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Surveillance of Influenza a Virus in Environmental Ice and Water Samples

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Surveillance of Influenza a Virus in Environmental Ice and Water Samples i SURVEILLANCE OF INFLUENZA A VIRUS IN ENVIRONMENTAL ICE AND WATER SAMPLES Gang Zhang A dissertation Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY December 2007 Committee: Scott Rogers, Advisor Robert Midden Graduate Faculty Representative Carmen Fioravanti George Bullerjahn John Castello ii ABSTRACT Scott O. Rogers, Advisor Influenza A virus (IAV) is an important human pathogen. IAV infects humans and also a variety of other warm-blooded animals, including various domestic and wild fowl, many domestic and wild mammals. In wild aquatic birds, IAVs primarily are enteric viruses. IAV may have reached evolutionary stasis in birds. As the primary reservoir of all IAV subtypes, wild aquatic fowl play an important role in the ecology of IAV, by maintaining various subtypes of IAV and continuously transmitting genes and viral strains to other host species. Among wild aquatic birds, transmission of IAV occurs through the “oral-fecal” pathway. Environmental ice is a good reservoir for preserving microorganisms alive for long periods of time. In this study, we hypothesized that environmental ice was a good abiotic reservoir for preserving IAV virions shed by wild birds. IAV H1 gene sequences were detected in ice and water samples collected from northeastern Siberian lakes (Lake Park, Lake Edoma). After cloning and sequencing, 83 unique sequences were derived from a Lake Park ice sample and 1 unique sequence was derived from a Lake Edoma water sample. Phylogenetic analysis indicated that the sequences were heterogenous. The sequences shared similarities to IAVs isolated from humans in the 1930s in Europe and in the 1960s in Japan. Through this study, a procedure for developing high sensitivity PCR-based methods for virological surveillance of IAV was established. Although no evidence on the viability of the IAV contained in environmental ice and water was obtained, our results indicated that IAV could be preserved alive in the lake ice. This is supported by the fact that IAV RNA fragments of iii more than 600 bp were found in the ice. Therefore, environmental ice might act as the abiotic reservoir for infectious IAV, and possibly many other waterborne viruses. iv ACKNOWLEDGMENT I want to express my sincere appreciation to my major advisor, Dr. Scott O. Rogers, for his guidance, kindness, and patience. What I learned from him is more than doing research. The days I spend in his lab are an inerasable memory in my life. I also want to express my gratitude to my committee members. Thank you for arranging time to attend my presentations and give valuable suggestions to my research. Thanks for Dr. Fioravanti for using his equipment. I appreciate Dr. John Castello for his very careful reading of the dissertation, and a lot of detailed revisions and critical comments. Thanks to my friends and labmates, Seung-Geuk Shin, Vincent Theraisnathan, Ram Satish Veerapaneni, Tom D’Elia, Lorena Harris, Zeynep Kocer, Farida Sidiq, and America Vicol for their friendship and the good time we spend together. Special thanks to Seung- Geuk Shin for the help he gave me when I just joined the lab. I want to thank my parents for the everlasting love and support. I want to express my sincere appreciation to my girlfriend Chia-Jui Tsai for her love and support and understanding. v TABLE OF CONTENTS Page CHAPTER I. LITERATURE REVIEW............................................................................... 1 An introduction to IAV.............................................................................................. 3 The structure of an IAV virion................................................................................... 4 The life cycle of IAV ….. .......................................................................................... 16 Influenza pandemics .................................................................................................. 20 The ecology of IAV ................................................................................................... 21 Human IAV: appearance, disappearance and reappearance...................................... 23 The perpetuation of IAV in environmental ice and water ......................................... 25 The evolution of IAVs ............................................................................................... 26 Predict the evolutionary trend and upcoming pandemics.......................................... 33 Methods in IAV surveillance..................................................................................... 34 Phylogenetic analysis methods .................................................................................. 35 Literature cited…. …….. …….. ……....................................................................... 41 CHAPTER II. SURVEILLANCE OF INFLUENZA A VIRUSES IN ENVIRONMENTAL ICE AND WATER SAMPLES ......................................................... 58 INTRODUCTION………………. ........................................................................................ 59 MATERIALS AND METHODS………………................................................................... 62 Primer design ............................................................................................................ 62 IAV strains ……………………………………………………………………...…. 63 Measurement of primer sensitivity ........................................................................... 63 vi Ice and water samples ................................................................................................ 63 Processing of samples…………………………………………………………........ 64 RT-PCR, semi-nested/nested-PCR, and sequencing …………………………. ....... 65 RESULTS………………. ..................................................................................................... 68 Primer selection………………................................................................................. 68 Assays on environmental ice and water samples………………............................... 68 DISCUSSION………………................................................................................................ 72 LITERATURE CITED………………. ................................................................................. 76 CHAPTER III. EVIDENCE OF INFLUENZA A VIRUS RNA IN SIBERIAN LAKE ICE……………………….. ................................................................................................... 81 INTRODUCTION……… .........................................................................................……… 82 MATERIALS AND METHODS…...........................................................................……… 84 Ice and water samples… ................................................................................……… 84 Sample processing….....................................................................................……… 87 Molecular assays…........................................................................................……… 88 Data analysis ............................................................................................................ 90 RESULTS ………….. ...............................................................................................……… 91 DISCUSSION……… ………..........................................................................................….. 97 LITERATURE CITED…..… ..........................................................................................….. 101 vii CHAPTER IV. SUPPLEMENT……………………….. ..................................................... 106 LITERATURE CITED .......................................................................................................... 110 APPENDIX A. GENBANK ACCESSION NUMBERS. APPENDIX B. Zhang, G., D. Shoham, D. Gilichinsky, S. Davydov, J. D. Castello, and S. O. Rogers.2006. Evidence of Influenza A Virus RNA in Siberian Lake Ice. J. Virol. 80(24), 12229-12235. viii LIST OF FIGURES Figure Page CHAPTER I 1 Diagram of an IAV virion.......................................................................................... 5 2 Conserved ends of vRNA segments .......................................................................... 5 3 Schematic representation of the bicistronic mRNA for PB1 and PB1-F2 protein .... 8 4 Schematic representation of HA protein and the cleavage site.................................. 8 5 Schematic representation for the mRNA and coding region of influenza segment 7…………………………………………………………………………………….. 13 6 Schematic representation for the mRNA and coding region of influenza NS1 and NS2 proteins ............................................................................................................ 15 CHAPTER III 1 Locations of lakes assayed…………………………………………......................... 85 2 Neighbor-joining phylogram of the influenza virus hemagglutinin H1 gene sequences from Lake Park ice (collected in March 2002) and Lake Edoma water (collected in September 2001)…… ........................................................................... 92 3 Maximum parsimony phylogram of a wide selection of hemagglutinin H1 gene sequences……….. ..................................................................................................... 94 ix LIST OF TABLES Table Page CHAPTER II 1 Primers selected for detection of IAV genes……. .................................................... 67 2 RT-PCR assays on northeastern Siberian lake ice and lake water samples............... 69 3 RT-PCR assays on glacial ice samples and water samples collected
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