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Downloaded by Mcgill University 10/04/2015 14:12:50 CELLULAR MECHANISMS OF BRAIN-DERIVED NEUROTROPHIC FACTOR MEDIATED SYNAPSE REORGANIZATION FOLLOWING HIPPOCAMPAL INJURY By, Raminder Gill, B. Sc. Department of Pharmacology & Therapeutics McGill University Montréal, Québec, Canada April 2015 A thesis submitted to McGill University in partial fulfillment of the requirements of the degree of Doctor of Philosophy © Raminder Gill, 2015 TABLE OF CONTENTS TABLE OF CONTENTS .............................................................................................................. i ABSTRACT .................................................................................................................................. iv RÉSUMÉ ..................................................................................................................................... vii ACKNOWLEDGMENTS ............................................................................................................ x ABBREVIATIONS ..................................................................................................................... xii PREFACE ................................................................................................................................... xiv CONTRIBUTIONS TO ORIGINAL SCIENCE .................................................................... xvi CHAPTER 1. INTRODUCTION ................................................................................................ 1 1.1. GENERAL BACKGROUND ............................................................................................ 1 1.2. OVERVIEW OF THE HIPPOCAMPUS ........................................................................ 2 1.3. NEURONAL MORPHOLOGY AND FUNCTIONALITY ........................................... 7 1.3.1. Dendritic Spine and Axon Development ....................................................................... 8 1.3.2. Excitatory Neurotransmission in CA1 Pyramidal Neurons ......................................... 10 1.3.3. Synaptic Plasticity of Excitatory Synapses ................................................................. 13 1.3.4. Inhibitory Neurotransmission in CA1 Pyramidal Neurons ......................................... 16 1.3.5. Synaptic Plasticity of Inhibitory Synapses .................................................................. 19 1.4. HIPPOCAMPUS AND INJURY .................................................................................... 23 1.4.1. Epilepsy ....................................................................................................................... 23 1.4.2. Ischemia and Stroke ..................................................................................................... 27 1.4.3. Defects in Plasticity Following Brain Injury ............................................................... 30 1.5. NEUROTROPHIC FACTORS AND THEIR RECEPTORS ...................................... 33 1.5.1. Overview of Neurotrophins ......................................................................................... 33 1.5.2. Neurotrophin Receptors and Signaling Cascades ........................................................ 35 1.5.2.1. Trk Receptor Signaling ........................................................................................ 37 1.5.2.2. p75NTR Signaling .................................................................................................. 38 1.6. BRAIN-DERIVED NEUROTROPHIC FACTOR ....................................................... 41 1.6.1. Transcription, Secretion and Processing of BDNF ..................................................... 41 1.6.2. Activity-Dependent Regulation of BDNF ................................................................... 43 1.6.3. BDNF in Synapse Development.................................................................................. 45 1.6.3.1. BDNF and Development of Excitatory Synapses ................................................. 45 1.6.3.2. BDNF and Development of Inhibitory Synapses ................................................. 47 1.6.3. BDNF and Glutamatergic Plasticity ............................................................................. 49 1.6.4.1. Role of BDNF in Excitatory Presynaptic Plasticity ............................................. 50 1.6.4.2. Role of BDNF in Excitatory Postsynaptic Plasticity ........................................... 50 1.6.5. BDNF and GABAergic plasticity ................................................................................ 51 1.6.6. BDNF and Brain Injuries ............................................................................................. 53 1.7. ORGANOTYPIC HIPPOCAMPAL SLICE CULTURES .......................................... 57 CHAPTER 2. BDNF AND PROBDNF DIFFERENTIALLY REGULATE ISCHEMIA- INDUCED PLASTICITY OF GABAERGIC AND GLUTAMATERGIC SYNAPSES OF CA1 PYRAMIDAL NEURONS ................................................................................................ 60 FOREWORD ........................................................................................................................... 60 2.1. ABSTRACT ...................................................................................................................... 61 i 2.2. INTRODUCTION ............................................................................................................ 62 2.3. MATERIALS AND METHODS..................................................................................... 64 2.3.1. Ethics Statement .......................................................................................................... 64 2.3.2. Hippocampal Slice Cultures and Oxygen-Glucose Deprivation ................................. 64 2.3.3. Propidium Iodide Staining, Immunofluorescence and Confocal Microscopy ............ 65 2.3.4. Dendrite Reconstructions, Spine Quantification and Puncta Quantification .............. 66 2.3.5. Electrophysiological Recordings and Analysis ........................................................... 67 2.3.6. RT-qPCR ..................................................................................................................... 69 2.3.7. Pharmacological Treatments ....................................................................................... 69 2.3.8. Biolistic Gene Transfection ......................................................................................... 70 2.3.9. Statistical Analysis ...................................................................................................... 71 2.4. RESULTS .......................................................................................................................... 72 2.4.1. Area CA1 is selectively affected following OGD in organotypic hippocampal slices 72 2.4.2. OGD disrupts excitatory synapses morphologically and functionally ........................ 74 2.4.3. OGD disrupts GABAergic inhibitory synapses morphologically and functionally .... 77 2.4.4. Expression of bdnf mRNA increases after OGD and TrkB-Fc treatment rescues OGD- induced excitatory synapse deficit ......................................................................................... 84 2.4.5. TrkB-Fc treatment rescues OGD-induced inhibitory synapse deficit ......................... 88 2.4.6. Blocking mBDNF prevents gephyrin downregulation but not dendritic spine loss .... 92 2.4.7. Preventing ERK1/2 activation and blocking GSK3β prevents gephyrin degradation, but not dendritic spine loss .................................................................................................... 98 2.4.8. Blocking proBDNF and p75NTR prevents dendritic spine loss but not gephyrin loss 108 2.5. CONCLUSION ............................................................................................................... 112 2.5.1. OGD leads to loss of glutamatergic and GABAergic synapses in CA1 neurons and increases bdnf mRNA expression ........................................................................................ 112 2.5.2. mBDNF disrupts GABAergic synapses after OGD .................................................. 114 2.5.3. proBDNF and p75NTR disrupt glutamatergic synapses after OGD ............................ 116 CHAPTER 3. BLOCKING BDNF INHIBITS INJURY INDUCED HYPEREXCITABILITY OF HIPPOCAMPAL CA3 NEURONS ...................................... 119 FOREWORD ......................................................................................................................... 119 3.1. ABSTRACT .................................................................................................................... 120 3.2. INTRODUCTION .......................................................................................................... 121 3.3. MATERIALS AND METHODS................................................................................... 123 3.3.1. Ethics Statement ........................................................................................................ 123 3.3.2. Hippocampal Slice Cultures and Schaffer Collateral Lesions................................... 123 3.3.3. Visualization of CA3 Pyramidal Neurons ................................................................. 124 3.3.4. Electrophysiological Recordings and Analysis ......................................................... 124 3.3.5. Immunohistochemistry .............................................................................................. 126 3.3.6. RT-qPCR ..................................................................................................................
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