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The Evolution of Non-visual Photopigments in the Central Nervous System of Vertebrates

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Evolution of Visual and Non-visual Pigments

Part of the book series: Springer Series in Vision Research ((SSVR,volume 4))

Abstract

In addition to classical image-forming vision, the vertebrates exhibit a range of non-image-forming light detection systems that utilise opsin photopigments. Within the CNS these systems are present in a range of anatomical locations that include both eye and brain. In mammals the eye is both responsible and required for all commonly measured responses to light. By contrast, non-mammalian vertebrates possess a wide range of intrinsically photoreceptive sites. Members of the non-visual opsin family include exorhodopsin, pinopsin, vertebrate ancient opsin (VA), parietopsin, parapinopsin, teleost multiple tissue opsin (TMT), encephalopsin (OPN3), neuropsin (OPN5), peropsin, retinal G protein-coupled receptor (RGR) and melanopsin (OPN4). Opsin-based photopigments have evolved to mediate specific photoreceptive tasks in different light environments, each exhibit functional properties that are tuned to the biological task in which they are involved. Examination of the classes of opsin involved reveals a range of adaptions particularly in spectral sensitivity, chromophore handling and signalling mechanisms. The loss of extraocular light detection in the mammals is associated with an evolutionary reduction in the non-visual opsin representation in the mammalian genome. One clear exception to this is the retention of the melanopsin (OPN4M) gene and the expression of this opsin protein in a single class of mammalian retinal ganglion cell. Exploring the diversity of melanopsin proteins in the lower vertebrates suggests that the property of chromophore biochemistry and bistability does not necessarily define an opsin class and may have evolved more than once.

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References

  • Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Signaling through G-protein-linked cell-surface receptors. In: Molecular biology of the cell, 4th edn. New York: Garland Science. 2002.

    Google Scholar 

  • Arendt J. Melatonin and the pineal gland: influence on mammalian seasonal and circadian physiology. Rev Reprod. 1998;3:13–22.

    PubMed  CAS  Google Scholar 

  • Arendt D. The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet. 2008;9:868–82.

    PubMed  CAS  Google Scholar 

  • Arshavsky VY, Lamb TD, Pugh Jr EN. G proteins and phototransduction. Annu Rev Physiol. 2002;64:153–87.

    PubMed  CAS  Google Scholar 

  • Bagnara JT, Hadley ME. Endocrinology of the amphibian pineal. Integr Comp Biol. 1970;10:201–16.

    CAS  Google Scholar 

  • Barlow HB. Purkinje shift and retinal noise. Nature. 1957;179:255–6.

    PubMed  CAS  Google Scholar 

  • Barnard AR, Hattar S, Hankins MW, Lucas RJ. Melanopsin regulates visual processing in the mouse retina. Curr Biol. 2006;16:389–95.

    PubMed  CAS  Google Scholar 

  • Bellingham J, Foster RG. Opsins and mammalian photoentrainment. Cell Tissue Res. 2002;309: 57–71.

    PubMed  CAS  Google Scholar 

  • Bellingham J, Whitmore D, Philp AR, Wells DJ, Foster RG. Zebrafish melanopsin: isolation, tissue localisation and phylogenetic position. Mol Brain Res. 2002;107:128–36.

    PubMed  CAS  Google Scholar 

  • Bellingham J, Wells DJ, Foster RG. In silico characterisation and chromosomal localisation of human RRH (peropsin)–implications for opsin evolution. BMC Genomics. 2003;4:3.

    PubMed  PubMed Central  Google Scholar 

  • Bellingham J, Chaurasia SS, Melyan Z, Liu C, Cameron MA, Tarttelin EE, Iuvone PM, Hankins MW, Tosini G, Lucas RJ. Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. PLoS Biol. 2006;4:e254.

    PubMed  PubMed Central  Google Scholar 

  • Benoit J. Le role des yeux dans l’action stimulante de la lumiere sur le developpement testiculaire chez le canard. CR Soc Biol (Paris). 1935a;118:669–71.

    Google Scholar 

  • Benoit J. Stimulation par la lumiere artificielle du developpment testiculaire chez des canards aveugles par section du nerf optique. C R Seances Soc Biol Fil. 1935b;120:133–6.

