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Th2 T Cells Are Required for Biomaterial-Mediated Functional Muscle Regeneration

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Th2 T Cells Are Required for Biomaterial-Mediated Functional Muscle Regeneration TH2 T CELLS ARE REQUIRED FOR BIOMATERIAL-MEDIATED FUNCTIONAL MUSCLE REGENERATION by Kaitlyn Noelle Sadtler A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland March, 2016 © 2016 Kaitlyn Sadtler All Rights Reserved Abstract Regenerative medicine therapies that primarily target stem cells have achieved limited success. An alternative strategy is to focus on immune cells, the first responders to traumatic wounds, which can interact directly with biomaterial scaffolds. Here, we investigate how biomaterial scaffolds shape the immune microenvironment in non- traumatic subcutaneous and traumatic muscle wounds (VML) and ultimately impact tissue regeneration. A diverse population of immune cells is recruited into scaffolds and the surrounding area, including macrophages, dendritic cells, T lymphocytes and B lymphocytes. The scaffolds induced a pro-regenerative type-2 response, which, in the VML is characterized by an mTOR/Rictor-dependent Th2 pathway and IL-4-dependent macrophage polarization, critical for functional muscle regeneration. Targeting the adaptive components of the immune system during the process of biomaterials design may support the development of future therapies that efficiently control immune balance in tissues, ultimately stimulating tissue repair. Thesis Readers Jennifer Elisseeff, Ph.D. Department of Biomedical Engineering, Johns Hopkins University Drew Pardoll, M.D. Ph.D. Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine ii Acknowledgements The past 3.5 years have been some of the most exciting, stressful, rewarding years of my life. Throughout that time, I have had the chance to work with amazing individuals and meet friends I will have for the rest of my life. Professionally, I would like to thank Ken Estrellas, a fellow graduate student in the Elisseeff lab that helped me immensely with the muscle studies. He was always willing to lend a hand with dissections, sample preparation, histology and manuscript editing. This included meeting me in lab at 5:00am to start processing samples that I had to have at the core facility by noon, even bringing me in breakfast one of the mornings after I slept at lab. Ken – I cannot thank you enough, you have some of the greatest motivation and the best heart I have seen in science, and wish you the best in your career and life. Additionally, I would like to thank both Vince Beachley and Matt Wolf, who were in the lab as postdocs. Vince, you were my mentor during my rotation even though you had no idea what I was doing with all the immunology, you were always there to lend a helping hand and tell me to relax a bit when I tried to get everything done in a short period of time. Matt, after Vince left, you got to deal with the hyper-productive grad student with a heavy dose of immunology. You helped out more than I could have hoped, your knowledge of the field and biomaterials was very helpful as I waded through the biomaterial and engineering literature as a molecular biologist, and have become a great friend who is always willing to take a red pen to anything I write and provide amazing feedback. For about a year, right when things started picking up, I worked with an undergraduate student, Brian Allen, who has since moved on to grad school. Brian, thanks for all of your help in sample prep and PCR. Couldn’t have finished these experiments as quickly without your helping hand. Best of luck in your career, you will do great things. Franck Housseau, from the Pardoll lab, thank you very much for all of your iii guidance in immunology, and being open to the new project and field as it developed, your guidance and willingness to answer my questions is greatly appreciated. Additionally, I would like to thank the members of my thesis committee (Dr. Andrew Ewald, Dr. Jordan Green, Dr. Jonathan Schneck) that guided me through my project and helped me with paper planning and my plans after graduate school. Dr. Drew Pardoll, my committee chair, I greatly appreciate the collaboration with your lab and all of the insight you had from your years of immunology experience, and your excitement and enthusiasm for the project. Finally, my PI, Dr. Jennifer Elisseeff. Jennifer, I couldn’t have asked for a better advisor, you challenged me and gave me the resources to grow as a scientist. The opportunities I had in your lab were amazing, from the research at Hopkins and collaborations stretching multiple differences, to conferences taking me to exciting places and meeting some of the biggest names in the field. I cannot thank you enough. Personally, I have met many amazing people at Hopkins. A non-exhaustive list of friends I’d like to thank for being there throughout the years includes Rebecca Tweedell, Donna Dang, Meredith Stone, Jackie Pham, Melissa Bowman, Emily Bergbower, Iris Chen, Alex Mims, Nina Hosmane, Karen Cravero, Katie and Kyle Bruner, Ashley Cook, Kathleen Cunningham, and Heather Jacobs. I’d especially like to thank Rebecca Tweedell who was my roommate and classmate for the first two years of grad school. We worked together through first year classes, and sitting together while studying for our qualifying exams for weeks in silent solidarity. You are one of the best friends I have made during grad school and always there when experiments failed or things got too stressful, and on the other side you were always there for celebratory pie or froyo when we got things right. From the minute I was born, my family has always supported me in my endeavors. My brother, Sean, thanks for being there for Sam and I when we were growing up, and being an amazing friend and brother. Sam, my sister and partner in iv adventure. Life is always interesting when you are around, you are always there to take a phone call, and up for an adventure at any time. I cannot wait for our future explorations around the world, you are amazing, the first doctor in our family and the best sister I could’ve asked for. Mom and Dad, I couldn’t have done any of this without you. Thank you for supporting me through the years and always promoting me to do my best, even when I didn’t think I could achieve it. Thank you for making me stubborn and driven, and willing to help others along the way. You always told me I could achieve whatever I set my mind to and, well, here is the result of that. This is for you two. v Table of Contents Abstract .................................................................................................................... ii Acknowledgements ................................................................................................. iii List of Abbreviations ............................................................................................. viii List of Tables ............................................................................................................ x List of Figures .......................................................................................................... xi Chapter 1: Introduction ............................................................................................. 1 Introduction ........................................................................................................... 2 Tissue-Based Class Control............................................................................................ 2 Immune Privileged Sites and Clonal Ignorance ............................................................... 4 Development and The Immune System .................................................................. 5 Shared Signaling Molecules: Immune Response and Developmental Biology ................. 5 Functional Healing: Tissue Engineering’s Approach to Development............................... 7 Polymer Scaffolds and the Surrounding Tissue Environment ................................... 9 Polyethylene glycol (PEG) Hydrogels ............................................................................ 10 Foreign Body Response (FBR) Microenvironment......................................................... 11 Synthetics Coated with Extracellular Matrix (ECM) Scaffolds......................................... 11 Decellularized Extracellular Matrix: A Model and Scaffold ..................................... 12 Small Intestinal Submucosa (SIS) ................................................................................. 12 Urinary Bladder Matrix (UBM) ....................................................................................... 13 Acellular Adipose Tissue (AAT)..................................................................................... 13 As an Immunomodulatory Reagent and Tissue Model................................................... 15 Biochemical and Physical Alterations of Scaffolds................................................. 16 Physical Alteration of ECM & Synthetics ............................................................... 17 Cyclodextrin and RGD modification of Polymeric Scaffolds ........................................... 18 Growth Factor Modification and Modulation of Microenvironment .................................. 18 Summary ............................................................................................................ 19 Chapter 2: Methods................................................................................................. 24 Tissue ECM Preparation .....................................................................................
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