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Inhibiting Phosphorylation and Aggregation of Tau Protein Using R Domain Peptide Mimetics a Dissertation Presented to the Facul

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Inhibiting Phosphorylation and Aggregation of Tau Protein Using R Domain Peptide Mimetics a Dissertation Presented to the Facul Inhibiting Phosphorylation and Aggregation of Tau Protein Using R Domain Peptide Mimetics A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Najah A. Alqaeisoom August 2019 © 2019 Najah A. Alqaeisoom. All Rights Reserved. 2 This dissertation titled Inhibiting Phosphorylation and Aggregation of Tau Protein Using R Domain Peptide Mimetics by NAJAH A. ALQAEISOOM has been approved for the Department of Chemistry and Biochemistry and the College of Arts and Sciences by Justin M. Holub Assistant Professor of Biochemistry Joseph Shields Interim Dean, College of Arts and Sciences 3 ABSTRACT ALQAEISOOM, NAJAH A., Ph.D., August 2019, Chemistry Inhibiting Phosphorylation and Aggregation of Tau Protein Using R Domain Peptide Mimetics Director of Dissertation: Justin M. Holub Tau protein plays a crucial role in stabilizing microtubules inside neuronal axons and maintaining the structural integrity of neurons. Binding of tau to microtubules at tau repeat domains (R) is regulated by phosphorylation. This phosphorylation is regulated by a family of enzymes called kinases. Under pathological conditions, tau is hyperphosphorylated by elevated activity of kinases such as the microtubule affinity- regulating kinase (MARK) proteins, leading to complete detachment of tau, microtubule collapse and ultimately, neuronal cell death. The free, hyper-phosphorylated tau proteins aggregate into insoluble prion-like oligomers which have been implicated in neurodegenerative diseases, including Alzheimer's disease (AD) and frontotemporal dementia. There is currently no treatment to prevent the progression of AD; all medications available today only reduce the symptoms of the disease. Moreover, using small molecule kinase inhibitors as treatment can cause serious negative side effects because of their lack of specificity. The research outlined in this work aims to develop a metabolically stable, selective peptide-based MARK kinase inhibitor that targets MARK proteins. This peptide-based inhibitor, designated tR1, was designed as a direct sequence memetic of the microtubule-binding R1 repeat domain of tau. Here, we show that tR1 4 peptides can inhibit MARK2 activity and reduce the level of tau phosphorylation in vitro and in cultured rat primary cortical neurons. In the second segment of this project, we attempted to inhibit tau aggregation in vitro using peptide-based aggregation inhibitors. Here, we synthesized peptides designated (an-R3, PHF6, and PHF6*) which mimic nucleating sites in the microtubule binding repeat domain of full-length tau. We hypothesized that these peptides would associate with tau protein and block further tau aggregation. We assessed the ability of these three peptides to inhibit tau aggregation using in vitro heparin-induced tau aggregation assay. The aggregation products were analyzed by SDS-PAGE analysis and by circular dichroism (CD) spectropolarimetry. We provide evidence that the nucleation site located in R3 repeat domain of tau is more prone to aggregation than in R2 repeat domain. Moreover, we show that amphiphilic peptide sequences, in which polar or charged residues alternate with hydrophobic amino acids, are important for tau nucleation and aggregation. 5 DEDICATION I dedicated this work to my parents, husband and my family 6 ACKNOWLEDGMENTS First, I would like to acknowledge my advisor, Dr. Justin Holub for his support, patience, understanding, and his step by step guidance. I also would like to thank my dissertation committee members, Dr. Marcia Kieliszewski, Dr. Robert Colvin, Dr. Jana Houser, and Dr. Jixin Chen for their time, efforts and their valuable comments to edit and improve my work. Special thanks to the Saudi Arabian Cultural Mission (SACM) for their financial support and covering all the cost of my study at Ohio University. I also would like to sincerely thank my lab mates: Tang Tang, Ranju Pokhrel, Chang Xu, Nahar Khairun, and Maya Sattler for their kindness, care, assistance, support and for creating a friendly and convenient research environment. Thanks to Dr. Michael Held group and Dr. Jennifer Hines group who always help me whenever I ask them for help. I acknowledge my collaborator Dr. Cheng Qian form Dr. Robert Colvin group for his cooperation with me on the work reported in Chapter 1. His significant contributions were of great help in getting the results of my first project. Special thanks to Danushka Arachchige from Dr. Holub’s group for assisting in my research and helping me when I was not able to work in the lab. Finally, I would like to thank my family, my husband, and my friends for their love, support and for wishing me the success. 7 TABLE OF CONTENTS Page Abstract ...........................................................................................................................3 Dedication .......................................................................................................................5 Acknowledgments ...........................................................................................................6 List of Tables................................................................................................................. 10 List of Figures ............................................................................................................... 11 List of Abbreviations ..................................................................................................... 13 Chapter 1: Introduction .................................................................................................. 15 The Discovery of Tau Protein and its Role in Stabilizing Microtubules .................... 15 Biochemical Characterization of Tau ....................................................................... 15 Pathological Tau, Causes and Consequences ............................................................ 17 Hyperphosphorylation of Tau Protein and the Formation of NFTs ........................... 19 Pathological Tau Transmission ................................................................................ 23 Therapeutic Strategies for the Inhibition of Tauopathies........................................... 25 Inhibiting Tau Hyperphosphorylation ................................................................. 26 Increasing of Microtubule Stability .................................................................... 28 Increasing Tau Clearance ................................................................................... 30 Tau Immunotherapy ........................................................................................... 33 Active Immunization .................................................................................... 33 Passive Immunization................................................................................... 34 Inhibition of Tau Aggregation ............................................................................ 35 Inhibiting Tau Misfolding ............................................................................ 37 Disrupting Tau Dimerization ........................................................................ 38 Accelerating Tau Aggregation ...................................................................... 39 β-sheet Breakers ........................................................................................... 39 Peptide-Based Therapeutic for Tauopathies ........................................................ 41 MARK Protein Activity, Inhibition by Small Molecules Versus Peptides ........... 43 Chapter 2: Inhibiting Tau Phosphorylation Using Human Tau Peptide-Based R Domain Mimetics ....................................................................................................................... 46 Introduction ............................................................................................................. 46 Materials .................................................................................................................. 49 8 Methods ................................................................................................................... 51 Peptide Preparation ............................................................................................ 51 Peptide Synthesis ......................................................................................... 51 Labeling of Synthesized Peptides ................................................................. 52 Capping of Synthesized Peptides .................................................................. 52 Cleavage of the Peptides from the Resin ....................................................... 53 Purification and Quantification of Peptides ................................................... 53 Characterization of Peptides by Analytical HPLC and Mass Spectrometry ... 54 Protein Preparation ............................................................................................. 54 MARK2 Preparation .................................................................................... 54 hTau K18 Preparation .................................................................................. 56 Structural Analysis for MARK2 and hTau K18 by Circular Dichroism ......... 58 Evaluating the In Vitro Activity of Recombinant MARK2 ........................... 59 In Vitro tR1 Stability Assessment .....................................................................
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