    Google Scholar 

  • Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002;295:1070–3.

    PubMed  CAS  Google Scholar 

  • Blackshaw S, Snyder SH. Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family. J Neurosci. 1997;17:8083–92.

    PubMed  CAS  Google Scholar 

  • Blackshaw S, Snyder SH. Encephalopsin: a novel mammalian extraretinal opsin discretely localized in the brain. J Neurosci. 1999;19:3681–90.

    PubMed  CAS  Google Scholar 

  • Briggs WR, Spudich JL. Handbook of photosensory receptors. West Sussex: Wiley; 2006.

    Google Scholar 

  • Cheng N, Tsunenari T, Yau KW. Intrinsic light response of retinal horizontal cells of teleosts. Nature. 2009;460:899–903.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cowing JA, Arrese CA, Davies WL, Beazley LD, Hunt DM. Cone visual pigments in two marsupial species: the fat-tailed dunnart (Sminthopsis crassicaudata) and the honey possum (Tarsipes rostratus). Proc Biol Sci. 2008;275:1491–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokomy J, Yau KW, Gamlin PD. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature. 2005;433:749–54.

    PubMed  CAS  Google Scholar 

  • Davies WL, Carvalho LS, Cowing JA, Beazley LD, Hunt DM, ARRESE CA. Visual pigments of the platypus: a novel route to mammalian colour vision. Curr Biol. 2007;17:R161–3.

    PubMed  CAS  Google Scholar 

  • Davies WL, Hankins MW, Foster RG. Vertebrate ancient opsin and melanopsin: divergent irradiance detectors. Photochem Photobiol Sci. 2010;9:1444–57.

    PubMed  CAS  Google Scholar 

  • Davies WI, Turton M, Peirson SN, Follett BK, Halford S, Garcia-Fernandez JM, Sharp PJ, Hankins MW, Foster RG. Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response. Biol Lett. 2012a;8(2):291–4.

    PubMed  PubMed Central  Google Scholar 

  • Davies WI, Zheng L, Hughes S, Tamai TK, Turton M, Halford S, Foster RG, Whitmore D, Hankins MW. Functional diversity of melanopsins and their global expression in the teleost retina. Cell Mol Life Sci. 2011;68:4115–32.

    PubMed  CAS  Google Scholar 

  • Davies WI, Collin SP, Hunt DM. Molecular ecology and adaptation of visual photopigments in craniates. Mol Ecol. 2012b;21:3121–58.

    PubMed  CAS  Google Scholar 

  • Davies WI, Tay BH, Zheng L, Danks JA, Brenner S, Foster RG, Collin SP, Hankins MW, Venkatesh B, Hunt DM. Evolution and functional characterisation of melanopsins in a deep-sea chimaera (elephant shark, Callorhinchus milii). PLoS One. 2012c;7:e51276.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Diel S, Klass K, Wittig B, Kleuss C. Gbetagamma activation site in adenylyl cyclase type II. Adenylyl cyclase type III is inhibited by Gbetagamma. J Biol Chem. 2006;281:288–94.

    PubMed  CAS  Google Scholar 

  • Dodt E, Meissl H. The pineal and parietal organs of lower vertebrates. Experientia. 1982;38:996–1000.

    PubMed  CAS  Google Scholar 

  • Douglas RH, Partridge JC. On the visual pigments deep-sea fish. J Fish Biol. 1997;50:68–85.

    CAS  Google Scholar 

  • Engbretson GA. Neurobiology of the lacertilian parietal eye system. Ethol Ecol Evol. 1992;4: 89–107.

    Google Scholar 

  • Fain GL, Matthews HR, Cornwall MC, Koutalos Y. Adaptation in vertebrate photoreceptors. Physiol Rev. 2001;81:117–51.

    PubMed  CAS  Google Scholar 

  • Fasick JI, Cronin TW, Hunt DM, Robinson PR. The visual pigments of the bottlenose dolphin (Tursiops truncatus). Vis Neurosci. 1998;15:643–51.

    PubMed  CAS  Google Scholar 

  • Fernandes AM, Fero K, Arrenberg AB, Bergeron SA, Driever W, Burgess HA. Deep brain photoreceptors control light-seeking behavior in zebrafish larvae. Curr Biol. 2012;22:2042–7.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Fitzgibbon J, Hope A, Slobodyanyuk SJ, Bellingham J, Bowmaker JK, Hunt DM. The rhodopsin-encoding gene of bony fish lacks introns. Gene. 1995;164:273–7.

