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Punta Toro Virus Infection in Mice: Strain Differences in Pathogenesis and Regulation of Interferon Response Pathways

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Punta Toro Virus Infection in Mice: Strain Differences in Pathogenesis and Regulation of Interferon Response Pathways Utah State University DigitalCommons@USU All Graduate Theses and Dissertations Graduate Studies 5-2009 Punta Toro Virus Infection in Mice: Strain Differences in Pathogenesis and Regulation of Interferon Response Pathways Michelle Mendenhall Utah State University Follow this and additional works at: https://digitalcommons.usu.edu/etd Part of the Biology Commons Recommended Citation Mendenhall, Michelle, "Punta Toro Virus Infection in Mice: Strain Differences in Pathogenesis and Regulation of Interferon Response Pathways" (2009). All Graduate Theses and Dissertations. 425. https://digitalcommons.usu.edu/etd/425 This Thesis is brought to you for free and open access by the Graduate Studies at DigitalCommons@USU. It has been accepted for inclusion in All Graduate Theses and Dissertations by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. PUNTA TORO VIRUS INFECTION IN MICE: STRAIN DIFFERENCES IN PATHOGENESIS AND REGULATION OF INTERFERON RESPONSE PATHWAYS by Michelle Mendenhall A thesis submitted in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE in Bioveterinary Science Approved: ________________________ ________________________ Brian B. Gowen Dale L. Barnard Major Professor Committee Member ________________________ ________________________ Lee Rickords Kenneth L. White Committee Member Department Head ________________________ Byron R. Burnham Dean of Graduate Studies UTAH STATE UNIVERSITY Logan, Utah 2009 ii ABSTRACT Punta Toro Virus Infection in Mice: Strain Differences in Pathogenesis and Regulation of Interferon Response Pathways by Michelle Mendenhall, Master of Science Utah State University, 2009 Major Professor: Brian B. Gowen Department: Animal, Dairy and Veterinary Science The Adames strain of Punta Toro virus (PTV-A) causes acute hepatic disease in hamsters and mice similar to that seen in natural Rift Valley fever virus (RVFV) infection, while the Balliet strain (PTV-B) is apathogenic. The ability of PTV-A to suppress the interferon (IFN) response has been demonstrated in hamsters and is thought to be a contributing factor to PTV-A’s pathogenicity in hamsters. PTV-B is not assumed to exhibit this IFN-antagonistic activity, as it stimulates production of significantly higher IFN-β levels. To elucidate the role of IFN in resistance of mice to PTV-B infection, we utilized mice deficient in a critical IFN signaling protein, STAT-1. We found that these mice were drastically more susceptible to PTV-B, which caused 100% lethality compared to 0% in their wild-type counterparts. STAT-1 deficient mice were also more susceptible to PTV-A, as these mice succumbed to infection significantly earlier than wildtype mice (p=0.0058). We sought to determine whether PTV-A’s IFN-antagonistic mechanism is iii functional in mice by examining expression of IFN-β in primary macrophages infected with either strain. We found that IFN-β protein concentration is higher in samples taken from PTV-B-infected cells. We employed quantitative PCR arrays specific to IFN signaling and response pathways to evaluate changes in gene expression throughout the course of infection with either virus strain. We found several genes with differentially regulated expression between PTV-A- and PTV-B-infected macrophages, including Ifnβ1 and multiple Ifnα subtypes. Also, several genes coding for inflammatory and chemotactic molecules, Cxcl11, Cxcl10, Cxcl9, Vcam1, and Il6, demonstrated increased expression in PTV-B samples compared to PTV-A. Of particular interest, Isg20, a 3’-5’ exonuclease with specificity for single-stranded RNA, was stimulated ~2-fold higher by PTV-B, and Iigp1, from the family of GTPases associated with host defense against intracellular pathogens, was stimulated ~2.7-fold higher by PTV-B. The individual functions of each of these genes in mouse resistance to PTV-B could be a focus of future studies to better understand essential host defense mechanisms to phleboviral infection. (92 pages) iv ACKNOWLEDGMENTS I wish there was a way to thank every person who has influenced or helped me along the way during the course of this research. I would, however, like to acknowledge some of the people without whom it would not have been possible. First, the Institute for Antiviral Research, the National Institute of Health, and the Center for Integrated Biosystems Research Program for supporting and funding the project. I am very appreciative of my graduate committee, Brian Gowen, Dale Barnard, and Lee Rickords for their invaluable guidance and time. I am especially grateful to Brian for his unfailing patience and encouragement. I would also like to