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Post-Translational Sumoylation Dynamically Regulates Voltage- Gated Potassium Channel, Kv4.2

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Post-Translational Sumoylation Dynamically Regulates Voltage- Gated Potassium Channel, Kv4.2 Georgia State University ScholarWorks @ Georgia State University Biology Dissertations Department of Biology 8-10-2021 Post-translational SUMOylation dynamically regulates voltage- gated potassium channel, Kv4.2 Meghyn Welch Follow this and additional works at: https://scholarworks.gsu.edu/biology_diss Recommended Citation Welch, Meghyn, "Post-translational SUMOylation dynamically regulates voltage-gated potassium channel, Kv4.2." Dissertation, Georgia State University, 2021. https://scholarworks.gsu.edu/biology_diss/251 This Dissertation is brought to you for free and open access by the Department of Biology at ScholarWorks @ Georgia State University. It has been accepted for inclusion in Biology Dissertations by an authorized administrator of ScholarWorks @ Georgia State University. For more information, please contact [email protected]. Post-translational SUMOylation dynamically regulates voltage-gated potassium channel, Kv4.2 by Meghyn Welch Under the Direction of Deborah Baro, PhD A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the College of Arts and Sciences Georgia State University 2021 ABSTRACT The family of voltage-gated Kv4 ion channels (Kv4.1-3) mediates the transient A-type potassium currents, IA, and is an important regulator of neuronal signaling. Aberrations in Kv4 channel expression and/or function are associated with several disease states, including chronic pain, epilepsy, Alzheimer’s disease, Huntington’s disease and major depressive disorder. Kv4 channels exist as ternary complexes with potassium channel interacting proteins and dipeptidyl peptidase-like proteins. Multiple ancillary proteins also associate with the Kv4 ternary complex throughout its lifetime. Little is known about the regulation of protein-protein interactions within Kv4 macromolecular complexes. Small ubiquitin-like modifier (SUMO) is a peptide that is post- translationally conjugated to lysine (K) residues on target proteins. This post-translational modification dynamically regulates protein-protein interactions. It can either promote or prevent a given interaction. This dissertation research investigated if/how post-translational SUMOylation moderated Kv4.2 protein-protein interactions to tune IA. Kv4.2 has several putative SUMOylation sites. Two conserved sites were examined in this work: K437 and K579. SUMOylating K579 increased IA when Kv4.2 existed in the ternary complex but decreased IA when Kv4.2 was expressed alone. Studies to identify the mechanism indicated that K579 SUMOylation increased IA by promoting ternary complex recycling after endocytosis, most likely by blocking an interaction with a ubiquitin ligase and thereby reducing a ubiquitin lysosome sorting signal. In contrast, when Kv4 was not incorporated into a ternary complex, K579 SUMOylation blocked an unknown protein-protein interaction that altered channel gating to reduce IA. SUMOylation at the second site, K437, had no effect when Kv4.2 was incorporated into the ternary complex, but increased the insertion of electrically silent channels when Kv4.2 was expressed alone. The mechanism underpinning increased surface expression was not examined. These dissertation findings were the first to demonstrate that Kv4.2 can be SUMOylated to regulate IA, that SUMOylation modulates Kv4.2 internalization and that the effect of SUMOylation depends upon the available interactome. INDEX WORDS: Small ubiquitin-like modifier (SUMO), Ion channel, Voltage-gated potassium channel, Kv4, A-type potassium current, Trafficking Copyright by Meghyn Alyce Welch 2021 Post-translational SUMOylation dynamically regulates voltage-gated potassium channel, Kv4.2 by Meghyn Welch Committee Chair: Deborah Baro Committee: Chun Jiang Aaron Roseberry Electronic Version Approved: Office of Graduate Services College of Arts and Sciences Georgia State University August 2021 v DEDICATION This work is dedicated to my family, especially my Mom, Dad and sister. I would not have been able to accomplish this without you all. Thank you! vi ACKNOWLEDGEMENTS First, I would like to thank my Ph.D. advisor, Dr. Deborah Baro. You have helped me become a confident researcher and have provided invaluable support and guidance over the years. Second, I would like to thank my dissertation committee – Dr. Chun Jiang and Dr. Aaron Roseberry. Thank you for your advice and support throughout my Ph.D. I would also like to thank the current and former members of the Baro lab – Lori Forster, Leslie-Anne Jansen, Anna Parker, Selin Atlas, Debasmita De, Janhavi Dubhashi, Sarah Tasneem, Justin Serna, Brenda Okonkwo, and Sasha Guillory. Specifically, I would like to say