    PubMed  CAS  Google Scholar 

  • Foa A, Basaglia F, Beltrami G, Carnacina M, Moretto E, Bertolucci C. Orientation of lizards in a Morris water-maze: roles of the sun compass and the parietal eye. J Exp Biol. 2009;212: 2918–24.

    PubMed  Google Scholar 

  • Foster RG, Follett BK. The involvement of a rhodopsin-like photopigment in the photoperiodic response of the Japanese quail. J Comp Physiol. 1985;157:519–28.

    CAS  Google Scholar 

  • Foster RG, Menaker M. Circadian photoreception in mammals and other vertebrates. In: Wetterberg L, editor. Light and biological rhythms in man. New York: Pergamon; 1993. p. 73–91.

    Google Scholar 

  • Foster RC, Follett BK, Lythgoe JN. Rhodopsin-like sensitivity of extra-retinal photoreceptors mediating the photoperiodic response in quail. Nature. 1985;313:50–2.

    PubMed  CAS  Google Scholar 

  • Foster RG, Schalken JJ, Timmers AM, De Grip WJ. A comparison of some photoreceptor characteristics in the pineal and retina. I. The Japanese quail (Coturnix coturnix). J Comp Physiol A. 1989;165:553–63.

    Google Scholar 

  • Foster RG, Provencio I, Hudson D, Fiske S, De Grip W, Menaker M. Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A. 1991;169:39–50.

    PubMed  CAS  Google Scholar 

  • Foster RG, Grace MS, Provencio I, Degrip WJ, Garcia-Fernandez JM. Identification of vertebrate deep brain photoreceptors. Neurosci Biobehav Rev. 1994;18:541–6.

    PubMed  CAS  Google Scholar 

  • Foster RG, Provencio I, Bovee-Geurts PHM, Degrip WJ. The photoreceptive capacity of the developing pineal gland and eye of the golden hamster (Mesocricetus auratus). J Neuroendocrinol. 2003;15:355–63.

    PubMed  CAS  Google Scholar 

  • Freedman MS, Lucas RJ, Soni B, Von Schantz M, Muñoz M, David-Gray Z, Foster R. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science. 1999;284:502–4.

    PubMed  CAS  Google Scholar 

  • Frigato E, Vallone D, Bertolucci C, Foulkes NS. Isolation and characterization of melanopsin and pinopsin expression within photoreceptive sites of reptiles. Naturwissenschaften. 2006;93: 379–85.

    PubMed  CAS  Google Scholar 

  • Frisch KV. Beiträge zur Physiologie der Pigmentzellen in der Fischhaut. Pflug Arch. 1911;138: 319–87.

    Google Scholar 

  • Gamlin PD, McDougal DH, Pokorny J, Smith VC, Yau KW, Dacey DM. Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vision Res. 2007;47:946–54.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gerkema MP, Davies WI, Foster RG, Menaker M, Hut RA. The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc Biol Sci. 2013;280:20130508.

    PubMed  PubMed Central  Google Scholar 

  • Gu Y, Oberwinkler J, Postma M, Hardie RC. Mechanisms of light adaptation in Drosophila photoreceptors. Curr Biol. 2005;15:1228–34.

    PubMed  CAS  Google Scholar 

  • Güler AD, Ecker JL, Lall GS, Haq S, Altimus CM, Liao HW, Barnard AR, Cahill H, Badea TC, Zhao H, Hankins MW, Berson DM, Lucas RJ, Yau KW, Hattar S. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature. 2008;453:102–5.

    PubMed  PubMed Central  Google Scholar 

  • Halford S, Freedman MS, Bellingham J, Inglis SL, Poopalasundaram S, Soni BG, Foster RG, Hunt DM. Characterization of a novel human opsin gene with wide tissue expression and identification of embedded and flanking genes on chromosome 1q43. Genomics. 2001;72:203–8.

