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An Investigation Into the Heterogeneity of Insect Arylalkylamine N-Acyltransferases

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An Investigation Into the Heterogeneity of Insect Arylalkylamine N-Acyltransferases University of South Florida Scholar Commons Graduate Theses and Dissertations Graduate School 11-4-2019 An Investigation into the Heterogeneity of Insect Arylalkylamine N-Acyltransferases Brian G. O'Flynn University of South Florida Follow this and additional works at: https://scholarcommons.usf.edu/etd Part of the Biochemistry Commons Scholar Commons Citation O'Flynn, Brian G., "An Investigation into the Heterogeneity of Insect Arylalkylamine N-Acyltransferases" (2019). Graduate Theses and Dissertations. https://scholarcommons.usf.edu/etd/8674 This Dissertation is brought to you for free and open access by the Graduate School at Scholar Commons. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Scholar Commons. For more information, please contact [email protected]. An Investigation into the Heterogeneity of Insect Arylalkylamine N-Acyltransferases by Brian G. O’Flynn A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Chemistry College of Arts and Sciences University of South Florida Major Professor: David J. Merkler, Ph.D. Bill J. Baker, Ph.D. Ioannis Gelis, Ph.D. Yu Chen, Ph.D. Date of Approval: October 16, 2019 Keywords: AANAT, Insecticide, Acetylation, Fatty-acid Amide, Tribolium castaneum Copyright © 2019, Brian G. O’Flynn “In order to be irreplaceable, one must always be different” Coco Chanel ACKNOWLEDGEMENTS I would first thank Dr. David Merkler, for his tireless mentorship and guidance throughout my time at USF. The wisdom and knowledge he has shared with me have been invaluable in every aspect of my life. I can only hope I have returned his support in part through my work here and can look forward to the next stages of our affiliation as colleagues and friends. Further, I would like to thank my committee members, Dr. Ioannis Gelis, Dr. Yu Chen, and Dr. Bill Baker, for all the collaborations and beneficial discussions shared over the years. I am especially grateful to Dr. Baker, for offering me the opportunity to join USF Chemistry, back when I was a directionless undergraduate. I would also like to thank all the members of the Merkler lab, past and present. Without your advice, inspiration, and friendship, I would not have made it this far. This is especially true for Dr. Ryan Anderson and Gabby Suarez. The times we spent together, in lab and out, were unforgettable, and made even the toughest days better. I also had the great fortune to mentor several incredible undergraduates. The countless hours they devoted to their research became the backbone of this dissertation. I thank you all for your tireless contribution, especially Karin Claire Prins and Britney Shepherd, for who I am grateful not just for your amazing work ethic, but also the positivity you brought to the lab. Thank you also to Dr. Richard Pollenz and the STEM Academy. Being a graduate mentor was one of the most amazing experiences of my life, and I look forward to the exciting future of this program. To all my friends in Ireland, thank you for always being there for me. I will never take for granted the feeling of going home and feeling like I never left. To those in Florida who welcomed me so warmly, I am eternally grateful. A special mention must be given to Periodically Right, and all those trivia nights and tailgates that kept me sane and social. To Briana, words cannot describe the impact you have had in my life. You have been my best friend, and I can only hope I make you half as proud of me as I am of you. Finally, I would like to thank my family for their constant support. To Mam and Dad, you have always been there for me, and I will never be able to repay all you have given. But I will try. To Lisa and Keith, thank you for being my benchmark for how to get the most out of life. I will never stop looking up to you. To Nanny and aunt Geraldine, may you rest in peace. I carry your memory with me always. TABLE OF CONTENTS LIST OF TABLES ............................................................................................................iv LIST OF FIGURES ..........................................................................................................vi ABSTRACT .....................................................................................................................ix CHAPTER ONE: INTRODUCTION AND MOTIVATION ................................................. 1 1.1 Enzyme heterogeneity ................................................................................ 1 1.2 A brief history of pesticides ......................................................................... 3 1.3 Insecticide resistance .................................................................................. 5 1.4 AANATs as a potential insecticide target .................................................... 7 1.5 References ................................................................................................ 15 CHAPTER TWO: INSECT AANATS: MECHANISMS AND ROLE IN FATTY ACID AMIDE BIOSYNTHESIS ............................................................................................... 26 2.1 Introduction ............................................................................................... 26 2.2 N-Acetylation of the aromatic acids and aromatic amino acid – derived metabolites ............................................................................ 29 2.3 Insect AANAT – Kinetic mechanism .......................................................... 34 2.4 Insect AANAT – Catalytic mechanism ....................................................... 36 2.5 Insect AANAT – a “timezyme”? ................................................................. 47 2.6 Conclusion ................................................................................................ 49 2.7 References ................................................................................................ 50 CHAPTER THREE: IDENTIFICATION OF CATALYTICALLY DISTINCT AANAT SPLICOFORMS FROM TRIBOLIUM CASTANEUM ..................................................... 68 3.1 Introduction ............................................................................................... 68 3.2 Results and discussion ............................................................................. 70 3.2.1 Amine screening .......................................................................... 70 3.2.2 Amine steady-state kinetic constants ........................................... 71 3.2.3 Acyl-CoA steady-state kinetic constants ...................................... 73 3.2.4 Importance of the AANAT N-terminus ......................................... 74 3.3 Conclusion ................................................................................................ 78 3.4 Materials and methods .............................................................................. 78 3.4.1 Cloning of TcAANAT1b ................................................................ 78 3.4.2 Screening assay .......................................................................... 79 3.5 References ................................................................................................ 82 i CHAPTER FOUR: CHARACTERIZATION OF AANAT FROM TRIBOLIUM CASTANEUM: A POTENTIAL NEXT-GENERATION INSECTICIDE TARGET ............ 89 4.1 Introduction ............................................................................................... 89 4.2 Results and discussion ............................................................................. 92 4.2.1 Acyl-CoA steady-state kinetic constants ...................................... 92 4.2.2 Amino steady-state kinetic constants ........................................... 93 4.2.3 Product characterization .............................................................. 94 4.2.4 TcAANAT0 kinetic mechanism .................................................... 95 4.2.5 Crystal structure and mutagenesis of TcAANAT0 ...................... 103 4.2.6 TcAANAT0 chemical mechanism .............................................. 107 4.3 Conclusion .............................................................................................. 112 4.4 Experimental procedures ........................................................................ 112 4.4.1 Materials .................................................................................... 112 4.4.2 Cloning of T. castaneum AANAT0 ............................................. 113 4.4.3 Determination of enzyme activity ............................................... 114 4.4.4 Determination of kinetic mechanism .......................................... 114 4.4.5 Determination of acetyl-CoA binding constants ......................... 117 4.4.6 Determination of pH-dependence .............................................. 118 4.4.7 Product characterization ............................................................ 119 4.4.8 TcAANAT0 mutagenesis............................................................ 119 4.4.9 TcAANAT0 crystallization .......................................................... 120 4.4.10 X-ray data collection and refinement ......................................... 120 4.5 References .............................................................................................. 120 CHAPTER FIVE: Bm-iAANAT3: EXPRESSION AND CHARACTERIZATION OF A NOVEL ARYLALKYLAMINE N-ACYLTRANSFERASE FROM BOMBYX MORI ..... 130 5.1 Introduction ............................................................................................
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