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NCS-1 Protein Upregulation Facilitates Chronic Hypoxia- Induced Respiratory Adaptation in Lymnaea Stagnalis

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NCS-1 Protein Upregulation Facilitates Chronic Hypoxia- Induced Respiratory Adaptation in Lymnaea Stagnalis NCS-1 protein upregulation facilitates chronic hypoxia- induced respiratory adaptation in Lymnaea stagnalis by Yi Quan A thesis submitted in conformity with the requirements for the degree of Master of Science Graduate Department of Physiology University of Toronto © Copyright by Yi Quan 2012 NCS-1 protein upregulation facilitates chronic hypoxia-induced respiratory adaptation in Lymnaea stagnalis Yi Quan Master of Science Graduate Department of Physiology University of Toronto 2012 Abstract Chronic hypoxia is a consequence of many common diseases, including sleep apnea and chronic lung disease. As there is no cure for many of these diseases, managing the symptoms of these diseases, including hypoxia is of great clinical importance. Preliminary data from the Feng lab show that the calcium binding protein neuronal calcium sensor-1 (NCS-1) is upregulated in the central nervous system of the freshwater pond snail Lymnaea stagnalis following chronic hypoxia treatment. This upregulation coincides with increased aerial respiratory activity. Furthermore, knockdown of NCS-1 attenuates hypoxia-induced facilitation of aerial respiration. Since this aerial respiratory activity is controlled by a respiratory central pattern generator (rCPG), it is hypothesized that hypoxia-induced upregulation of NCS-1 may regulate rCPG activity. Using intercellular sharp electrode recording, I show that in response to chronic hypoxia treatment, there is increased bursting activity and altered action potential profile in the pacemaker neuron of the rCPG, RPeD1. Knockdown of NCS-1 partially prevents these hypoxia- induced changes. Our findings suggest that NCS-1 upregulation is necessary for chronic hypoxia-induced respiratory adaptation. ii Acknowledgments I would like to thank my supervisor – Dr. Feng – for giving me this opportunity to work in this exciting field, and for all her help, guidance and support during this journey. I would also like to thank my committee members – Dr. Charlton and Dr. Jankov – for all their time, suggestions and attention to my work. It was a pleasure working alongside other scientists-in-training in Dr. Feng’s lab: Nasrin Nejatbakhsh, Andrew Barszczyk, and Marielle Deurloo. I am grateful to Qing Li for teaching me Western blots. I would also like to thank Tom Lu and Kathy Li for teaching me intracellular recordings, Mila Aleksic for teaching me qPCR, Mike Qiu and Ryan Instrum for their technical assistance. I would especially like to thank Dr. Jeffrey Dason for his generosity, expertise and for giving me the opportunity to work with him. Thanks to Dr. Rene Prashad, for his advice and assistance and Dr. Alex Smith, for his constructive criticisms. I would also like to thank Dr. Sun, for giving me the opportunity to collaborate with him, and his lab members – Dr. Pei Lin and Dr. Ammar Alibrahim, Christine Bae – it was a pleasure working with you. Thank you. iii Table of Contents Acknowledgments ........................................................................................................................................................iii Table of Contents ......................................................................................................................................................... iv List of Tables ............................................................................................................................................................... vii List of Figures ............................................................................................................................................................viii List of Appendices ........................................................................................................................................................ ix 1 Introduction........................................................................................................................................................... 1 1.1 General Overview ........................................................................................................................................ 1 1.2 Introduction to chronic hypoxia ................................................................................................................... 1 1.2.1 Definition of chronic hypoxia ............................................................................................................. 1 1.2.2 Classification of chronic hypoxia ........................................................................................................ 1 1.2.3 Physiological classification of hypoxia ............................................................................................... 2 1.2.4 Causes of chronic hypoxia .................................................................................................................. 2 1.3 Effects of Hypoxia in Mammalian Systems ................................................................................................. 2 1.3.1 Evolutionarily conserved response to hypoxia .................................................................................... 2 1.3.2 Changes to ion currents in neurons ..................................................................................................... 6 1.3.2.1 Changes in potassium channels in response to chronic hypoxia ................................................. 6 1.3.2.2 Chronic hypoxia-induced changes in Ca2+ currents and channels .............................................. 7 1.3.3 Hypoxia and calcium regulation .......................................................................................................... 7 1.3.4 Calcium binding proteins .................................................................................................................... 8 1.4 Introduction to the Neuronal Calcium Sensor (NCS) Family ...................................................................... 9 1.4.1 Discovery of NCS-1 .......................................................................................................................... 11 1.4.2 Structure ............................................................................................................................................ 14 1.4.3 Expression of NCS-1 ......................................................................................................................... 17 1.4.4 Function: Regulation of basal synaptic transmission and short-term plasticity by NCS-1 ................ 17 1.4.4.1 NCS-1 and Ca2+ channels ......................................................................................................... 18 1.4.4.2 NCS-1 and PI4Kβ ..................................................................................................................... 19 iv 1.4.5 Function: Regulation of K+ channels ................................................................................................. 21 1.4.6 Function: Neuroprotection ................................................................................................................ 21 1.4.7 Function: Hypoxia tolerance ............................................................................................................. 22 1.5 Lymnaea stagnalis as an experimental model ............................................................................................ 22 1.5.1 Lymnaea stagnalis ............................................................................................................................. 23 1.5.2 Aerial respiratory behavior and respiratory central pattern generator ............................................... 23 1.5.3 Hypoxic modulation of rCPG ............................................................................................................ 30 1.5.4 Hypoxia-induced molecular changes................................................................................................. 30 1.6 Hypotheses ................................................................................................................................................. 31 1.6.1 Rationale ........................................................................................................................................... 31 1.6.2 Objectives and Hypotheses ............................................................................................................... 31 1.6.3 Experimental Approach ..................................................................................................................... 32 2 Materials and Methods ........................................................................................................................................ 33 2.1 Animals ...................................................................................................................................................... 33 2.2 Hypoxia treatment ...................................................................................................................................... 33 2.3 Intracellular recordings of RPeD1 ............................................................................................................. 33 2.3.1 Samples ............................................................................................................................................. 33 2.3.2 Semi-intact preparations .................................................................................................................... 34 2.3.3 Electrophysiological recording .........................................................................................................
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