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Investigation of the Roles of Ebola Virus RNA- Dependent RNA Polymerase and Its Co-Factor VP35 with the Host

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Investigation of the Roles of Ebola Virus RNA- Dependent RNA Polymerase and Its Co-Factor VP35 with the Host Investigation of the roles of Ebola virus RNA- dependent RNA polymerase and its co-factor VP35 with the host Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by Jordana Muñoz-Basagoiti May 2019 II AUTHOR’S DECLARATION Apart from the help and advice acknowledged, this thesis represents the unaided work of the author …………………………….. Jordana Muñoz-Basagoiti May 2019 This research was carried out in the Department of Infection Biology, Institute of Global health, University of Liverpool. III Acknowledgments First of all, I would like to thank my supervisors, Prof. Julian Hiscox and Prof. Miles Carroll, for having given me the opportunity of doing my PhD at the University of Liverpool and taken me to conferences in amazing places such as Crete and Singapore. Specially, thanks Julian for having guided me through the journey during these 3 years. Not less important, I would also like to thank my postdoc, my colleague and good friend Dr. Isabel García-Dorival, for her wisdom, her patience and her belief I would go through it and make it. You embraced me from the first day I arrived at Liverpool and have been my mentor in the lab and one of my pillars through my journey. Many thanks to Dr. Stuart Armstrong for his help with mass spectrometry and scientific knowledge, and to the rest of the Hiscox group and IC2 colleagues, wonderful people with whom I have shared loads of good moments in and out of work. Not related to my work, I want to thank Alessandra for being the perfect flatmate (cleaning-obsessed and a good cook who would always feed me!), and for making me laugh even in the worst of the days. Last but not least, I wanted to thank my family and friends in Catalunya. Mama, papa, Clàudia i tieta Nuri, gràcies per fer-me sentir encara part del vostre dia a dia tot i estar a 1400 km de distància. Les visites anuals, les trucades setmanals i els whatsapps diaris m’han donat força i han fet que l’anyorança no se’m mengés, sobretot a l’inici d’aquesta aventura. Ari, Eli, Tere, Brian, Alba i Carlota, gràcies per compartir les vostres vivències doctorals, pel suport des de que vem sortir de la carrera pensant que ens menjariem el món i l’amistat que n’ha sortit d’ella. IV I per acabar, no menys important, gràcies Judith per compartir gairebé tot aquest viatge al meu costat. Gràcies per confiar en mi, seguir al meu costat fins i tot a tants quilòmetres de distància i per recordar-me que sóc forta dia sí i dia també. Gràcies a tots! V Abstract Ebola virus (EBOV) was first identified in 1976 and, since then, small outbreaks have been occurring in central and West African countries. The largest EBOV outbreak until now, taking place from year 2013 to 2016, left more than 28.000 cases and 11.000 deaths. EBOV is a highly contagious and virulent pathogen with no FDA-licensed therapeutic available yet. Huge efforts are currently being made for the development of effective antiviral therapeutics and the investigation of viral evolution dynamics in correlation with its virulence. Viruses are obliged parasites of the host cell in order to accomplish every stage of their biological life cycle. For viral RNA synthesis, occurring in the cell cytoplasm, Ebola virus must interact with host proteins, which at the same time can be exploited as potential antiviral targets. In this study, co- immunoprecipitation and high-throughput label-free proteomics are used to elucidate novel protein associations between EBOV VP35, L and host factors. Biological importance of the host proteins DYNLL1 and CALM on Ebola virus life cycle is assessed by using small molecule inhibitors in an EBOV minigenome system in cellular culture, resulting in a significant decrease of viral replication when either of the cellular factors is antagonised. The study of VP35 is taken further and the phenotypic changes on the protein functionality during the early beginning of the 2013-2016 West African outbreak are characterised, demonstrating slight differences on the viral protein performance that could help understand better Ebola virus virulence. Overall, this thesis provides a better understanding of the interactions that Ebola virus establishes with its host, the implications that single mutations can have on viral proteins functionality and the EBOV pathogenesis. VI Table of contents AUTHOR’S DECLARATION .................................................................................... III Acknowledgments ............................................................................................... IV Abstract ............................................................................................................... VI Table of contents ................................................................................................ VII List of figures ..................................................................................................... XIII List of abbreviations ........................................................................................ XVIII Chapter 1: Introduction to Ebola virus ................................................................ 23 1.1. Introduction to the Ebola virus biology .................................................... 24 1.1.1. Taxonomy and classification ............................................................. 24 1.1.1.1. Order Mononegavirales ............................................................ 24 1.1.1.2. Family Filoviridae ...................................................................... 25 1.1.2. Genome organisation and Ebola virus genetics ................................ 27 1.1.3. Mutation rate and defecting interfering particles (DIPs) .................. 28 1.1.4. Ebolavirus replication cycle ............................................................... 28 1.1.5. Attachment and entry ....................................................................... 29 1.1.6. Transcription and replication ............................................................ 30 1.1.7. Virion assembly and release ............................................................. 30 1.1.8. Viral proteins ..................................................................................... 31 1.1.1.3. Nucleoprotein (NP) ................................................................... 32 1.1.1.4. Viral protein 35 (VP35) .............................................................. 32 1.1.1.5. Viral protein 40 (VP40) .............................................................. 32 1.1.1.6. Glycoprotein (GP) ...................................................................... 33 1.1.1.7. Viral protein 30 (VP30) .............................................................. 33 1.1.1.8. Viral protein 24 (VP24) .............................................................. 34 1.1.1.9. RNA-dependent RNA polymerase (L) ........................................ 34 1.2. Reverse genetics ....................................................................................... 35 VII 1.2.1. History of reverse genetics and replicon systems ............................. 35 1.2.2. EBOV replicon system ....................................................................... 36 1.3. EBOV virus-like particles (VLP) .................................................................. 38 1.4. Ebola Virus Disease ................................................................................... 38 1.4.1. EBOV discovery, epidemiology, economic and social impact ........... 39 1.4.1.1. EBOV discovery ......................................................................... 39 1.4.1.2. Epidemiology ............................................................................. 39 1.4.1.3. Economic and social impact ...................................................... 40 1.4.2. Reservoirs, transmission and persistence ......................................... 41 1.4.3. Pathogenesis and host immune response ........................................ 41 1.4.4. EBOV suppression of host antiviral responses .................................. 43 1.5. Therapeutics for EVD ................................................................................ 44 1.5.1. Current state of vaccine development .............................................. 44 1.5.2. Current state of treatment development ......................................... 45 1.5.2.1. Small molecule inhibitors .......................................................... 45 1.5.2.1. Immune-based therapeutics ..................................................... 45 1.6. Research aims and objectives ................................................................... 47 Chapter 2: Materials and Methods ..................................................................... 48 2.1. Recombinant protein constructs .............................................................. 49 2.1.1. Fluorescent fusion vector cloning ..................................................... 49 2.1.1.1. EBOV EGFP-VP35 and VP35-EGFP, mutated VP35-encoding vectors and pL-mCherry ................................................................................ 49 2.2. Analysis of 2014-2015 EBOV VP35 sequences .......................................... 51 2.3. DNA methods ............................................................................................ 51 2.3.1. Transformation of cells ..................................................................... 51 2.3.1.1. DH5α competent cells ..............................................................
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