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Immune Characterization and Phase I Clinical Testing of an Adipose Extracellular Matrix-Derived Biomaterial for Soft Tissue Reconstruction

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Immune Characterization and Phase I Clinical Testing of an Adipose Extracellular Matrix-Derived Biomaterial for Soft Tissue Reconstruction IMMUNE CHARACTERIZATION AND PHASE I CLINICAL TESTING OF AN ADIPOSE EXTRACELLULAR MATRIX-DERIVED BIOMATERIAL FOR SOFT TISSUE RECONSTRUCTION by Amy Elizabeth Anderson A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland October 2017 © 2017 Amy Elizabeth Anderson All Rights Reserved ABSTRACT Adipose tissue is used by surgeons for a variety of applications, including soft tissue reconstruction and wound healing. However, harvesting adipose tissue from patients presents challenges such as donor-site morbidity, outcome variability, and insufficient tissue volumes. To address this clinical challenge, we aimed to create an "off-the-shelf" adipose material using mechanical and chemical processing techniques which remove lipids and living cells while processing the tissue into an injectable form preferred by patients and physicians. A Phase I clinical study conducted in eight healthy volunteers assessed the safety and tolerability of Acellular Adipose Tissue (AAT) – an adipose extracellular matrix-derived biomaterial intended for the repair of soft tissue defects in humans. The trial evaluated subcutaneous injections of AAT administered in redundant tissues previously scheduled for removal in an elective surgical procedure (i.e. panniculectomy) between 1 and 18 weeks post-injection. AAT was well-tolerated in this first-in-human study and demonstrated satisfactory participant comfort and physician ease-of-use ratings. No patients experienced an adverse or unanticipated event related to their study participation. Additionally, we evaluated immune profiles of AAT in both human and murine tissue samples to quantify the presence of T cells, B cells, dendritic cells, macrophages, M1- polarized (inflammatory) macrophages, and M2-polarized (wound-healing) macrophages. Our clinical results indicate that the populations of immune cells migrating into AAT from the surrounding tissue match those of native adipose in terms of cell type and gene expression. For some patients at early excision times, AAT was associated with pro- regenerative immune responses, including M2 macrophage polarization and increased IL-4 expression. Addition in vivo studies investigated the local immunological microenvironment ii created by AAT in both non-traumatic and injured environments, as the ability to modulate immune response in a targeted approach may be used to improve wound healing. These studies also aimed to characterize the effect of xenogeneic ECM vs. syngeneic ECM in a mouse model of volumetric muscle loss (VML). Overall, our preclinical and clinical findings show that AAT is a promising new therapeutic tool for soft tissue reconstruction and is safe for subcutaneous use in humans. Further studies, including a Phase II trial, are necessary to determine clinical efficacy. Advisor: Jennifer H. Elisseeff, Ph.D. Thesis Committee: Damon S. Cooney, M.D., Ph.D. (Reader) Jeff W. M. Bulte, Ph.D. (Chair) William Guang Wong, Ph.D. Drew Pardoll, Ph.D. Patrick Byrne, M.D. iii ACKNOWLEDGEMENTS I would like to acknowledge the many individuals who helped make this work possible. The members of the Elisseeff lab who provided intellectual and technical support were invaluable both in my personal development and in the success of this work. Dr. Zayna Nahas and Dr. Iwen Wu pioneered much of the early process development and preclinical studies that would become the foundation of my thesis and enable us to obtain approval to begin human testing. Jessica Yang also helped introduce me to the adipose ECM project and provided much of my initial training. I am deeply thankful for their contributions (and meticulous record keeping), without which this project would never have existed. I also would like to acknowledge the people who helped make the clinical trial possible, including our team of physicians (Drs. Damon Cooney and Patrick Byrne), our trial manager (Carisa Cooney), our regulatory and manufacturing consultant (Susan Wade), and clinical fellows (Rachael Payne and Jeff Aston). My advisor, Dr. Jennifer Elisseeff, has been a constant source of inspiration. My appreciation of her incredible work ethic and breadth of knowledge has grown continually over the past six years, because it is hard to imagine anyone more ambitious or dedicated to growing her ecosystem. Her direction of this project and help thinking through the tough questions has been invaluable – when I am hung up on details, she can always help me see the big picture. While setting a high bar as an investigator, Dr. Elisseeff still manages to be a kind and flexible supervisor who prioritizes the career goals of her students. It is uncommon to find all of these qualities in a mentor, and I am eternally grateful for the opportunities she has given me. iv I worked alongside many fantastic people during my years in the Elisseeff laboratory; however, one person’s contribution to my work stands well above all the others. Alexis Parrillo was my close partner and a dear friend throughout these studies and shares in every success. Whether we were disemboweling mice, wading through buckets of human fat or simply thinking though yet another experiment together, Alexis never failed to brighten my day and always helped turn daunting tasks into new achievements. Lastly, I am grateful for the support of my friends and family, without whom I would not be where (or who) I am today. I could not have asked for a better group of people to share the graduate school experience with than my CMM classmates. I would like to thank my parents, Lisa and Tim Anderson, and sister, Kelsey, for their unwavering faith in my decisions, even when my choices took me far from home. Finally, I want to thank Ashkon – my best friend and partner in everything (outside the lab) – for being my imperturbable rock and for following me across the country to be a part of this adventure with me. v TABLE OF CONTENTS ABSTRACT ........................................................................................................................................... ii ACKNOWLEDGEMENTS .................................................................................................................. iv TABLE OF CONTENTS ...................................................................................................................... vi LIST OF FIGURES ............................................................................................................................. viii LIST OF TABLES ................................................................................................................................ ix 1. INTRODUCTION .......................................................................................................................... 1 2. BIOCHEMICAL CHARACTERIZATIONS OF ACELLULAR ADIPOSE TISSUE (AAT) – AN ADIPOSE EXTRACELLULAR MATRIX-DERIVED BIOMATERIAL .............................. 9 2.1. Introduction ................................................................................................................................ 9 2.2. Materials and Methods ............................................................................................................. 13 2.2.1. Adipose processing and AAT manufacturing .................................................................. 13 2.2.2. Collagen content ............................................................................................................... 14 2.2.3. SDS-PAGE ....................................................................................................................... 14 2.2.4. Lipid content ..................................................................................................................... 15 2.2.5. Cell migration ................................................................................................................... 15 2.2.6. Residuals testing ............................................................................................................... 17 2.2.7. Statistical analyses ............................................................................................................ 18 2.3. Results ...................................................................................................................................... 18 2.3.1. Adipose processing and AAT manufacturing .................................................................. 18 2.3.2. Collagen content ............................................................................................................... 19 2.3.3. SDS-PAGE ....................................................................................................................... 20 2.3.4. Lipid content ..................................................................................................................... 21 2.3.5. Cell migration ................................................................................................................... 22 2.3.6. Residuals testing ............................................................................................................... 23 2.4. Discussion ................................................................................................................................ 24 3. IMMUNE CHARACTERIZATION OF AAT IN MURINE MODELS OF WOUND HEALING ............................................................................................................................................ 31 3.1. Introduction .............................................................................................................................
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