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Proquest Dissertations Sites and Roles of Arrestin Phosphorylation in Regulating Interactions between Arrestin and Rhodopsin of Squid Eyes Xinyu Guan A thesis submitted in conformity with the requirements for the degree of M.Sc. Graduate Department of Pharmacology and Toxicology University of Toronto © Copyright by Xinyu Guan (2008) Library and Bibliotheque et 1*1 Archives Canada Archives Canada Published Heritage Direction du Branch Patrimoine de I'edition 395 Wellington Street 395, rue Wellington Ottawa ON K1A0N4 Ottawa ON K1A0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-45178-6 Our file Notre reference ISBN: 978-0-494-45178-6 NOTICE: AVIS: The author has granted a non­ L'auteur a accorde une licence non exclusive exclusive license allowing Library permettant a la Bibliotheque et Archives and Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par telecommunication ou par Plntemet, prefer, telecommunication or on the Internet, distribuer et vendre des theses partout dans loan, distribute and sell theses le monde, a des fins commerciales ou autres, worldwide, for commercial or non­ sur support microforme, papier, electronique commercial purposes, in microform, et/ou autres formats. paper, electronic and/or any other formats. The author retains copyright L'auteur conserve la propriete du droit d'auteur ownership and moral rights in et des droits moraux qui protege cette these. this thesis. Neither the thesis Ni la these ni des extraits substantiels de nor substantial extracts from it celle-ci ne doivent etre imprimes ou autrement may be printed or otherwise reproduits sans son autorisation. reproduced without the author's permission. In compliance with the Canadian Conformement a la loi canadienne Privacy Act some supporting sur la protection de la vie privee, forms may have been removed quelques formulaires secondaires from this thesis. ont ete enleves de cette these. While these forms may be included Bien que ces formulaires in the document page count, aient inclus dans la pagination, their removal does not represent il n'y aura aucun contenu manquant. any loss of content from the thesis. Canada Sites and Roles of Arrestin Phosphorylation in Regulating Interactions between Arrestin and Rhodopsin of Squid Eyes Xinyu Guan A thesis submitted in conformity with the requirements for the degree of M.Sc. Graduate Department of Pharmacology and Toxicology University of Toronto, 2008 Abstract In squid (Loligo pealei], activation of phototransduction is mediated by rhodopsin isomerization to metarhodopsin and the activation of a phospholipase C pathway, resulting in depolarization of the retinal membrane. Inactivation is mediated by squid rhodopsin kinase (SQRK) and arrestin. Arrestin binding to metarhodopsin is the key inactivation step and SQRK-mediated phosphorylation of rhodopsin is not required for arrestin binding. SQRK can also phosphorylate arrestin, a function that is not shared by other receptor kinases. To determine the site(s) and function of arrestin phosphorylation, I expressed recombinant arrestins in E. coli and used site-directed mutagenesis. Squid arrestin was phosphorylated at Ser392 and/or Ser397 by SQRK. Arrestin phosphorylation did not affect arrestin binding to rhodopsin in the light but inhibited its binding to dark-adapted membranes. Furthermore, the phosphorylation significantly increased arrestin dissociation from dark-adapted membranes at high salt concentrations in vitro. This work suggested that the role of arrestin phosphorylation was to increase dissociation of the protein from rhodopsin once it has been photoconverted back to inactive state. ii Acknowledgements I was born in a small town in China, a place so remote and peaceful that even the keenest journalist may have forgotten its existence. In my world, imagination is the king. But even in my wildest dreams, I have never anticipated to study abroad or to learn any stories happening inside the world of cells. Everything happening now seems so unbelievable, but in the same time, is so believable because of you, my mentors Drs. Jane Mitchell and Hee-Won Park. Thank you so much for taking me as your student and for giving your guidance, encouragement and patience throughout my work. I would also like to thank my advisor Dr. James Wells for his advice during the course of my degree. To the additional members of my committee, Drs, J. Peter McPherson and Scott Heximer, thank you very much for your contribution to my defense. I also want to give my thanks to my colleagues Walter Swardfager, Lick Lai, Lynle Go, Rosalia Yoon, Shara Hong and Mike Mattocks. It has been my pleasure to learn and work with you. To you, the student who is about to continue on this work, I wish you read