Evolution of opsins and phototransduction

Opsins are the universal photoreceptor molecules of all visual systems in the animal kingdom. They can change their conformation from a resting state to a signalling state upon light absorption, which activates the G protein, thereby resulting in a signalling cascade that produces physiological responses. This process of capturing a photon and transforming it into a physiological response is known as phototransduction. Recent cloning techniques have revealed the rich and diverse nature of these molecules, found in organisms ranging from jellyfish to humans, functioning in visual and non-visual phototransduction systems and photoisomerases. Here we describe the diversity of these proteins and their role in phototransduction. Then we explore the molecular properties of opsins, by analysing site-directed mutants, strategically designed by phylogenetic comparison. This site-directed mutant approach led us to identify many key features in the evolution of the photoreceptor molecules. In particular, we will discuss the evolution of the counterion, the reduction of agonist binding to the receptor, and the molecular properties that characterize rod opsins apart from cone opsins. We will show how the advances in molecular biology and biophysics have given us insights into how evolution works at the molecular level.

[1]  R. Foster,et al.  Teleost multiple tissue (tmt) opsin: a candidate photopigment regulating the peripheral clocks of zebrafish? , 2003, Brain research. Molecular brain research.

[2]  Y. Shichida,et al.  E113 is required for the efficient photoisomerization of the unprotonated chromophore in a UV-absorbing visual pigment. , 2008, Biochemistry.

[3]  J. Nathans,et al.  Molecular genetics of inherited variation in human color vision. , 1986, Science.

[4]  Y. Fukada,et al.  Exo-rhodopsin: a novel rhodopsin expressed in the zebrafish pineal gland. , 1999, Brain research. Molecular brain research.

[5]  J. Nathans,et al.  Peropsin, a novel visual pigment-like protein located in the apical microvilli of the retinal pigment epithelium. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[6]  K. Hofmann,et al.  Opsin/all-trans-retinal complex activates transducin by different mechanisms than photolyzed rhodopsin. , 1996, Biochemistry.

[7]  D. Arendt Evolution of eyes and photoreceptor cell types. , 2003, The International journal of developmental biology.

[8]  S. Snyder,et al.  Parapinopsin, a Novel Catfish Opsin Localized to the Parapineal Organ, Defines a New Gene Family , 1997, The Journal of Neuroscience.

[9]  S. Hattar,et al.  Melanopsin Regulates Visual Processing in the Mouse Retina , 2006, Current Biology.

[10]  Y. Tsukahara,et al.  Interaction of GTP‐binding protein Gq with photoactivated rhodopsin in the photoreceptor membranes of crayfish , 1993, FEBS letters.

[11]  María del Pilar Gomez,et al.  Light Transduction in Invertebrate Hyperpolarizing Photoreceptors: Possible Involvement of a Go-Regulated Guanylate Cyclase , 2000, The Journal of Neuroscience.

[12]  A. Terakita,et al.  Conserved proline residue at position 189 in cone visual pigments as a determinant of molecular properties different from rhodopsins. , 2002, Biochemistry.

[13]  D. Larhammar,et al.  Extensive duplications of phototransduction genes in early vertebrate evolution correlate with block (chromosome) duplications. , 2004, Genomics.

[14]  M. Grossmann,et al.  G Protein-coupled Receptors , 1998, The Journal of Biological Chemistry.

[15]  D. Kojima,et al.  Single amino acid residue as a functional determinant of rod and cone visual pigments. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Toshiyuki Okano,et al.  The primary structure of iodopsin, a chicken red‐sensitive cone pigment , 1990, FEBS letters.

[17]  A. Terakita,et al.  A rhodopsin exhibiting binding ability to agonist all-trans-retinal. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Bok,et al.  Retinal Pigment Epithelium-Retinal G Protein Receptor-Opsin Mediates Light-dependent Translocation of All-trans-retinyl Esters for Synthesis of Visual Chromophore in Retinal Pigment Epithelial Cells* , 2008, Journal of Biological Chemistry.

[19]  W. P. Hayes,et al.  A Novel Human Opsin in the Inner Retina , 2000, The Journal of Neuroscience.

[20]  Satoru Kawamura,et al.  Rod and cone photoreceptors: molecular basis of the difference in their physiology. , 2008, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[21]  Y. Shichida,et al.  Photochemical and biochemical properties of chicken blue-sensitive cone visual pigment. , 1997, Biochemistry.

[22]  M. Max,et al.  Pineal opsin: a nonvisual opsin expressed in chick pineal , 1995, Science.

[23]  Toshiyuki Okano,et al.  Pinopsin is a chicken pineal photoreceptive molecule , 1994, Nature.