acknowledge all those who helped with set up, data collection, analysis, and writing of the results for the project, particularly Isaac Wong and his technicians and Ramona Skirpstunas of the Ross A. Smart Veterinary Diagnostic Lab. Special thanks to Kie-Hoon Jung, Quinton Winger, and Jillian Guttormsen for their endless advice and support. Finally, I wish to express my gratitude to my family and friends who provided both the outlet and the extra push when I needed them. Sincere thanks to you all! Michelle Mendenhall v CONTENTS Page ABSTRACT ....................................................................................................................... ii ACKNOWLEDGMENTS ................................................................................................ iv LIST OF TABLES ............................................................................................................ vi LIST OF FIGURES ......................................................................................................... vii CHAPTER 1. INTRODUCTION ......................................................................................1 LITERATURE REVIEW .....................................................................3 OBJECTIVES .....................................................................................25 2. METHODS AND RESULTS ....................................................................27 EXPERIMENTAL DESIGN...............................................................27 MATERIALS AND METHODS.........................................................28 RESULTS............................................................................................32 3. CONCLUSION .........................................................................................55 LITERATURE CITED .....................................................................................................64 APPENDICES ..............................................................................................................73 vi LIST OF TABLES Table Page 1 Disease parameters in STAT-1 KO vs. WT mice at time of death ......................44 A-1 Expression of IFN and related genes at 16 hours p.i............................................74 A-2 Expression of IFN and related genes at 24 hours p.i............................................75 A-3 Expression of IFN and related genes at 36 hours p.i............................................77 A-4 Expression of IFN and related genes at 48 hours p.i............................................79 vii LIST OF FIGURES Figure Page 1 Survival of C57BL/6J mice infected with PTV-A or PTV-B ..............................33 2 Pathology of PTV infection in mice.....................................................................35 3 Mean virus titers in tissue samples from PTV-infected C57BL/6J mice .............37 4 Serum ALT levels of C57BL/6J mice infected with PTV strains........................39 5 Serum interferon levels in C57BL/6J mice infected with PTV strains ................40 6 Survival of PTV-infected STAT-1 knockout mice ..............................................42 7 Systemic and tissue virus and ALT in PTV-A infected STAT-1 knockout vs. wildtype mice..................................................................................................45 8 PTV growth in IFN-incompetent Vero 76 and IFN competent TG-elicited PEC cell cultures ..................................................................................................47 9 IFN-β induction by PTV strains in TG-elicited PECs .........................................49 10 Expression of genes with significant differences between PTV-A and PTV-B infected macrophages at one or more time points ...................................51 11 Network of immune response genes associated with genes differentially expressed between PTV-A and PTV-B-infected macrophages at 24 hours p.i..........................................................................................................................54 A-1 Expression of IFN and related genes at 16 hours p.i............................................81 A-2 Expression of IFN and related genes at 24 hours p.i............................................82 A-3 Expression of IFN and related genes at 36 hours p.i............................................83 A-4 Expression of IFN and related genes at 48 hours p.i............................................84 1 CHAPTER 1 INTRODUCTION Rift valley fever (RVF) is an acute, febrile disease of domestic ruminants, especially sheep, cattle and goats, which can also be transmitted to humans. The disease had caused extensive losses of sheep and cattle in Kenya before the turn of the century, as well as a liver disease in humans during certain wet years (Shimshony and Barzilai, 1983; Swanepoel and Coetzer, 1994), but the causative agent was
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