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Inflamin from Aipysurus Eydouxii: a Novel Toxin

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Inflamin from Aipysurus Eydouxii: a Novel Toxin INFLAMIN FROM AIPYSURUS EYDOUXII: A NOVEL TOXIN INDUCING INFLAMMATION BHASKAR BARNWAL (M.Tech.), IIT A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY DEPARTMENT OF BIOLOGICAL SCIENCES FACULTY OF SCIENCE NATIONAL UNIVERSITY OF SINGAPORE 2012 Acknowledgements Firstly, I am thankful to God for giving me strength and courage to overcome my failures. I am heavily indebted to National University of Singapore for awarding me the research scholarship. I am thankful to the Department of Biological Sciences for giving me an opportunity to conduct research. I would like to express my sincere gratitude to my supervisor Professor R. Manjunatha Kini for providing me a wonderful opportunity to work in his lab as an independent researcher. I am thankful for his constant encouragement and scientific input throughout my four years of research life. The most important thing which I learnt from him is to plan the experiments carefully before doing it. He also has a great role in polishing my presentation skills. I would like to thank Associate Professor J. Sivaraman for advising me on crystallization studies of inflamin. I would also like to thank Associate Professor Peter Wong for advising me on functional studies of my project. I am grateful to Assistant Professor Ajay Kumar Sharma and Dr. D. Garai who always guided me during my tough times. I am also thankful to Professor D. Das, Professor S. Dey, Professor A. K. Das and Professor R. K. Sen for providing me a strong background in various fields of biotechnology and biochemical engineering. I would like to thank Reena, Mrs Chan and Priscilla for all the official work and queries. Thanks a lot for your patience. I am thankful to all the past and present lab mates for helping me at one time or the other. I am thankful to Dr. Robin and Tzer Fong for teaching me molecular biology. I am grateful to Dr. Raghu and Sheena for teaching me HPLC and ESI-MS, i respectively. I am thankful to Dr. Amrita, Bidhan, Sindhuja, Saran and Summer for helping me in animal experiments and cell culture. I am extremely thankful to Dr. Girish for teaching me the nitty-gritty details of various instruments and techniques which helped me a lot in troubleshooting. My special thanks to my wife Garvita who has helped me in expression of the protein and animal experiments. I would also like to thank Dr. Ryan, Dr. Reza, Dr. Guna Shekhar, Dr. Pushpalatha, Dr. Alex, Dr. Cho Yeow, Dr. Shiyang, Dr. Aktar, Dr. Shifali, Angelina, Angie, Aldo, Nazir, Hoi Yee, Pei Ying, Vui Yin, Ritu, Janaki and Varuna for all the help they have done. I would like to thank all the members of structural biology lab 1-5 as well as plant morphogenesis lab for their help during various stages of my work. I extend my gratitude to Bee Ling, Xianhui and Say Tin for helping me during my research work. I can never forget those coffee sessions which was basically our discussion time for our project work. We (Girish, Vivek, Amrita, Garvita and off course me) used to discuss our success and failures to come up with new strategies and ideas. It was a perfect time to release our frustration and get back to work with full enthusiasm. I have no words for the help and guidance given by Girish, Amrita and Vivek. My wife Garvita has supported me at the personal as well as professional front. I apologize for releasing my frustration on her whenever the experiment did not work. Without the help of these four important people in my life, I would have not completed this project. I am extremely thankful to my father Dr. G. P. Barnwal and especially my mother Mrs. Meera Rani for the belief they had on me. My mother has always encouraged and motivated me to do well. I am also thankful to my father-in-law Mr. Suresh Chand Dhokeria and my mother-in-law Mrs. Sadhana Dhokeria for supporting me. I ii extend my gratitude to all my siblings who saw me through tough times and I am heartily thankful to them for whatever help they have given to me. I would also like to thank my uncle and aunty in Singapore who provided me home away from home. I greatly appreciate all the people who have ever helped me in some way or the other. Lastly, I would like to thank those mice and rats who had sacrificed their life for the experiments