    PubMed  CAS  Google Scholar 

  • Halford S, Pires SS, Turton M, Zheng L, Gonzalez-Menendez I, Davies WL, Peirson SN, Garcia-Fernandez JM, Hankins MW, Foster RG. VA Opsin-Based Photoreceptors in the Hypothalamus of Birds. Curr Biol. 2009;19:1396–402.

    PubMed  CAS  Google Scholar 

  • Hankins MW, Lucas RJ. The primary visual pathway in humans is regulated according to long-term light exposure through the action of a nonclassical photopigment. Curr Biol. 2002;12: 191–8.

    PubMed  CAS  Google Scholar 

  • Hao W, Fong HKW. Blue and ultraviolet light-absorbing opsin from the retinal pigment epithelium. Biochemistry. 1996;35:6251–6.

    PubMed  CAS  Google Scholar 

  • Hara T, Hara R. Rhodopsin and retinochrome in the squid retina. Nature. 1967;214:573–5.

    PubMed  CAS  Google Scholar 

  • Hartwig HG, van Veen T. Spectral characteristics of visible radiation penetrating into the brain and stimulating extraretinal photoreceptors—transmission recordings in vertebrates. J Comp Physiol A. 1979;130:277–82.

    Google Scholar 

  • Hattar S, Liao HW, Takao M, Berson DM, Yau KW. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002;295:1065–70.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG, Yau KW. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature. 2003;424:76–81.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Heesy CP, Hall MI. The nocturnal bottleneck and the evolution of mammalian vision. Brain Behav Evol. 2010;75:195–203.

    PubMed  Google Scholar 

  • Hope AJ, Partridge JC, Dulai KS, Hunt DM. Mechanisms of wavelength tuning in the rod opsins of deep-sea fishes. Proc Biol Sci. 1997;264:155–63.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hughes S, Hankins MW, Foster RG, Peirson SN. Melanopsin phototransduction: slowly emerging from the dark. Prog Brain Res. 2012a;199:19–40.

    PubMed  CAS  Google Scholar 

  • Hughes S, Welsh L, Katti C, Gonzalez-Menendez I, Turton M, Halford S, Sekaran S, Peirson SN, Hankins MW, Foster RG. Differential expression of melanopsin isoforms Opn4L and Opn4S during postnatal development of the mouse retina. PLoS One. 2012b;7:e34531.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hunt DM, Dulai KS, Partridge JC, Cottrill P, Bowmaker JK. The molecular basis for spectral tuning of rod visual pigments in deep-sea fish. J Exp Biol. 2001;204:3333–44.

    PubMed  CAS  Google Scholar 

  • Hunt DM, Carvalho LS, Cowing JA, Davies WL. Evolution and spectral tuning of visual pigments in birds and mammals. Philos Trans R Soc Lond B Biol Sci. 2009;364:2941–55.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Isoldi MC, Rollag MD, De Lauro Castrucci AM, Provencio I. Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin. Proc Natl Acad Sci U S A. 2005;102: 1217–21.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jenkins A, Muñoz M, Tarttelin EE, Bellingham J, Foster RG, Hankins MW. VA opsin, melanopsin, and an inherent light response within retinal interneurons. Curr Biol. 2003;13:1269–78.

    PubMed  CAS  Google Scholar 

  • Jiang M, Pandey S, Fong HKW. An opsin homologue in the retina and pigment epithelium. Invest Ophthalmol Vis Sci. 1993;34:3669–78.

    PubMed  CAS  Google Scholar 

  • Kang SW, Leclerc B, Kosonsiriluk S, Mauro LJ, Iwasawa A, El Halawani ME. Melanopsin expression in dopamine-melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds. Neuroscience. 2010;170:200–13.

    PubMed  CAS  Google Scholar 

  • Kasai A, Oshima N. Light-sensitive motile iridophores and visual pigments in the neon tetra, Paracheirodon innesi. Zoolog Sci. 2006;23:815–9.

    PubMed  CAS  Google Scholar 

  • Kasper G, Taudien S, Staub E, Mennerich D, Rieder M, Hinzmann B, Dahl E, Schwidetzky U, Rosenthal A, Rump A. Different structural organization of the encephalopsin gene in man and mouse. Gene. 2002;295:27–32.

    PubMed  CAS  Google Scholar 

  • Kawamura S, Yokoyama S. Expression of visual and nonvisual opsins in American chameleon. Vision Res. 1997;37:1867–71.

