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Orthologous Gene Swapping and Experimental Evolution Provide Novel Way to Study Essential Poxvirus Genes

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Orthologous Gene Swapping and Experimental Evolution Provide Novel Way to Study Essential Poxvirus Genes ABSTRACT Title of Dissertation: ORTHOLOGOUS GENE SWAPPING AND EXPERIMENTAL EVOLUTION PROVIDE NOVEL WAY TO STUDY ESSENTIAL POXVIRUS GENES Carey A. Stuart, Doctor of Philosophy, 2018 Dissertation directed by: Dr. Bernard Moss, Adjunct Professor, National Institutes of Health and Dr. Jeffrey DeStefano, Professor, Biological Sciences Program The transcriptional program of poxviruses is divided into early, intermediate and late phases enabled by a multisubunit DNA-dependent RNA polymerase and stage-specific transcription factors that recognize cognate promoters. Although promoter sequences are highly conserved among the different chordopoxvirus genera, the transcription factors exhibit considerable amino acid divergence that parallels the evolutionary distance of the host species. Thus, the large/small subunits of the intermediate transcription factors (ITFs) of salmon gill poxvirus, crocodilepox, canarypox, and myxoma have 23/29, 40/31, 51/38 and 58/65 % amino acid identity, respectively, to the vaccinia virus (VACV) orthologs. The purpose of the present study was to determine the functional interchangeability of the ITF subunits and their putative interactions with other elements of the transcriptional machinery. A quantitative readout of ITF function using firefly luciferase (Fluc) was obtained. The activity of the large subunit orthologs was greater than that of the small subunit orthologs, with both sets following the degree of sequence similarity in relation to VACV. The same pattern was obtained with both heterospecific (e.g., myxoma large and VACV small subunits) and homospecific (e.g., myxoma large and small subunits) pairings, suggesting inefficient interactions with other elements of the transcription system. When recombinant hybrid VACV expressing the Myxoma virus (MYXV) ortholog of the small subunit (A8) were blind passaged multiple times, their replicative abilities were enhanced. Complete genome sequencing of the virus populations revealed five mutations present in the two largest subunits of the viral RNA polymerase (RNAP) and two predicted expression-enhancing mutations around the translation initiation site of the MYXV A8 ortholog. Amplicon sequencing was used to quantify the frequency of each mutation in its respective population, which revealed that they increased as passaging occurred. This indicated a correlation with increased fitness, which then needed to be confirmed, so these mutations were all experimentally introduced into the original hybrid virus and demonstrated to enhance virus replication independently. These mutations were then characterized to determine their specific effects on the viral RNAP (vRNAP) and viral replication and transcription. This approach could have broader applications for studying essential genes in poxviruses and other viruses as well. ORTHOLOGOUS GENE SWAPPING AND EXPERIMENTAL EVOLUTION PROVIDE NOVEL WAY TO STUDY ESSENTIAL POXVIRUS GENES by Carey A. Stuart Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2018 Advisory Committee: Professor Jeffrey DeStefano, Chair Dr. Bernard Moss, Co-Chair Assistant Professor George Belov Professor James Culver Dr. Alison McBride © Copyright by Carey A. Stuart 2018 Dedication To my parents, Colin and Marcia Stuart, to whom I am eternally grateful for everything you have given me, and to Caspar, my cousins, and the rest of my family, for always supporting me. ii Acknowledgements I would like to thank my PI, Dr. Bernard Moss, for his seemingly limitless patience mentoring me. I would also like to thank the members of my committee for their guidance during my thesis. In addition, I would like to extend special thanks to Dr. Linda Wyatt, Catherine Cotter, Dr. Sara Reynolds, Dr. Seong-In Hyun, Dr. Tatiana Senkevich, Erik Zhivkoplias, and The Science Wives, who gave me an immeasurable amount of technical advice and moral support over the years. Finally, to all the past and current members of the Moss and Berger labs, past and current LVD Administrative Staff, and past and current people in the UMD BISI and Virology Programs, I say thank you for all your help and support over these last few years. iii Table of Contents Dedication ..................................................................................................................... ii Acknowledgements ...................................................................................................... iii Table of Contents ......................................................................................................... iv List of Tables ................................................................................................................ x List of Figures .............................................................................................................. xi List of Abbreviations .................................................................................................. xii Chapter 1: Introduction ................................................................................................. 1 Chapter 2: Literature Review ........................................................................................ 5 2.1 The Poxviridae .............................................................................................. 5 2.1.1 Classification............................................................................................. 5 2.1.2 Orthopoxviruses ........................................................................................ 7 2.1.3 Virion Chemical Composition .................................................................. 8 2.1.4 Virion Morphology ................................................................................... 9 2.1.5 Polypeptide Components of the Virion................................................... 10 2.1.6 Genome Organization ............................................................................. 12 2.1.7 Genome Nomenclature ........................................................................... 14 2.2 Virus Lifecycle............................................................................................ 17 2.2.1 Attachment and Entry into Cells ............................................................. 17 2.2.2 MV Entry ................................................................................................ 17 2.2.3 Attachment Proteins ................................................................................ 19 2.2.4 Entry Proteins.......................................................................................... 20 2.2.5 EV Entry ................................................................................................. 23 2.2.6 Signaling Receptors ................................................................................ 24 iv 2.2.7 Cellular Lipid Composition .................................................................... 25 2.2.8 Syncytia Formation ................................................................................. 27 2.2.9 Superinfection Inhibition ........................................................................ 28 2.3 Genome Replication.................................................................................... 29 2.3.1 Uncoating and DNA Synthesis ............................................................... 30 2.3.2 Origin of Replication .............................................................................. 31 2.3.3 DNA Replication Model ......................................................................... 32 2.3.4 Enzymes Involved in DNA Precursor Metabolism ................................ 33 2.3.5 Viral Proteins Involved in DNA Replication .......................................... 36 2.3.6 Concatemer Resolution ........................................................................... 39 2.3.7 Homologous Recombination .................................................................. 42 2.3.8 Viral DNA-Associated Proteins .............................................................. 44 2.4 Virion Morphogenesis, Maturation, and Egress ......................................... 47 2.4.1 Crescent and IV Formation ..................................................................... 48 2.4.2 VMAPs ................................................................................................... 51 2.4.3 Core Protein Association with IVs ......................................................... 55 2.4.4 D13 Scaffold and Rifampicin ................................................................. 56 2.4.5 Genome Packaging ................................................................................. 57 2.4.6 Packaging of the Transcriptional Complex............................................. 58 2.4.7 MV Formation ........................................................................................ 59 2.4.8 Intramolecular Disulfide Bonds .............................................................. 60 2.4.9 Proteolytic Processing ................................................................................ 61 2.4.10 MV Occlusion .......................................................................................... 61 2.4.11 EV Formation........................................................................................... 63 2.4.12 Wrapping of EVs ....................................................................................
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