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Venoms-Based Discovery of Novel Modulators of Human Neuronal Α7 and Α3* Nicotinic Acetylcholine Receptors Rosa Esther Prahl Msc

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Venoms-Based Discovery of Novel Modulators of Human Neuronal Α7 and Α3* Nicotinic Acetylcholine Receptors Rosa Esther Prahl Msc Venoms-based discovery of novel modulators of human neuronal α7 and α3* nicotinic acetylcholine receptors Rosa Esther Prahl MSc. Cell Biology A thesis submitted for the degree of Master of Philosophy at The University of Queensland in 2016 Institute for Molecular Bioscience ABSTRACT Nicotinic acetylcholine receptors (nAChRs) are pentameric ligand-gated channels that contain combinations of α and β subunits (heteromeric) or only five α subunits (homomeric). To date, 12 subunits have been cloned. Although different types of neuronal nAChRs are expected to occur in vivo, most structure-activity relationship studies have been carried out for just a few neuronal subtypes. Clinical and basic research has shown that cholinergic receptors play a role in several disorders of the nervous system such as chronic pain, Alzheimer’s disease and addiction to nicotine, alcohol and drugs. Unfortunately, the lack of selective modulators for each subtype of nAChR makes their pharmacological characterization difficult, which has slowed the development of therapeutic nAChR modulators with high selectivity and absence of off-target side effects. Animal venoms have proven to be an excellent natural source of bioactive molecules with activity against ion channels. Venoms from different snakes and in particular molluscs of the Conus genus have been an important source of modulators of cholinergic receptors. However, spider and scorpion venoms have been studied less extensively and there are only two examples of cholinergic receptor modulators reported from arachnid venom. Thus, the primary goal of this thesis was to identify novel modulators of the human ganglionic α3* nAChR (where the asterisk indicates that β subunits form part of the heteropentameric receptor) and the homomeric neuronal α7 nAChR using spider and scorpion venoms. “Hit” venoms from a selection of “modern” and “primitive” spiders were identified via high-throughput screens against the α3* and α7 nAChRs endogenously expressed in SH-SY5Y cells. A total of 71 spider venoms were screened, with representatives from nine different taxonomic families. The resulting data showed that 91% of the venoms presented some activity against the nAChR subtypes tested and most of these were non-selective blockers of the α3* and α7 subtypes. Toxins directed against vertebrate nAChRs likely evolved through frequent interactions between spiders and small vertebrate predators. Our data revealed that nAChR agonists are likely to be present in venom of the “primitive” spiders 2 and therefore were probably basally recruited in spider venom. In summary, the screening of spider venoms against vertebrate cholinergic receptors provided information about the origin and evolution of toxins against vertebrate receptors. The search for nAChR modulators was extended to scorpion venoms that are recognized as sources of toxins that affect primarily the properties of voltage-gated sodium and potassium channels. In this work, venoms from Androctonus australis, Androctonus crassicauda, Leirurus quinquestriatus and Grosphus grandidieri (Buthidae) and Heterometus spinnifer (Scorpionidae) were screened against the α3* and α7 nAChRs using SH-SY5Y cells. The venom of Heterometrus spinnifer was found to contain an agonistic compound. Activity guided-fractionation allowed isolation of the “hit” toxin, and it was identified by high-resolution mass spectrometry as senecioylcholine. This non-peptide toxin has not previously been identified in arachnids but it was previously isolated from some marine gastropods (Muricidae). It shows high toxicity against vertebrates. Thus, this non-peptide toxin is likely to function in defence against vertebrate predators. 3 DECLARATION BY AUTHOR This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis. 4 PUBLICATIONS DURING CANDIDATURE No publications. PUBLICATIONS INCLUDED IN THIS THESIS No publications. 5 CONTRIBUTION BY OTHERS TO THE THESIS Prof. Richard Lewis and Dr Irina Vetter (Institute for molecular Bioscience) supported during the screening of “hit” toxins of the 71 venoms with their expertise in FLIPR assays. Chapter 1 Dr Volker Herzig (Institute for Molecular Bioscience) performed HPLC fractionation of crude venom from Macrothele gigas. Dr Irina Vetter (Institute for Molecular Bioscience) performed one FLIPR assay that was mentioned in section 2.3.4. Chapter 2 HPLC fractionation of crude venom from Heterometrus spinnifer was performed by Dr Niraj Bende (Institute for Molecular Bioscience). Dr Angela Salim identified the “hit” toxin from Heterometrus spinnifer as senecioylcholine using high-resolution electrospray ionization mass spectrometry. She also performed as well as the co-elution of the native compound with its synthetic form, and two of its synthetic isomers (tigloylcholine and angeloylcholine). Pratik Neupane carried out the chemical synthesis of senecioylcholine, tigloylcholine and angeloylcholine. Angela and Pratik were involved in the writing of the protocol for identification and chemical synthesis of senecioylcholine. Angela and Pratik are members of the group of Prof. Robert Capon at The Institute for Molecular Bioscience. 6 STATEMENT OF PARTS OF THE THESIS SUBMITTED TO QUALIFY FOR THE AWARD OF ANOTHER DEGREE None. 7 ACKNOWLEDGEMENTS I thank Prof. Glenn King, Prof. Richard Lewis, Prof. Robert Capon, Dr Amanda Carozzi, Dr Irina Vetter, Dr Angela Salim, Pratik Neupane and Sassan Ranhama for their time, efforts and suggestions during the course of my thesis. This work was funding and supported by the following institutions: Postgraduate studies of The University of Queensland (UQ), the UQ Institute for Molecular Bioscience, and a program grant from the Australian National Health & Medical Research Council. I dedicate this thesis to the Holy Father, my husband Torben and my son Clouseau. 8 KEYWORDS spider venom, scorpion venom, ligand gated calcium channel, α7 nicotinic acetylcholine receptors, α3* nicotinic acetylcholine receptors, FLIPR, high throughput screening, choline ester, senecioylcholine AUSTRALIAN AND NEW ZEALAND STANDARD RESEARCH CLASSIFICATIONS (ANZSRC) ANZSRC code: 060101, Analytical Biochemistry, 80% ANZSRC code: 060199, Biochemistry and Cell Biology not elsewhere classified, 20% FIELDS OF RESEARCH (FOR) CLASSIFICATION FoR code: 0601, Biochemistry and Cell Biology, 80% FoR code: 0699, Other Biological Sciences, 20% 9 TABLE OF CONTENTS Abstract ........................................................................................................................ 2 Declaration by author ................................................................................................... 4 Publications during candidature .................................................................................... 5 Publications included in this thesis ................................................................................ 5 Contribution by others to the thesis .............................................................................. 6 Statement of parts of the thesis submitted to qualify for the award of another degree . 7 Acknowledgements ....................................................................................................... 8 Keywords ...................................................................................................................... 9 Australian and New Zealand Standard Research Classifications (ANZSRC) ..................... 9 Fields of Research (FoR) Classification ........................................................................... 9 Table of Contents ......................................................................................................... 10 List of figures and Tables .............................................................................................. 12 List of abbreviations ................................................................................................................................................ 14 CHAPTER 1 — Introduction ..........................................................................................
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