related to this thesis. Bhaskar Barnwal August, 2012 iii Table of contents Acknowledgements i Table of contents iv Summary ix List of tables xi List of figures xii Abbreviations xv CHAPTER ONE: Introduction 1 1.1 Snakes 2 1.1.1 Venom gland 2 1.1.2 Evolution of venom gland 3 1.2 Venomous snakes 3 1.2.1 Classification of venomous snakes 4 1.2.2 Marbled sea snake (Aipysurus eydouxii) 4 1.3 Snake venom 7 1.3.1 Snake venom composition 8 1.3.1.1 Enzymatic proteins 8 1.3.1.1.1 Phospholipases A2 (PLA2) 9 1.3.1.1.2 Acetylcholinesterases 12 1.3.1.1.3 L-Amino acid oxidases 12 1.3.1.2 Non-enzymatic proteins 14 1.3.1.2.1 Three-finger toxins 14 1.3.1.2.2 Sarafotoxins 15 1.3.1.2.3 Cysteine-rich secretory proteins (CRISPs) 17 iv 1.3.1.2.4 Snake venom nerve growth factors 20 1.3.1.2.5 Waprins 23 1.4 Inflammation 23 1.4.1 Macrophages 25 1.4.2 Phospholipases 26 1.4.3 Cytosolic phospholipases A2 (cPLA2) 26 1.4.4 Eicosanoids 28 1.4.5 Prostanoids biosynthesis: the COX pathway 29 1.5 Focus of this study 31 CHAPTER TWO: Expression and purification of inflamin 34 2.1 Introduction 35 2.2 Materials and Methods 37 2.2.1 Materials 37 2.2.2 Cloning of the synthetic gene 37 2.2.3 Preparation of competent cells 38 2.2.4 Heat-shock transformation 41 2.2.5 Plasmid DNA isolation 41 2.2.6 DNA sequencing and analysis 42 2.2.7 Expression of protein 42 2.2.8 Sodium dodecyl sulfate - polyacrylamide gel electrophoresis 43 2.2.9 Purification of protein 43 2.2.9.1 Affinity purification 44 2.2.9.2 RP-HPLC purification 45 2.2.10 Molecular mass determination 45 2.2.11 Refolding of protein 46 v 2.3 Results 46 2.3.1 Expression of inflamin 46 2.3.2 Affinity purification 48 2.3.3 RP-HPLC purification 50 2.3.4 Refolding and RP-HPLC purification 50 2.4 Discussion 54 2.5 Conclusion 56 CHAPTER THREE: Functional characterization of inflamin 57 3.1 Introduction 58 3.2 Materials and Methods 61 3.2.1 Materials 61 3.2.2 Hemolytic assay 61 3.2.3 Animals 62 3.2.4 In vivo effects of inflamin 62 3.2.4.1 Writhing induced by inflamin 62 3.2.4.2 Effect of inflamin on prostanoid synthesis 63 3.2.4.3 Edema induced by inflamin 63 3.2.5 Cell culture 63 3.2.6 Cell viability assay 64 3.2.7 Prostanoids assay 64 3.2.8 COX enzymatic activity assay 65 3.2.9 Western blotting 66 3.2.10 cPLA2 enzymatic activity assay 67 3.3 Results 67 3.3.1 Hemolytic activity 67 vi 3.3.2 Inflamin induces inflammation 68 3.3.3 Inflamin induces prostanoids release in the peritoneal cavity 71 3.3.4 Production of 6-keto PGF1α by RAW264.7 cells 72 3.3.5 Effect of inflamin on COX enzymatic activity and expression 80 3.3.6 Effect of inhibitors on 6-keto PGF1α production by RAW264.7 80 cells 3.3.7 Effect of inflamin on cPLA2 enzymatic activity, expression and 81 Phosphorylation 3.4 Discussion 87 3.5 Conclusion 93 CHAPTER FOUR: Structural characterization of inflamin 94 4.1 Introduction 95 4.2 Materials and Methods 97 4.2.1 Materials 97 4.2.2 Circular dichroism (CD) spectroscopy 97 4.2.3 Disulfide linkage determination 98 4.2.4 Crystallization of inflamin 99 4.3 Results 99 4.3.1 Circular dichroism (CD) spectroscopy 99 4.3.2 Disulfide linkage determination 99 4.3.3 Crystallization of inflamin 107 4.4 Discussion 108 4.5 Conclusion 109 CHAPTER FIVE: Conclusions and future perspectives 110 5.1 Conclusions 111 vii 5.2 Future perspectives 113 5.2.1 Identification of receptor 114 5.2.2 Biophysical studies of inflamin 114 5.2.3 Structure-function relationship of inflamin 115 5.2.4 Structural determination of inflamin 115 Bibliography 117 Appendix 138 viii Summary Due to low yield, the venom of Aipysurus eydouxii (Marbled sea snake) snake has not been extensively studied. However, partial cDNA library of A. eydouxii venom gland was constructed by our lab, which revealed the presence of few novel proteins. One of them showed no sequence similarity with any sequence in the database, but had a long open reading frame. The deduced protein sequence contained 113 amino acid residues with a 19-residue signal peptide at the N-terminal and the mature protein of 94 amino acid residues including 6 cysteine residues. Since these clones encode a cysteine-rich, secreted protein similar to most proteins in snake venoms, we were intrigued to understand its structure and function. In this study, we describe the recombinant expression, purification, folding and characterization of inflamin, the first member of a novel family of snake venom proteins.
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