thank you to Anna Parker, Lori Forster and Leslie-Anne Jansen. You all have provided so much encouragement throughout the years. Thank you all for letting me run ideas by you, your advice, your willingness to always help, and your friendship! I would also like to thank members of the Jiang and Roseberry labs for your technical help over the years. Finally, thank you to the Brains and Behavior Fellowship program for the support over the years. vii TABLE OF CONTENTS ACKNOWLEDGEMENTS ....................................................................................................... VI LIST OF TABLES ...................................................................................................................... XI LIST OF FIGURES .................................................................................................................. XII 1 INTRODUCTION............................................................................................................. 1 1.1 Role of the transient A-type potassium current in the nervous system .................. 1 1.2 Kv4 macromolecular complex .................................................................................... 4 1.3 Small ubiquitin-like modifier is a dynamic modification that organizes protein- protein interactions ...................................................................................................... 9 1.4 Hypothesis ................................................................................................................... 14 2 CHAPTER 1: SUMOYLATING TWO DISTINCT SITES ON THE A-TYPE POTASSIUM CHANNEL KV4.2, INCREASES SURFACE EXPRESSION AND DECREASES CURRENT AMPLITUDE .................................................................... 19 2.1 Abstract ....................................................................................................................... 20 2.2 Introduction ................................................................................................................ 21 2.3 Materials and Methods .............................................................................................. 23 2.3.1 Plasmids and antibodies ......................................................................................... 23 2.3.2 Site-directed mutagenesis ....................................................................................... 24 2.3.3 Rat Brain Membrane preparations ........................................................................ 25 2.3.4 Cell culture ............................................................................................................. 25 2.3.5 Generating cell lines stably expressing wild-type and mutant Kv4.2g ................. 25 viii 2.3.6 Transient transfections ........................................................................................... 26 2.3.7 Immunoprecipitation .............................................................................................. 27 2.3.8 Western Blot ........................................................................................................... 27 2.3.9 Biotinylation assay to measure surface expression ............................................... 28 2.3.10 Whole cell patch clamp electrophysiology ............................................................. 30 2.3.11 Statistical analysis .................................................................................................. 31 2.4 Results ......................................................................................................................... 31 2.4.1 Kv4.2 is SUMOylated in the rodent brain ............................................................. 31 2.4.2 Kv4.2 channels are SUMOylated in a heterologous expression system ............... 32 2.4.3 SUMOylation of the Kv4.2 channel can be manipulated in a heterologous expression system ................................................................................................... 33 2.4.4 Increased SUMOylation of Kv4.2 channels alters the properties of IA ................ 34 2.4.5 Kv4.2 SUMOylation regulates channel surface expression ................................. 34 2.4.6 SUMOylation at K579 is responsible for the decrease in IA Gmax, while SUMOylation at K437 mediates the increase in Kv4.2 surface expression when SUMOylation is enhanced. .................................................................................... 35 2.4.7 There is a significant decrease in IA Gmax in HEK cells transiently transfected with Kv4.2g K579R compared to Kv4.2g. .............................................................. 38 2.5 Discussion .................................................................................................................... 40 2.5.1 The function of Kv4 channel SUMOylation ........................................................
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