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Characterizing Vertebrate Rhodopsin Natural Variation in Evolution, Function, and Disease

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Characterizing Vertebrate Rhodopsin Natural Variation in Evolution, Function, and Disease CHARACTERIZING VERTEBRATE RHODOPSIN NATURAL VARIATION IN EVOLUTION, FUNCTION, AND DISEASE by Nihar Bhattacharya A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Cell and Systems Biology University of Toronto © Copyright by Nihar Bhattacharya (2018) CHARACTERIZING VERTEBRATE RHODOPSIN NATURAL VARIATION IN EVOLUTION, FUNCTION, AND DISEASE Nihar Bhattacharya Doctor of Philosophy Department of Cell and Systems Biology University of Toronto 2018 ABSTRACT Vertebrate dim light vision is mediated by the rod visual pigment, rhodopsin, a member of the G protein-coupled receptor (GPCR) superfamily of proteins. In the dark, rhodopsin is covalently bound to a vitamin A-derived 11-cis chromophore, which acts as an inverse agonist to stabilize the inactive state of rhodopsin. When exposed to light of a maximal wavelength (λmax), the 11-cis retinal chromophore isomerizes to an all-trans conformation, initiating a series of structural shifts to the light-activated state of rhodopsin. This results in a signalling cascade within the rod photoreceptor cell and, ultimately, the perception of light. The goal of this thesis is to investigate natural variation in rhodopsin function in the context of evolutionary adaptation, chromophore usage, and disease mutations. Following a general introduction, in Chapter II, I characterize the visual system of the diurnal colubrid snake Pituophis melanoleucus using immunohistochemistry of retinal sections and spectroscopy of ii purified visual pigments expressed in vitro, revealing an unusual rhodopsin with cone opsin properties found in cone-like rod photoreceptors. In Chapter III, I investigate the effects of the rare vertebrate chromophore, 11-cis 3,4 dehydroretinal (A2), on the spectral and non- spectral properties of rhodopsin. In Chapters IV and V, I study the effects of pathogenic mutations in rhodopsin that cause the retinal degenerative disease retinitis pigmentosa (RP). In Chapter IV of my thesis, I identify the phenotype of RP mutations found in the extracellular loop 2 of rhodopsin and assess the effects of functional rescue using two different approaches. Finally, in Chapter V, I characterize three novel RP mutations to investigate the relationship between the in vitro and clinical disease phenotypes. The investigations in this thesis expand our understanding of snake retinal evolution, the role of the chromophore in rhodopsin function, and the effect of pathogenic mutations on rhodopsin structure and function. This thesis combines data from non-model organisms, non- mammalian chromophores, and non-wildtype pathogenic mutations to significantly increase our understanding of the scope of rhodopsin functionality. iii ACKNOWLEDGMENTS Over the last 6 years, I have grown, matured, and changed so much that when I think of myself pre-Toronto, I can hardly believe that was me. There are so many people I have to acknowledge and thank for this transformation. I would like to begin by thanking my supervisor, Belinda Chang. The experiences I had in her lab have been formative and helped shape me as a researcher and scientist. I thank her for indulging my biochem-y/wet lab ways while also hammering me into something resembling a coherent writer. I thank her for letting me try out new things and for allowing me to gain experience in so many other facets of research on top of those that are typical for a graduate student. I would like to thank my supervisory committee: Vince Tropepe and Jane Mitchell. They’ve made every single one of my committee meetings an absolute delight and were a source of great feedback and advice. I’d also like to thank Dr. David Hunt for agreeing to be my external, and Jennifer Mitchell for agreeing to be my internal examiner. I would also like to acknowledge Les Buck for his feedback and comments during my appraisal exam. I’d like to thank Vince again for being such a wonderful collaborator on the snake project. Also, Massimo Olivucci and Akimori Wada for their patience and guidance during our collaboration on the A2 project. I would also like to thank Elise Heon for her contribution to the RP project. I thank Henry Hong and the Imaging Facility in Ramsay Wright for his help with everything microscopy related. Also, my thanks to Tamar, Ian and Jim for all the assistance and conversations over the years, all three of you made my PhD a more pleasant experience. I would also like to thank the Vision Science Research Program and Janet Wong for funding me and for exposing me to the larger world of ophthalmology. iv I’d also like to thank Melody, Chris, Ken, Tanja, Nyla and the rest of the teaching staff for giving me the opportunity to