[24]  K. Yau,et al.  Molecular Properties of Rhodopsin and Rod Function* , 2007, Journal of Biological Chemistry.

[25]  D. Oprian,et al.  Constitutively active mutants of rhodopsin , 1992, Neuron.

[26]  Markus Eilers,et al.  Changes in interhelical hydrogen bonding upon rhodopsin activation. , 2005, Journal of molecular biology.

[27]  D. Hunt,et al.  Characterization of a novel human opsin gene with wide tissue expression and identification of embedded and flanking genes on chromosome 1q43. , 2001, Genomics.

[28]  Hugh M Robertson,et al.  G Protein-Coupled Receptors in Anopheles gambiae , 2002, Science.

[29]  Axel Meyer,et al.  Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? , 2008, Molecular biology and evolution.

[30]  Y. Fukada,et al.  Is chicken green-sensitive cone visual pigment a rhodopsin-like pigment? A comparative study of the molecular properties between chicken green and rhodopsin. , 1994, Biochemistry.

[31]  M. Biel,et al.  Melanopsin and rod–cone photoreceptive systems account for all major accessory visual functions in mice , 2003, Nature.

[32]  K. Fahmy,et al.  Identification of glutamic acid 113 as the Schiff base proton acceptor in the metarhodopsin II photointermediate of rhodopsin. , 1994, Biochemistry.

[33]  Y. Fukada,et al.  Identification of rhodopsin in the pigeon deep brain , 1998, FEBS letters.

[34]  Eisuke Eguchi,et al.  A survey of 3-dehydroretinal as a visual pigment chromophore in various species of crayfish and other freshwater crustaceans , 1987, Experientia.

[35]  Y. Fukada,et al.  Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Y. Tsukahara,et al.  A Novel Go-mediated Phototransduction Cascade in Scallop Visual Cells* , 1997, The Journal of Biological Chemistry.

[37]  Todd H. Oakley,et al.  The Origins of Novel Protein Interactions during Animal Opsin Evolution , 2007, PloS one.

[38]  Russell G Foster,et al.  Neuropsin (Opn5): a novel opsin identified in mammalian neural tissue 1 , 2003, FEBS letters.

[39]  J. Dowling,et al.  Differential expression of duplicated VAL‐opsin genes in the developing zebrafish , 2008, Journal of neurochemistry.

[40]  Akihisa Terakita,et al.  Parietal-Eye Phototransduction Components and Their Potential Evolutionary Implications , 2006, Science.

[41]  Satchidananda Panda,et al.  Melanopsin Is Required for Non-Image-Forming Photic Responses in Blind Mice , 2003, Science.

[42]  L. Chittka,et al.  The evolution of color vision in insects. , 2001, Annual review of entomology.

[43]  Y. Fukada,et al.  PHOTOSENSITIVITIES OF IODOPSIN AND RHODOPSINS , 1992, Photochemistry and photobiology.

[44]  A. Terakita,et al.  Origin of the vertebrate visual cycle: Genes encoding retinal photoisomerase and two putative visual cycle proteins are expressed in whole brain of a primitive chordate , 2003, The Journal of comparative neurology.

[45]  K. Yau,et al.  Diminished Pupillary Light Reflex at High Irradiances in Melanopsin-Knockout Mice , 2003, Science.

[46]  E. Pugh,et al.  Mouse Cones Require an Arrestin for Normal Inactivation of Phototransduction , 2008, Neuron.

[47]  H. Fong,et al.  The Endogenous Chromophore of Retinal G Protein-coupled Receptor Opsin from the Pigment Epithelium* , 1999, The Journal of Biological Chemistry.

[48]  K. Hiraki,et al.  On the three visual pigments in the retina of the firefly squid, Watasenia scintillans , 1990, Journal of Comparative Physiology A.

[49]  H. Dartnall The photosensitivities of visual pigments in the presence of hydroxylamine. , 1968, Vision research.

[50]  K. Kubokawa,et al.  Amphioxus homologs of Go‐coupled rhodopsin and peropsin having 11‐cis‐ and all‐trans‐retinals as their chromophores , 2002, FEBS letters.

[51]  A. Terakita,et al.  Expression and comparative characterization of Gq‐coupled invertebrate visual pigments and melanopsin , 2008, Journal of neurochemistry.

[52]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[53]  Solomon H. Snyder,et al.  Encephalopsin: A Novel Mammalian Extraretinal Opsin Discretely Localized in the Brain , 1999, The Journal of Neuroscience.

[54]  Masao Yoshida,et al.  Pinopsin expressed in the retinal photoreceptors of a diurnal gecko , 2001, FEBS letters.