this part before jumping into the discussion section. When I look back the two years I have spent working on this project with Dr. Mitchell, I felt it had been one of the best decisions I had made. "Some are born great, some achieve greatness, and some have the greatness thrust upon them." Unfortunately, you may not register your name in the short list of great people even with great results from this work, but I hope you would one day realize that this may be the first step towards the rest of a meaningful life. Enjoy. iii Table of Contents Abstract ii Acknowledgements Hi Table of Contents iv List of Figures vi List of Tables vi List of Abbreviations vii 1. Introduction 1-29 1.1 Invertebrate Eyes 2 1.2 Molecular Pathways of Phototransduction 2 1.2.1 Squid Rhodopsin 5 1.2.2 G Protein 10 1.2.3 Phospholipase C 13 1.2.4 IP3/DAG Signaling Pathway 14 1.3 Termination of Phototransduction 15 1.3.1 Rhodopsin Kinase 16 1.3.1.1 Mammalian G-protein Coupled Receptor Kinase 16 1.3.1.2 Invertebrate Rhodopsin Kinase 17 1.3.2 Arrestin 18 1.3.2.1 Arrestin Structure 19 1.3.2.2 Invertebrate Arrestin 21 1.4 Phosphorylation of Arrestin 27 1.5 Rationale, Research Goals and Hypotheses 28 2. Materials and Methods 29-34 2.1 Materials 29 2.2 Preparation of Dark-Adapted Salt-Washed Rhabdomeric Membranes 29 2.3 cDNA Preparation and Mutation 30 2.4 Production of Recombinant Arrestin 31 2.5 Enrichment of Recombinant Arrestin 31 2.6 Arrestin Phosphorylation Assays 32 2.7 Membrane Association Assays 32 2.8 Membrane Dissociation Assays 33 2.9 Other Methods 33 3. Results 34-58 3.1 Solubility of Recombinant sArr 34 3.2 Recombinant sArr Production and Enrichment 41 3.3 Phosphorylation of Recombinant sArr 45 3.3.1 SQRK-Dependent sArr Phosphorylation 45 3.3.2 Membrane and Calcium Effects on sArr Phosphorylation 47 3.4 Determination of the Sites of Phosphorylation on sArr 47 3.5 Membrane Binding Assays 50 3.6 Membrane Dissociation Assays 54 iv 4. Discussion 59-71 4.1 Recombinant sArr Production and Purification 59 4.2 Phosphorylation of sArr by SQRK 63 4.2.1 Membrane Effect on sArr Phosphorylation 63 4.2.2 Calcium Effect on sArr Phosphorylation 65 4.2.3 Phosphorylation and Clathrin-Binding Sites on sArr 66 4.3 Functional Role of the Phosphorylation 67 4.3.1 Phosphorylation and Arrestin Binding to Membranes 67 4.3.2 Phosphorylation and Arrestin Dissociation from Membranes 68 4.4 Modeling the Arrestin-Mediated Receptor Desensitization and Future Studies 69 5. Appendix 72 6. Reference 73-81 v List of Figures Introduction Figure 1. Squid Eye and Camera-Type Vision 3 Figure 2. Squid Photoreceptors 4 Figure 3. Activation of Invertebrate Visual Signaling Pathway 6 Figure 4. Three-Dimentional Structure of Squid Rhodopsin 8 Figure 5. Sequence Alignment of Loligo pealei and Todarodes pacificus Rhodopsins 9 Figure 6. Hypothetical Structure of a Complex Composed of GtaPy with Rhodopsin 12 Figure 7. Three-Dimensional Structure of Mammalian B-Arrestin 20 Figure 8. Model of Mammalian Arrestin Binding to Activated Receptors 22 Figure 9. Alignment of Amino Acid Sequences of Arrestins 25 Results Figure 10. Solubility of rsArrWT & IPTG Concentrations and Growth Temperatures 36 Figure 11. Solubility of rsArrWT in Origami Cells 38 Figure 12. Solubility of GST- and HisMBP-Tagged rsArrWT 39 Figure 13. Effects of Lysis Buffer pH on rsArrWT Solubility 40 Figure 14. Representation of the rsArrWT Enrichment Process 42 Figure 15. Representation of the rsArr3A Enrichment Process 43 Figure 16. Representation of the rsArr2A3 Enrichment Process 44 Figure 17. SQRK-Dependent sArrWT Phosphorylation 46 Figure 18. Membrane Effects on rsArrWT Phosphorylation 48 Figure 19. Calcium Effect on rsArrWT Phosphorylation 49 Figure 20. Phosphorylation of rsArrWT and rsArr3A 51 Figure 21. Phosphorylation of rsArrWT, rsArr3A and rsArr2A3 52 Figure 22. Light-Dependent Membrane Binding of rsArrWT and rsArr3A 53 Figure 23. Effects of Phosphorylation on nsArr Binding to Membranes 55 Figure 24. Comparison between phosphorylated and unphosphorylated nsArr 56 Figure 25. Dissociation of nsArr from Dark Adapted Membranes 58 Discussion Figure 26. Model of Rhodopsin Cycle in Invertebrate Photoreceptors 71 List of Tables Table 1. Estimation of arrestin concentration and yield per 120 g cell paste 45 VI List of Abbreviation Xmax: maximum absorbance wavelength AEBSF: 4-(2-Aminoethyl] benzenesulfonyl fluoride hydrochloride ATP: adenosine triphosphate C-terminus: carboxyl-terminus cDNA: complementary dioxyribonucleotide sequence cGMP: cyclic guanosine monophosphate DAG: diacylglycerol DTT: dithiothreitol E. coli: Escherichia coli EDTA: ethylenediaminetetraacetic acid EGTA: ethylene glycol tetraacetic acid G protein: guanine nucleotide-binding protein GBy:
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