    PubMed  CAS  Google Scholar 

  • Kemp TS. The origin and early radiation of the therapsid mammal-like reptiles: a palaeobiological hypothesis. J Evol Biol. 2006;19:1231–47.

    PubMed  CAS  Google Scholar 

  • Kojima D, Mano H, Fukada Y. Vertebrate ancient-Long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J Neurosci. 2000;20:2845–51.

    PubMed  CAS  Google Scholar 

  • Kojima D, Torii M, Fukada Y, Dowling JE. Differential expression of duplicated VAL-opsin genes in the developing zebrafish. J Neurochem. 2008;104:1364–71.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kojima D, Mori S, Torii M, Wada A, Morishita R, Fukada Y. UV-sensitive photoreceptor protein OPN5 in humans and mice. PLoS One. 2011;6:e26388.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Korf HW, Møller M. The innervation of the mammalian pineal gland with special reference to central pinealopetal projections. Pineal Res Rev. 1984;2:41–86.

    Google Scholar 

  • Korf HW, Foster RG, Ekstrom P, Schalken JJ. Opsin-like immunoreaction in the retinae and pineal organs of four mammalian species. Cell Tissue Res. 1985a;242:645–8.

    PubMed  CAS  Google Scholar 

  • Korf HW, Møller M, Gery I, Zigler JS, Klein DC. Immunocytochemical demonstration of retinal S-antigen in the pineal organ of four mammalian species. Cell Tissue Res. 1985b;239:81–5.

    PubMed  CAS  Google Scholar 

  • Korf HW, Schomerus C, Stehle JH. The pineal organ, its hormone melatonin, and the photoneuroendocrine system. Adv Anat Embryol Cell Biol. 1998;146:1–100.

    PubMed  CAS  Google Scholar 

  • Koyanagi M, Terakita A, Kubokawa K, Shichida Y. Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis- and all-trans-retinals as their chromophores. FEBS Lett. 2002;531:525–8.

    PubMed  CAS  Google Scholar 

  • Koyanagi M, Kawano E, Kinugawa Y, Oishi T, Shichida Y, Tamotsu S, Terakita A. Bistable UV pigment in the lamprey pineal. Proc Natl Acad Sci U S A. 2004;101:6687–91.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Koyanagi M, Takada E, Nagata T, Tsukamoto H, Terakita A. Homologs of vertebrate Opn3 potentially serve as a light sensor in nonphotoreceptive tissue. Proc Natl Acad Sci U S A. 2013;110:4998–5003.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lucas SG, Luo Z. Adelobasileus from the Upper Triassic of West Texas: the oldest mammal. J Vert Paleontol. 1993;13:309–34.

    Google Scholar 

  • Lucas RJ, Freedman MS, Munoz M, Garcia-Fernandez JM, Foster RG. Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science. 1999;284:505–7.

    PubMed  CAS  Google Scholar 

  • Lucas RJ, Douglas RH, Foster RG. Characterization of an ocular photopigment capable of driving pupillary constriction in mice. Nat Neurosci. 2001;4:621–6.

    PubMed  CAS  Google Scholar 

  • Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau KW. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science. 2003;299:245–7.

    PubMed  CAS  Google Scholar 

  • Lupi D, Oster H, Thompson S, Foster RG. The acute light-induction of sleep is mediated by OPN4-based photoreception. Nat Neurosci. 2008;11:1068–73.

    PubMed  CAS  Google Scholar 

  • Lythgoe JN. The ecology of vision. Oxford: Clarendon; 1979.

    Google Scholar 

  • Lythgoe JN. Aspects of photoreception in aquatic environments. Symp Soc Exp Biol. 1985;39:373–86.

    PubMed  CAS  Google Scholar 

  • Maeda T, Van Hooser JP, Driessen CAGG, Filipek S, Janssen JJM, Palczewski K. Evaluation of the role of the retinal G protein-coupled receptor (RGR) in the vertebrate retina in vivo. J Neurochem. 2003;85:944–56.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Mano H, Kojima D, Fukada Y. Exo-rhodopsin: a novel rhodopsin expressed in the zebrafish pineal gland. Mol Brain Res. 1999;73:110–8.

