith, Dan, and Sorin for introducing me to the world of biomedical research. Thank you for taking your chances on an inexperienced undergraduate! To BDCP, Project D, imPulse, and the greater urban dance community for giving me a second life outside of science, and friends no matter where I go. To all my friends from Kindergarten to College, for always being there for me. To Mom, Dad, Tita, Jeff, and Sheryll, thank you for instilling and supporting my love for science since childhood. I literally wouldn’t be here without you. To Jean, for everything. I love you with all of my heart, and look forward to us forever. iii Table of Contents Abstract ............................................................................................................................................ ii Acknowledgements......................................................................................................................... iii List of Abbreviations ........................................................................................................................ v List of Tables ................................................................................................................................... vi List of Figures ................................................................................................................................. vii Chapter 1: Introduction ................................................................................................................... 1 Overview ...................................................................................................................................... 2 Duchenne Muscular Dystrophy (DMD) ....................................................................................... 3 Treatments and Therapies for DMD ............................................................................................ 4 Cellular Therapies in DMD ........................................................................................................... 6 Role of Myostatin Inhibition in DMD ........................................................................................... 7 Skeletal Muscle and the Immune System ................................................................................... 8 Biomaterials and Regenerative Medicine in Skeletal Muscle ................................................... 10 Overall Summary ....................................................................................................................... 11 Chapter 2: Fabrication and Characterization of Skeletal Muscle Hydrogel ................................... 12 Abstract ..................................................................................................................................... 13 Introduction ............................................................................................................................... 14 Materials and Methods ............................................................................................................. 15 Results ....................................................................................................................................... 20 Discussion .................................................................................................................................. 23 Figures ....................................................................................................................................... 26 Supplementary Data .................................................................................................................. 31 Chapter 3: Hydrogel-Mediated Effects on the Immune Microenvironment ................................. 34 Abstract ..................................................................................................................................... 35 Introduction ............................................................................................................................... 36 Materials and Methods ............................................................................................................. 37 Results ....................................................................................................................................... 40 Discussion .................................................................................................................................. 42 Figures ....................................................................................................................................... 45 Supplementary Data .................................................................................................................. 55 Chapter 4: Hydrogel-Mediated Transplantation of Skeletal Muscle Cells ..................................... 62 Abstract ..................................................................................................................................... 63 Introduction ............................................................................................................................... 64 Materials and Methods ............................................................................................................. 65 Results ....................................................................................................................................... 69 Discussion .................................................................................................................................. 71 Figures ....................................................................................................................................... 74 Chapter 5: Conclusions and Future Directions .............................................................................. 79 Conclusions ................................................................................................................................ 80 Future Directions ....................................................................................................................... 83 References ..................................................................................................................................... 85 Curriculum Vitae ............................................................................................................................ 97 iv List of Abbreviations AAV Adeno-Associated Viral Vector CD Cluster of Differentiation CTX Cardiotoxin DMD Duchenne Muscular Dystrophy dSKM Decellularized Skeletal Muscle DYS Dystrophin ECM Extracellular Matrix FACS Fluorescence Activated Cell Sorting H&E Hematoxylin and Eosin hESC Human Embryonic Stem Cell hESMyo hESC-derived myoblast hiPSC Human Induced Pluripotent Stem Cell hLAC Human Lamin A+C hLAM Human Laminin HA Hyaluronic Acid HA-NHS Hyaluronic Acid Succinimidyl Succinate IF Immunofluorescence IFN Interferon IL Interleukin MFI Mean Fluorescence Intensity NHS N-hydroxysuccinimide NRG NOD-Rag1null-IL2rgnull NSG NOD-SCID-IL2rgnull
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