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The Biology of the Influenza D Virus

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The Biology of the Influenza D Virus South Dakota State University Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange Electronic Theses and Dissertations 2020 The Biology of the Influenza D Virus Jieshi Yu South Dakota State University Follow this and additional works at: https://openprairie.sdstate.edu/etd Part of the Microbiology Commons Recommended Citation Yu, Jieshi, "The Biology of the Influenza D Virus" (2020). Electronic Theses and Dissertations. 3755. https://openprairie.sdstate.edu/etd/3755 This Dissertation - Open Access is brought to you for free and open access by Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange. For more information, please contact [email protected]. THE BIOLOGY OF THE INFLUENZA D VIRUS BY JIESHI YU A dissertation submitted in partial fulfillment of the requirements for the Doctor of Philosophy Major in Biological Sciences Specialization in Microbiology South Dakota State University 2020 ii DISSERTATION ACCEPTANCE PAGE Jieshi Yu This dissertation is approved as a creditable and independent investigation by a candidate for the Doctor of Philosophy degree and is acceptable for meeting the dissertation requirements for this degree. Acceptance of this does not imply that the conclusions reached by the candidate are necessarily the conclusions of the major department. Feng Li Advisor Date Volker Brozel Department Head Date Dean, Graduate School Date iii This dissertation is dedicated to my advisors, Dr. Feng Li and Dr. Dan Wang who guided and supported me over the years. iv ACKNOWLEDGEMENTS I would especially like to thank my family for giving me the constant love, support, understanding and encouragement. In particular, I would like to thank my parents, my wife, and my sisters. Without your help and support, I wouldn’t have achieved so much. I would like to thank my advisors, Dr. Feng Li and Dr. Dan Wang for guiding me, supporting me, and caring for me, in my life, study and work over the years. You have given me the warmth and comfort like at home though I am in a foreign country. You have set examples of outstanding as researchers, mentors, and instructors. I would like to thank my committee members Dr. Radhey Kaushik, Dr. Eric Nelson, and Dr. Suzette Burckhard. You provided amazing feedback and helpful guidance throughout the process of my study and research at South Dakota State University. I would like to thank the former and current Li and Wang Lab members: Dr. Chithra Sreenivasan (a friendly and knowledgeable expert in animal experiments), Dr. Chen Huang, Rongyuan Gao, Sunayana Shyam Jandhyala, Shamiq Aftab, Tirth Uprety, Dr. Ben Hause, Dr. Shaolun Zhai, Dr. Zhao Wang, Dr. Runxia Liu, Hunter Nedland, Busha Hika, Jared Wollman, Kabir Md Imtiazul, and Katherine Meyer for your great help and co-operation in my research work. v I would also like to thank Dr. Bin Zhou and Dr. Zizhang Sheng for your invaluable contributions towards my research projects. I gratefully acknowledge Dr. Steven Lawson, Aaron Singrey, Amanda Zubke and Travis Clement for your help in my animal experiments and research. I would like to thank my friends Dr. Zhanxin Wang and Zengbin Ma who have always been a huge support and encouragement to me for pursuing higher education abroad. I also wish to express my sincere thanks to Dr. Hexiao Zhang and Dr. Zhiguang Ran who recommended me to study with Dr. Feng Li in South Dakota State University. vi CONTENTS ABBREVIATIONS ............................................................................................................ x LIST OF FIGURES .......................................................................................................... xii LIST OF TABLES ........................................................................................................... xiv ABSTRACT ...................................................................................................................... xv CHAPTER 1. INTRODUCTION ....................................................................................... 1 1.1 Overview of the four types of influenza viruses ....................................................... 1 1.1.1 Taxonomy and classification .............................................................................. 1 1.1.2 Genomes and viral particles of influenza A, B, C, and D viruses ...................... 2 1.1.3 General characteristics of the four types of influenza viruses ............................ 4 1.2 The biology of the influenza D virus ........................................................................ 9 1.2.1 Epidemiology of IDV worldwide ....................................................................... 9 1.2.1.1 IDV in North America ................................................................................. 9 1.2.1.2 IDV in Europe ............................................................................................ 12 1.2.1.3 IDV in Asia ................................................................................................ 16 1.2.1.4 IDV in Africa ............................................................................................. 18 1.2.2 Pathogenicity and zoonotic potential of IDV ................................................... 19 1.2.2.1 Pathogenicity of IDV in swine and cattle .................................................. 19 1.2.2.2 Pathogenicity of IDV in other animals ...................................................... 22 1.2.2.3 Zoonotic potential of IDV .......................................................................... 23 1.2.3 Novel biology of IDV ....................................................................................... 25 vii 1.3 Research Aims......................................................................................................... 29 1.3.1 Hypothesis ........................................................................................................ 29 1.3.2 Specific Aims ................................................................................................... 30 CHAPTER 2. THE HEMAGGLUTININ-ESTERASE FUSION GLYCOPROTEIN IS A PRIMARY DETERMINANT OF THE EXCEPTIONAL THERMAL AND ACID STABILITY OF INFLUENZA D VIRUS ....................................................................... 31 2.1 Introduction ............................................................................................................. 31 2.2 Methods, results and discussion .............................................................................. 33 CHAPTER 3. DEVELOPMENT AND CHARACTERIZATION OF A REVERSE- GENETICS SYSTEM FOR INFLUENZA D VIRUS ..................................................... 42 3.1 Introduction ............................................................................................................. 42 3.2 Results ..................................................................................................................... 46 3.2.1 Generation of infectious influenza D/swine/Oklahoma/1314/2011 virus by the reverse-genetics system ............................................................................................. 46 3.2.2 Replication kinetics of continuously passaged influenza D/OK-RGS viruses at different temperatures ................................................................................................ 48 3.2.3 Receptor binding of the wild-type D/OK and rescued D/OK-RGS viruses ..... 50 3.2.4 Activity of the IDV RNP complex with PB1-E697K or PB2-L462F mutation 53 3.2.5 Recognition and transcription of the heterotypic promoter sequence by the IDV polymerase complex .................................................................................................. 57 3.3 Discussion ............................................................................................................... 62 3.4 Materials and methods ............................................................................................ 67 3.4.1 Cells, viruses, and antibodies ........................................................................... 67 viii 3.4.2 Construction of plasmids .................................................................................. 67 3.4.3 Transfection and rescue of recombinant viruses .............................................. 68 3.4.4 Virus replication assay ...................................................................................... 69 3.4.5 Hemagglutination-based competitive inhibition assay ..................................... 70 3.4.6 Minigenome replication assay .......................................................................... 70 3.4.7 Statistical analysis............................................................................................. 71 CHAPTER 4. IDENTIFICATION OF TWO RESIDUES WITHIN THE NUCLEOPROTEIN THAT CRITICALLY AFFECT THE REPLICATION FITNESS OF INFLUENZA D VIRUS ............................................................................................. 72 4.1 Introduction ............................................................................................................. 72 4.2 Results ..................................................................................................................... 75 4.2.1 The D/660 virus was superior to the D/OK virus in replication
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