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IDENTIFICATION OF A VIRAL DETERMINANT OF VIRULENCE IN ROSS RIVER VIRUS THAT MODULATES VIRAL REPLICATION AND FITNESS IN DISPARATE HOSTS by HENRI J JUPILLE B.S., Colorado Mesa University, 2005 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirements for the degree of Doctor of Philosophy Microbiology Program 2013 This thesis for the Doctor of Philosophy degree by Henri J. Jupille has been approved for the Microbiology Program by Dave Barton, Chair Thomas Morrison, Advisor Kathryn Holmes Caroline Kulesza David Beckham Date: 08/08/13 ii Jupille, Henri J. (Ph.D., Microbiology) Identification of a viral determinant of virulence in Ross River virus that modulates viral replication and fitness in disparate hosts. Thesis directed by Assistant Professor Thomas Morrison. ABSTRACT Alphaviruses such as Ross River virus (RRV) and chikungunya virus cause debilitating and often chronic rheumatic disease in humans and are responsible for explosive epidemics which cause millions of cases of musculoskeletal inflammatory disease. Despite these outbreaks, the pathogenesis of these viruses is poorly understood. Our studies identified an RRV strain (DC5692) which, in contrast to the T48 strain, failed to cause musculoskeletal inflammation in mice. Using chimeric virus studies based on the DC5692 and T48 strains, we identified unique virulence determinants within both the nsP1 and PE2 coding regions responsible for attenuation. Further study of these chimeric viruses showed that the specific mechanism of attenuation was different for the mutations in nsP1 and PE2, suggesting that they affect different aspects of the viral replication cycle. Through further study of the PE2 region, we identified a tyrosine (Y) to histidine (H) mutation at E2 position 18 (E2 Y18H) as a major attenuating mutation in mice. In vitro characterization studies showed that the E2 Y18H mutation caused a cell-type specific replication and fitness defect whereby a tyrosine conferred a large fitness advantage in mammalian cells, leading to enhanced viral replication in these cell types. In contrast, we showed a histidine at E2 position 18 iii conferred a fitness and replication advantage in mosquito cells. Additional studies showed that the E2 Y18H mutation increased release of non-infectious virions from mammalian cells. Taken together, these studies represent the first published reports of novel viral determinants of alphavirus-induced musculoskeletal disease located within the nsP1 and PE2 coding regions. Furthermore, the identification of a tyrosine or histidine residue at E2 position 18 in all alphaviruses in the Semliki Forest antigenic complex represents the first time a naturally occurring virulence determinant has been identified within the N-flap domain of E2. Subsequent studies showing that the residue at position 18 affects viral fitness suggest that it may be acting as a “switching residue” during replication in disparate hosts. Finally, identification of a late stage specific replication defect in mammalian cells suggests an important and novel role for the N-flap domain of E2 during the assembly of alphavirus virions. The form and content of this abstract are approved. I recommend its publication. Approved: Thomas Morrison iv DEDICATION I dedicate this work to my wife Marybeth, who has been an unwavering source of love and support throughout this entire process. Additionally, I would also like to dedicate this work to my parents who have supported me fully on my journey to this point in my life. I cannot imagine doing this without you all and am forever grateful for all the love and support you have given me over the years. v ACKNOWLEDGMENTS I would first like to thank the members of my committee for their many insightful questions and helpful advice throughout my research progression. I would also like to thank all past and present members of the Morrison Lab for all their assistance. I would like to extend special thanks to my mentor Dr. Morrison for allowing me the opportunity to join his lab, and for helping to train me to become a successful scientist. Without his patience and guidance, I would not be where I am today. I thank the many collaborators whose contributions allowed my research to move forward. Specifically, I would like to thank Drs. John Aaskov and Michael Rossmann for providing the anti-E2 monoclonal antibody. I would also like to acknowledge the funding sources at the National Institutes of Health. Finally, I would like to acknowledge the students, faculty and staff of the Microbiology Department for all their guidance and support over the years. vi TABLE OF CONTENTS CHAPTER I. INTRODUCTION ............................................................................................................ 1 The Alphaviruses ................................................................................................................. 1 The Arthritogenic Alphaviruses........................................................................................... 5 Chikungunya Virus. ....................................................................................................... 5 O’nyong-nyong Virus. ................................................................................................... 7 Ross River Virus. ........................................................................................................... 8 Sindbis Virus. ................................................................................................................ 8 Mayaro Virus. ............................................................................................................... 9 Rheumatic Disease in Humans During Alphavirus Infection ............................................. 10 Alphavirus Pathogenesis ................................................................................................... 13 Animal Models of Alphavirus-induced Rheumatic Disease .............................................. 16 Non-Human Primate Model of CHIKV Infection. ........................................................ 16 Mouse Model of CHIKV Pathogenesis in IFN Deficient Mice ..................................... 17 Other Animal Models. ................................................................................................ 17 Mouse Model of RRV- and CHIKV-induced Rheumatic Disease in Mice. ................... 18 Alphavirus Virions ............................................................................................................. 18 Alphavirus Genome........................................................................................................... 19 Alphavirus Gene Products and Functions ......................................................................... 23 Nonstructural Polyprotein Translation and Processing. ............................................ 23 nsP1. ..................................................................................................................... 24 vii nsP2. ..................................................................................................................... 24 nsP3. ..................................................................................................................... 25 nsP4. ..................................................................................................................... 26 Structural Polyprotein Translation and Processing. ................................................... 27 Capsid. .................................................................................................................. 28 PE2. ...................................................................................................................... 29 E1. ........................................................................................................................ 31 6K. ........................................................................................................................ 31 The Alphavirus Replication Cycle ...................................................................................... 32 Alphavirus Entry and Fusion Process.......................................................................... 32 Replication of Alphavirus RNA and Nonstructural Protein Processing. ..................... 33 Alphavirus Structural Protein Translation and Virion Assembly. ............................... 35 Alphavirus Determinants of Virulence .............................................................................. 38 Overview of Dissertation .................................................................................................. 39 II. MATERIALS AND METHODS ....................................................................................... 42 Viruses ............................................................................................................................... 42 Construction of Virus cDNAs ............................................................................................. 43 Site Directed Mutagenesis ................................................................................................ 45 Cells ................................................................................................................................... 46 RNA Infectivity Assays ....................................................................................................... 47 In Vitro Nonstructural Protein Processing .......................................................................
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