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The Role of Matrix Metalloproteinase 9 and Osteopontin in Synaptogenesis and Reinnervation of the Olfactory Bulb Following Brain Injury

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The Role of Matrix Metalloproteinase 9 and Osteopontin in Synaptogenesis and Reinnervation of the Olfactory Bulb Following Brain Injury Virginia Commonwealth University VCU Scholars Compass Theses and Dissertations Graduate School 2016 The Role of Matrix Metalloproteinase 9 and Osteopontin in Synaptogenesis and Reinnervation of the Olfactory Bulb Following Brain Injury Melissa A. Powell Virginia Commonwealth University Follow this and additional works at: https://scholarscompass.vcu.edu/etd Part of the Neuroscience and Neurobiology Commons © Melissa A. Powell Downloaded from https://scholarscompass.vcu.edu/etd/4646 This Dissertation is brought to you for free and open access by the Graduate School at VCU Scholars Compass. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of VCU Scholars Compass. For more information, please contact [email protected]. ©Melissa A. Powell 2016 All Rights Reserved The Role of Matrix Metalloproteinase 9 and Osteopontin in Synaptogenesis and Reinnervation of the Olfactory Bulb Following Brain Injury A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at Virginia Commonwealth University. by Melissa Ashley Powell Bachelor of Science, Hampton University, 2011 Director: Linda L. Phillips, Ph.D. Professor, Department of Anatomy and Neurobiology Virginia Commonwealth University Richmond, Virginia December, 2016 Acknowledgement I would first like to thank my advisor, Dr. Linda L. Phillips, for being a phenomenal mentor. I appreciate her confidence in my potential, as well as her tremendous patience as I learned and developed both personally and professionally. Her support, wealth of knowledge, and advice have been outstanding, and throughout the years, have shown me the traits of a great mentor who is genuinely vested in her students’ success. I would also like to thank my Ph.D. advisory committee members for being excellent sources of expertise to refine and improve my project. In particular, I thank Dr. Thomas M. Reeves for offering his assistance with statistics and graphic development and Dr. Patricia A. Trimmer for providing an opportunity for me to improve and learn new techniques in her laboratory. Dr. Dong Sun, Dr. Richard M. Costanzo, and Dr. Joseph Porter were instrumental in moving my project forward, and I value each of their respective contributions. In addition to the Department of Anatomy and Neurobiology as a whole, I am extremely grateful for the opportunities afforded me and the support for my career endeavors from the Neuroscience Program Director, Dr. John Bigbee, and the Chairman of our department, Dr. John T. Povlishock. I also owe the members of my laboratory, both past and present, my gratitude for training me, assisting in experiments, and being overall great sources of camaraderie during the past 4 years. Raiford T. Black, Nancy N. Lee, Terry Smith, and Nicholas Russell have made my experience in the Ph.D. program memorable and I sincerely cherish their kindness, advice, and humor, which made the rough days much easier. My friends and family, near and far, including my sorority sisters, have been major sources of encouragement, and I appreciate each and every one of them. I am truly grateful for my Stepdad for always lending an ear, a helping hand, and advice when I needed it most, and my Dad for always believing in me. Finally, I would like to recognize my fiancé and son for being such critical parts of my amazing support system, keeping me happy, levelheaded, and motivated to conclude this incredible journey. I dedicate these collective efforts to my Mom who has always been there for me, despite the circumstance, from the very beginning, and knows exactly what to say to inspire me to press on. ii Table of Contents List of Figures ............................................................................................................................... vii List of Abbreviations .......................................................................................................................x Abstract ..........................................................................................................................................xv Chapter 1: Introduction ................................................................................................................1 Traumatic Brain Injury ........................................................................................................2 Pathophysiology .......................................................................................................4 Neuroexcitation ........................................................................................................6 Positive and Negative Inflammatory Response to TBI ............................................7 Cell Death/Axonal Injury .......................................................................................12 Neuroplasticity after Traumatic Brain Injury ....................................................................17 Inflammation and plasticity ...................................................................................22 Extracellular Matrix ...........................................................................................................26 Proteoglycans and Cell Adhesion Molecules/Extracellular Matrix Role in TBI ...28 Matrix Metalloproteinases .....................................................................................32 MMPs 2 and 9 ........................................................................................................38 Osteopontin ........................................................................................................................41 Structure and Cell Signaling Properties .................................................................41 Role in Inflammation and CNS Disease ................................................................46 Role in CNS Injury and TBI ..................................................................................50 iii Role in CNS Injury and TBI ..................................................................................50 OPN Interaction with MMP9 .................................................................................52 Model System in Present Study: The Olfactory Bulb ........................................................56 Cellular Organization .............................................................................................56 Synapses of the Glomerular Layer .........................................................................64 Induction of Post-Traumatic Anosmia ...................................................................68 Diagnosis of Anosmia ............................................................................................70 Post-traumatic Anosmia and Quality of Life .........................................................72 OB Plasticity and Approaches for Inducing Repair ...............................................73 Treatment of Olfactory Dysfunction in Animal Models ........................................78 OB Synaptogenesis after Injury .............................................................................79 Mouse OB as a model of TBI-induced reactive synaptogenesis .......................................84 OB Deafferentation Models ...................................................................................84 MMP9 Knockout (KO) Mice, Brain Injury, and Neuroplasticity ..........................86 Summary and Hypothesis for Present Study .........................................................87 Chapter 2: Diffuse FPI leads to OB Reactive Synaptogenesis .................................................90 Abstract ..............................................................................................................................91 Introduction ........................................................................................................................92 Methods..............................................................................................................................96 Results ..............................................................................................................................101 Discussion ........................................................................................................................126 Summary ..........................................................................................................................139 iv Chapter 3: MMP9/OPN Signaling Marks OB Synaptic Reorganization after FPI ...................................................................................141 Abstract ............................................................................................................................142 Introduction ......................................................................................................................143 Methods............................................................................................................................147 Results ..............................................................................................................................152 Discussion ........................................................................................................................173 Summary ..........................................................................................................................184 Chapter 4: MMP9 KO Alters Progress of FPI-Induced OB Synapse Regeneration .................................................................................185
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