[55]  B. Knox,et al.  Enhancement of opsin activity by all-trans-retinal. , 1998, Experimental eye research.

[56]  D. Oprian,et al.  Identification of the Cl(-)-binding site in the human red and green color vision pigments. , 1993, Biochemistry.

[57]  K. J. Fryxell The evolutionary divergence of neurotransmitter receptors and second-messenger pathways , 1995, Journal of Molecular Evolution.

[58]  E. Meyerowitz,et al.  The evolution fo rhodopsins and neurotransmitter receptors , 1991, Journal of Molecular Evolution.

[59]  R. Hara,et al.  Vision in Octopus and Squid: Rhodopsin and Retinochrome in the Octopus Retina , 1967, Nature.

[60]  I. Shimizu,et al.  A novel isoform of vertebrate ancient opsin in a smelt fish, Plecoglossus altivelis. , 2002, Biochemical and biophysical research communications.

[61]  H. Khorana,et al.  Structure and function in rhodopsin: kinetic studies of retinal binding to purified opsin mutants in defined phospholipid-detergent mixtures serve as probes of the retinal binding pocket. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[62]  D. Arendt,et al.  Ciliary Photoreceptors with a Vertebrate-Type Opsin in an Invertebrate Brain , 2004, Science.

[63]  J. Bellingham,et al.  Sequence, genomic structure and tissue expression of carp (Cyprinus carpio L.) vertebrate ancient (VA) opsin , 2000, FEBS letters.

[64]  J. Pokorny,et al.  Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN , 2005, Nature.

[65]  T. Zars,et al.  The drosophila dgq gene encodes a Gα protein that mediates phototransduction , 1994, Neuron.

[66]  W. P. Hayes,et al.  Melanopsin: An opsin in melanophores, brain, and eye. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Tsutomu Kouyama,et al.  Crystal structure of squid rhodopsin , 2008, Nature.

[68]  W. Gehring,et al.  Evolution and Functional Diversity of Jellyfish Opsins , 2008, Current Biology.

[69]  M. Jiang,et al.  An opsin homologue in the retina and pigment epithelium. , 1993, Investigative ophthalmology & visual science.

[70]  D. Arendt,et al.  Ciliary Photoreceptors with a Vertebrate-Type Opsin in an Invertebrate Brain , 2004, Science.

[71]  R. Foster,et al.  A novel and ancient vertebrate opsin , 1997, FEBS letters.

[72]  M. Sano,et al.  Interaction of GTP‐binding proteins with calmodulin , 1986, FEBS letters.

[73]  A. Terakita,et al.  Highly conserved glutamic acid in the extracellular IV-V loop in rhodopsins acts as the counterion in retinochrome, a member of the rhodopsin family. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[74]  C. D. Sauer,et al.  Pteropsin: a vertebrate-like non-visual opsin expressed in the honey bee brain. , 2005, Insect biochemistry and molecular biology.

[75]  T. Zars,et al.  The Drosophila dgq gene encodes a G alpha protein that mediates phototransduction. , 1994, Neuron.

[76]  Y. Fukada,et al.  Vertebrate Ancient-Long Opsin: A Green-Sensitive Photoreceptive Molecule Present in Zebrafish Deep Brain and Retinal Horizontal Cells , 2000, The Journal of Neuroscience.

[77]  K. Katoh,et al.  Molecular Evolution of Arthropod Color Vision Deduced from Multiple Opsin Genes of Jumping Spiders , 2008, Journal of Molecular Evolution.

[78]  Kosuke Takano,et al.  Jellyfish vision starts with cAMP signaling mediated by opsin-Gs cascade , 2008, Proceedings of the National Academy of Sciences.

[79]  K. Palczewski,et al.  Crystal Structure of Rhodopsin: A G‐Protein‐Coupled Receptor , 2002, Chembiochem : a European journal of chemical biology.

[80]  T. Sakmar,et al.  Spectroscopic evidence for interaction between transmembrane helices 3 and 5 in rhodopsin. , 1998, Biochemistry.

[81]  A. Terakita,et al.  Bistable UV pigment in the lamprey pineal. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[82]  Y. Koutalos,et al.  Regeneration of bovine and octopus opsins in situ with natural and artificial retinals. , 1989, Biochemistry.

[83]  K. Hofmann,et al.  Complex formation between metarhodopsin II and GTP‐binding protein in bovine protoreceptor membranes leads to a shift of the photoproduct equilibrium , 1982, FEBS letters.

[84]  H. Khorana,et al.  Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. , 1989, Proceedings of the National Academy of Sciences of the United States of America.