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CHEMICAL BIODIVERSITY and SIGNALING: DETAILED ANALYSIS of Fmrfamide-LIKE NEUROPEPTIDES and OTHER NATURAL PRODUCTS by NMR and BIOINFORMATICS

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CHEMICAL BIODIVERSITY and SIGNALING: DETAILED ANALYSIS of Fmrfamide-LIKE NEUROPEPTIDES and OTHER NATURAL PRODUCTS by NMR and BIOINFORMATICS CHEMICAL BIODIVERSITY AND SIGNALING: DETAILED ANALYSIS OF FMRFamide-LIKE NEUROPEPTIDES AND OTHER NATURAL PRODUCTS BY NMR AND BIOINFORMATICS By AARON TODD DOSSEY A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2006 Copyright 2006 by Aaron Todd Dossey To my family; to members of the laboratory of Dr. Arthur S. Edison; and to God Almighty and the magnificent natural world he created which has given me much joy and a basis for my career in science. ACKNOWLEDGMENTS As with any endeavor one may pursue in life, I cannot take sole credit for anything I have done and, thus, thanks are certainly in order to those who have helped make my PhD possible. First and foremost, I would like to thank my family. In particular, I thank my grandparents, Jerry and Emma Dossey, and mother, Teresa (Dossey) Scott, for instilling in me three key components of my successes in life thus far: determination, a strong work ethic, and faith in myself. I would also like to thank God the creator for my life and the bountiful life forms of this earth that I enjoy studying every day. I would also like to thank Oklahoma State University and others who helped foster the early stages of my career in biochemistry. I thank Dr. Eldon C. Nelson, my undergraduate advisor, for showing great care about my career and keeping me focused and motivated on the career related aspects of my tenure there. For many interesting and encouraging conversations about entomology from which I learned a lot, I would like to thank Don C. Arnold, the curator of the Oklahoma State University Entomological Museum. I also thank the Southwestern Bell Telephone Corporation and Sylvia Coles Denebeim for supporting me through generous scholarships which helped tremendously with school related costs and allowed me to focus on my education. At the University of Florida (UF), I would like to thank Dr. Arthur Edison, my supervisory committee chair, for providing a research atmosphere that has allowed me to develop as a scientist. I also thank Dr. Edison for his patience while I was training in protein NMR and learning how to write scientific articles. I thank James R. Rocca in the iv UF AMRIS (Advanced Magnetic Resonance Imaging and Spectroscopy) facility for countless hours of help and discussion. His tireless efforts in NMR training were an invaluable complement to the training I received from Dr. Edison. Pat Jones, the Biochemistry department secretary, was also invaluable to me by keeping me in line with deadlines and course registration and I thank her for that as well. I also thank my supervisory committee members (Drs. Arthur S. Edison, Ben M. Dunn, Brian D. Cain, Joanna R. Long, and Stephen A. Hagen) for always being available to help guide me through my PhD studies. I also thank the University of Florida for awarding me the Grinter Fellowship for the first three years of my tenure there. For help with specific projects, others certainly deserve my thanks. I thank Dr. Cherian Zachariah for help, training, and experiments in protein expression and purification and NMR. For experiments performed and exciting discussion on phasmid insect pheromone chemistry, I thank Dr. Spencer Walse and James Rocca. For data resulting in my first publication (Chapter 3), I thank Drs. Mario de Bono, Peter Evans, and Vincenzina (Reale) Evans, and Heather Chatwin for bioassay experiments on FLP-18 related neuropeptides. For their support and friendship, I would like to thank Omjoy Ganesh, Iman Al-Naggar, Ramazan Ajredini, Fatma Kaplan, Dr. James Smith, and Dr. Terry B. Green (all fellow members of Dr. Edison’s lab). v TABLE OF CONTENTS page ACKNOWLEDGMENTS ................................................................................................. iv LIST OF TABLES...............................................................................................................x LIST OF FIGURES ........................................................................................................... xi ABSTRACT..................................................................................................................... xiii CHAPTER 1 INTRODUCTION ........................................................................................................1 Importance of Nematodes.............................................................................................1 FMRFamide-Like Neuropeptides (FLPs).....................................................................5 FLP Precursor Proteins..........................................................................................6 Receptors and Functions........................................................................................6 FLPs as Natural Products ......................................................................................9 Natural Products .........................................................................................................10 Dissertation Outline....................................................................................................13 2 BIOCHEMICAL PROPERTIES OF FLPS AND THEIR PRECURSOR PROTEINS FROM THE NEMATODE Caenorhabditis elegans..................................................17 Introduction.................................................................................................................17 Experimental Methods................................................................................................18 Data Mining for Nematode flp Precursor Protein Sequences .............................18 Alignment and Phylogenetic Analysis of flp Precursor Proteins ........................20 Analysis of Biochemical Properties of flp Precursor Proteins and Figure Generation........................................................................................................21 Analysis of FLP Mature Peptide Biochemical Properties...................................22 Results.........................................................................................................................23 Analysis of Biochemical Properties of flp Precursor Proteins ............................23 Sequence Repetition Patterns.......................................................................34 Charge Distribution......................................................................................35 Unstructured Propensity...............................................................................36 Other Features ..............................................................................................40 vi Biochemical Properties of Mature Processed FLPs ............................................41 Peptide Charge .............................................................................................44 Peptide Length and Amino Acid Conservation............................................44 Discussion...................................................................................................................47 Grouping of FLP Subfamilies by Precursor and Peptide Properties ...................47 The flp-1 Group............................................................................................48 The flp-6 Group............................................................................................49 The flp-7 Group............................................................................................49 The flp-20 Group..........................................................................................50 The flp-21 Group..........................................................................................51 Charge Compensation and Possible flp Precursor Structure...............................53 3 NMR ANALYSIS OF C. elegans FLP-18 NEUROPEPTIDES: IMPLICATIONS FOR NPR-1 ACTIVATION.......................................................................................55 Introduction.................................................................................................................55 Experimental Procedures............................................................................................56 Peptide Synthesis.................................................................................................56 Peptide Sample Preparation.................................................................................56 Biological Activity Assays:.................................................................................57 NMR Spectroscopy .............................................................................................58 Results.........................................................................................................................59 Peptide Design Rationale and Physiological Responses:....................................59 NMR Chemical Shifts Reveal Regions of flp-18 Peptides with Significant Structure:..........................................................................................................63 pH Dependence of Amide Proton Chemical Shifts Reveal Regions of flp-18 Peptides with Significant Structure:.................................................................67 pH Dependence of Arginine Side-Chains Reveal Long-Range Interactions: .....70 Quantitative Determination of pKa Reveals Multiple Interactions:....................70 Temperature Dependence of Amide Chemical Shifts Corroborates Regions with H-Bonding: ......................................................................................................74
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