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Structure-Function Analysis of the DNA Damage Repair Complex STR in Saccharomyces Cerevisiae Jessica Ashley Kennedy University of South Florida, [email protected]

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Structure-Function Analysis of the DNA Damage Repair Complex STR in Saccharomyces Cerevisiae Jessica Ashley Kennedy University of South Florida, Kennedy5@Mail.Usf.Edu University of South Florida Scholar Commons Graduate Theses and Dissertations Graduate School January 2015 Structure-Function Analysis of the DNA Damage Repair Complex STR in Saccharomyces cerevisiae Jessica Ashley Kennedy University of South Florida, [email protected] Follow this and additional works at: http://scholarcommons.usf.edu/etd Part of the Biology Commons Scholar Commons Citation Kennedy, Jessica Ashley, "Structure-Function Analysis of the DNA Damage Repair Complex STR in Saccharomyces cerevisiae" (2015). Graduate Theses and Dissertations. http://scholarcommons.usf.edu/etd/5713 This Dissertation is brought to you for free and open access by the Graduate School at Scholar Commons. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Scholar Commons. For more information, please contact [email protected]. Structure-Function Analysis of the DNA Damage Repair Complex STR in Saccharomyces cerevisiae by Jessica A. Kennedy A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Cell and Molecular Biology Department of Cell Biology, Microbiology, and Molecular Biology College of Arts and Sciences University of South Florida Co-Major Professor: Kristina Schmidt, Ph.D. Co-Major Professor: Gary Daughdrill, Ph.D. Stanley Stevens, Ph.D. Patrick Bradshaw, Ph.D. Date of Approval: June 29, 2015 Keywords: RecQ Helicases, Intrinsic Disorder, Unstructured Proteins Copyright © 2015, Jessica A. Kennedy DEDICATION I would like to dedicate this dissertation to all those that played a hand in educating me to this point. It is only because of their dedication to education that I am the student I am today. I owe the faculty of Sanders Memorial Elementary, Pine View Middle, Land O’ Lakes High, and University of South Florida for the tools and drive to reach this point. Thank you for challenging me and keeping me hungry. I would also like to dedicate this to my parents, Frederick and Nancy Kennedy, and particularly to my sisters Erin Kennedy and Mary Ghazarian, who are the perfect partners in academic crime. Thank you for listening to my complaints on the most rough days of the bench. Having someone who knows the struggle to succeed matters (even if they don’t really know what I do. C-3PO is not a gene). Lastly, I dedicate at least a small part of this to Amy Morrison and Charles Slowik, who kept me fed throughout the writing process. Your stress-eating sessions of delicious food make the whole process just a little easier. You are the truest friends. TABLE OF CONTENTS List of Tables ................................................................................................................... v List of Figures ................................................................................................................. vi List of Acronyms .............................................................................................................. ix Abstract .......................................................................................................................... xii Chapter One: Introduction ............................................................................................... 1 Founding Member of the RecQ Family of Helicases ............................................ 1 RecQ Helicase Structure and Function ................................................................ 2 RecQ Helicase in S. cerevisiae, Sgs1 .................................................................. 5 Characterization of the Δsgs1 Phenotype .................................................. 6 Role of Sgs1 in DNA Repair ...................................................................... 7 N-Terminal and Putative Sgs1 Protein/Protein Interactions ..................... 11 The RTR Complex: RecQ Interaction with Top3 and Rmi1 ...................... 14 Role and Interaction of Topoisomerase III (Top3) in RTR Complex ............................................................................... 14 Role and Interaction of Rmi1 in the RTR Complex .................. 15 RTR Complex Member in Humans: Rmi2 ................................ 17 RecQ Orthologs in Humans ................................................................................ 18 RecQL1 .................................................................................................... 18 RecQL5 .................................................................................................... 19 RecQL4 .................................................................................................... 21 WRN ........................................................................................................ 24 BLM ......................................................................................................... 30 Intrinsically Disordered Proteins/Regions (IDP/Rs) ............................................ 37 Characteristics of IDPs ............................................................................ 38 Prevalence of IDPs .................................................................................. 40 Thermodynamic Characteristics of IDPs .................................................. 40 Functional Advantage of IDPs ................................................................. 41 Evolutionary Advantage of IDPs .............................................................. 44 Examples of Intrinsic Disorder ................................................................. 45 Disorder in S. cerevisiae .......................................................................... 47 Disorder in RecQ Helicases ..................................................................... 47 References ......................................................................................................... 50 i Chapter Two: Materials and Methods............................................................................ 69 Site-Directed Mutagenesis ................................................................................. 69 Plasmid Isolation from Bacteria .......................................................................... 73 Gross Chromosomal Rearrangement (GCR) Assay ........................................... 73 Trichloroacetic Acid (TCA) Extraction ................................................................. 74 SDS-PAGE and Western Blot Analysis .............................................................. 74 Hydroxyurea Sensitivity Assay ........................................................................... 75 Yeast Mating for Diploids .................................................................................... 75 Lithium Acetate (LiAc) Transformation ............................................................... 76 Media Types ...................................................................................................... 77 References ......................................................................................................... 78 Chapter Three: A Transient α-Helical Molecular Recognition Element in the Disordered N-terminus of the Sgs1 Helicase is Critical for Chromosome Stability and Binding of Top3/Rmi1 ............................................................................ 79 Abstract .............................................................................................................. 79 Introduction ......................................................................................................... 80 Materials and Methods ....................................................................................... 83 Expression and Purification of Peptides for NMR Spectroscopy .............. 83 NMR Analysis .......................................................................................... 84 Hydroxyurea Hypersensitivity Assay ........................................................ 86 Top3 and Rmi1 Binding Assay ................................................................. 86 Gross-Chromosomal Rearrangement Assay ........................................... 88 Preparation of Yeast Whole-Cell Extracts by Trichloroacetic Acid Extraction ........................................................................................... 88 Results ............................................................................................................... 89 The First 125 Residues of the Structurally Disordered N-terminus of Sgs1 Contain Two Transient α-helices ............................................ 89 Functional Mapping of α-helices by Proline Mutagenesis ........................ 92 Disruption of Transient α-helices Impairs Complex Formation Between Sgs1, Top3 and Rmi1 ........................................................... 95 Integrity of Transient α-helices is Critical for Maintaining Chromosomal Stability ......................................................................... 96 Discussion .......................................................................................................... 97 References ....................................................................................................... 102 Figures and Tables ........................................................................................... 107 Chapter Four: The Role of Protein Disorder in Chromatin Processes of S.cerevisiae .............................................................................................................. 120 Introduction ......................................................................................................
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