    PubMed  CAS  Google Scholar 

  • Max M, McKinnon PJ, Seidenman KJ, Barrett RK, Applebury ML, Takahashi JS, Margolskee RF. Pineal opsin: a nonvisual opsin expressed in chick pineal. Science. 1995;267:1502–6.

    PubMed  CAS  Google Scholar 

  • Max M, Surya A, Takahashi JS, Margolskee RF, Knox BE. Light-dependent activation of rod transducin by pineal opsin. J Biol Chem. 1998;273:26820–6.

    PubMed  CAS  Google Scholar 

  • Meissl H. Photic regulation of pineal function. Analogies between retinal and pineal photoreception. Biol Cell. 1997;89:549–54.

    PubMed  CAS  Google Scholar 

  • Meissl H, Ueck M. Extra-ocular photoreception of the pineal-gland of the aquatic turtle Pseudemys-Scripta-Elegans. J Comp Physiol. 1980;140:173–9.

    Google Scholar 

  • Melchior B, Frangos JA. Galphaq/11-mediated intracellular calcium responses to retrograde flow in endothelial cells. Am J Physiol Cell Physiol. 2012;303:C467–73.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW. Addition of human melanopsin renders mammalian cells photoresponsive. Nature. 2005;433:741–5.

    PubMed  CAS  Google Scholar 

  • Menaker M, Underwood H. Extraretinal photoreception in birds. Photophysiology. 1976;23: 299–306.

    PubMed  CAS  Google Scholar 

  • Meredith RW, Gatesy J, Emerling CA, York VM, Springer MS. Rod monochromacy and the coevolution of cetacean retinal opsins. PLoS Genet. 2013;9:e1003432.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Minamoto T, Shimizu I. A novel isoform of vertebrate ancient opsin in a smelt fish, Plecoglossus altivelis. Biochem Biophys Res Commun. 2002;290:280–6.

    PubMed  CAS  Google Scholar 

  • Morimura H, Saindelle-Ribeaudeau F, Berson EL, Dryja TP. Mutations in RGR, encoding a light-sensitive opsin homologue, in patients with retinitis pigmentosa. Nat Genet. 1999;23: 393–4.

    PubMed  CAS  Google Scholar 

  • Moutsaki P, Bellingham J, Soni BG, David-Gray ZK, Foster RG. Sequence, genomic structure and tissue expression of carp (Cyprinus carpio L.) vertebrate ancient (VA) opsin. FEBS Lett. 2000;473:316–22.

    PubMed  CAS  Google Scholar 

  • Moutsaki P, Whitmore D, Bellingham J, Sakamoto K, David-Gray ZK, Foster RG. Teleost multiple tissue (tmt) opsin: a candidate photopigment regulating the peripheral clocks of zebrafish? Mol Brain Res. 2003;112:135–45.

    PubMed  CAS  Google Scholar 

  • Mure LS, Cornut PL, Rieux C, Drouyer E, Denis P, Gronfier C, Cooper HM. Melanopsin bistability: a fly’s eye technology in the human retina. PLoS One. 2009;4:e5991.

    PubMed  PubMed Central  Google Scholar 

  • Nagata T, Koyanagi M, Tsukamoto H, Terakita A. Identification and characterization of a protostome homologue of peropsin from a jumping spider. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2010;196:51–9.

    PubMed  CAS  Google Scholar 

  • Nakamura A, Kojima D, Imai H, Terakita A, Okano T, Shichida Y, Fukada Y. Chimeric nature of pinopsin between rod and cone visual pigments. Biochemistry. 1999;38:14738–45.

    PubMed  CAS  Google Scholar 

  • Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S, Hirunagi K, Ebihara S, Kubo Y, Yoshimura T. A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc Natl Acad Sci U S A. 2010;107:15264–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Nakatani Y, Morishita S. Comparing the human and fish genomes, Encylopedia of life sciences. Chichester: Wiley; 2008.

    Google Scholar 

  • Nathans J. Determinants of visual pigment absorbance: identification of the retinylidene Schiff’s base counterion in bovine rhodopsin. Biochemistry. 1990;29:9746–52.

    PubMed  CAS  Google Scholar 

  • Nelson RJ, Zucker I. Absence of extraocular photoreception in diurnal and nocturnal rodents exposed to direct sunlight. Comp Biochem Physiol A. 1981;69:145–8.