develop as a teacher and for giving me a space to retreat to in the building. I’d like to thank Virlana Shchuka for her friendship and all of the lovely and fascinating conversations we’ve had over the years. To all the Chang lab members, past and present, thank you for your friendship, your assistance, and your collaboration. I would specifically like to thank Amir for helping me so much with stats, Alex for his patient help with my figures and A2 brainstorming, Ryan for dealing with my naïveté with evolutionary biology, and Ben for being my RP and wet lab comrade in arms. I would especially like to thank Frances, Sarah, Eduardo and Gianni for keeping me laughing, keeping me well fed, keeping me nerdy, and for keeping me sane with constant supply of cute animal/Makwa/Tabi/Gia/Tess pics. I could write an entire paragraph of thanks for each of you. My thanks to you all, and I hope we keep in touch. To my extended dojo family, thank you for giving me a different perspective on things and for the extremely fun nights out. Specific thanks to Sacha, Elizabeth and Greg, Darby and Ece, and Patrice for keeping me limber. Finally, to my family: thank you for your patience with me and thank you for loving me. Choto Dida and Dadu and the Roy family, thank you for taking such good care of me in Toronto and Atlanta. To Dada and Boudi, thank you for flying me out to SF so many times and for being so supportive, for nurturing my artistic side and for being a source of calm and sanity for me. And to Ma and Baba, I don’t even know where to start. You’ve both helped me so much during my PhD. Thank you for all the trips, for all the nature retreats, for still taking care of me, for worrying about me. I love you all so much v TABLE OF CONTENTS ACKNOWLEDGMENTS ............................................................................................................IV TABLE OF CONTENTS ............................................................................................................VI LIST OF TABLES ..................................................................................................................VIII LIST OF FIGURES ...................................................................................................................IX LIST OF ABBREVIATIONS .......................................................................................................XI CHAPTER I: GENERAL INTRODUCTION..................................................................................... 1 1.1 - EYE ....................................................................................................................................... 1 1.2 - RETINA .................................................................................................................................. 6 1.3 - PHOTORECEPTORS ................................................................................................................. 9 1.3.1 - ROD AND CONE PHOTORECEPTORS ............................................................................... 10 1.3.2 - PHOTORECEPTOR TRANSMUTATION .............................................................................. 12 1.4 - PHOTOTRANSDUCTION ......................................................................................................... 16 1.5 - OPSINS ................................................................................................................................ 20 1.6 - RHODOPSIN ......................................................................................................................... 22 1.6.1 - RHODOPSIN STRUCTURE ............................................................................................... 23 1.6.2 - RHODOPSIN ACTIVATION .............................................................................................. 25 1.6.3 - RHODOPSIN VARIATION ................................................................................................ 28 1.7 - VERTEBRATE CHROMOPHORE .............................................................................................. 31 1.7.1 - THE A2 CHROMOPHORE ................................................................................................ 31 1.7.2 - RETINOID CYCLE .......................................................................................................... 34 1.8 - RETINAL DISEASE ................................................................................................................ 37 1.8.1 - RETINITIS PIGMENTOSA ................................................................................................ 37 1.8.2 - DISEASE MUTATIONS IN RHODOPSIN ............................................................................ 39 1.8.3 - RESCUE AND TREATMENT METHODS OF RETINITIS PIGMENTOSA .................................. 44 1.8.4 - RETINITIS PIGMENTOSA
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