    Google Scholar 

  • Nieto PS, Valdez DJ, Acosta-Rodriguez VA, Guido ME. Expression of novel opsins and intrinsic light responses in the mammalian retinal ganglion cell line RGC-5. Presence of OPN5 in the rat retina. PLoS One. 2011;6:e26417.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Nishimura T, Okano H, Tada H, Nishimura E, Sugimoto K, Mohri K, Fukushima M. Lizards respond to an extremely low-frequency electromagnetic field. J Exp Biol. 2010;213:1985–90.

    PubMed  Google Scholar 

  • Nissila J, Manttari S, Sarkioja T, Tuominen H, Takala T, Timonen M, Saarela S. Encephalopsin (OPN3) protein abundance in the adult mouse brain. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2012;198:833–9.

    PubMed  PubMed Central  Google Scholar 

  • Ohuchi H, Yamashita T, Tomonari S, Fujita-Yanagibayashi S, Sakai K, Noji S, Shichida Y. A non-mammalian type opsin 5 functions dually in the photoreceptive and non-photoreceptive organs of birds. PLoS One. 2012;7:e31534.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Okano T, Yoshizawa T, Fukada Y. Pinopsin is a chicken pineal photoreceptive molecule. Nature. 1994;372:94–7.

    PubMed  CAS  Google Scholar 

  • Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M. Crystal structure of rhodopsin: a G protein-coupled receptor. Science. 2000;289:739–45.

    PubMed  CAS  Google Scholar 

  • Panda S, Sato TK, Castrucci AM, Rollag MD, Degrip WJ, Hogenesch JB, Provencio I, Kay SA. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science. 2002;298:2213–6.

    PubMed  CAS  Google Scholar 

  • Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T. Illumination of the melanopsin signaling pathway. Science. 2005;307:600–4.

    PubMed  CAS  Google Scholar 

  • Pandey S, Blanks JC, Spee C, Jiang M, Fong HKW. Cytoplasmic retinal localization of an evolutionary homolog of the visual pigments. Exp Eye Res. 1994;58:605–13.

    PubMed  CAS  Google Scholar 

  • Peirson SN, Oster H, Jones SL, Leitges M, Hankins MW, Foster RG. Microarray analysis and functional genomics identify novel components of melanopsin signaling. Curr Biol. 2007;17:1363–72.

    PubMed  CAS  Google Scholar 

  • Philp AR, Bellingham J, Garcia-Fernandez JM, Foster RG. A novel rod-like opsin isolated from the extra-retinal photoreceptors of teleost fish. FEBS Lett. 2000a;468:181–8.

    PubMed  CAS  Google Scholar 

  • Philp AR, Garcia-Fernandez JM, Soni BG, Lucas RJ, Bellingham J, Foster RG. Vertebrate ancient (VA) opsin and extraretinal photoreception in the Atlantic salmon (Salmo salar). J Exp Biol. 2000b;203:1925–36.

    PubMed  CAS  Google Scholar 

  • Pires SS, Shand J, Bellingham J, Arrese C, Turton M, Peirson S, Foster RG, Halford S. Isolation and characterization of melanopsin (Opn4) from the Australian marsupial Sminthopsis crassicaudata (fat-tailed dunnart). Proc Biol Sci. 2007;274:2791–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pires SS, Hughes S, Turton M, Melyan Z, Peirson SN, Zheng L, Kosmaoglou M, Bellingham J, Cheetham ME, Lucas RJ, Foster RG, Hankins MW, Halford S. Differential expression of two distinct functional isoforms of melanopsin (Opn4) in the mammalian retina. J Neurosci. 2009;29:12332–42.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Provencio I, Jiang G, De Grip WJ, Pär Hayes W, Rollag MD. Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A. 1998;95:340–5.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. A novel human opsin in the inner retina. J Neurosci. 2000;20:600–5.

    PubMed  CAS  Google Scholar 

  • Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, Provencio I, Berson DM. Induction of photosensitivity by heterologous expression of melanopsin. Nature. 2005;433:745–9.

    PubMed  CAS  Google Scholar 

  • Quay WB. The parietal eye-pineal complex. London: Academic Press; 1979.

    Google Scholar 

  • Radu RA, Hu J, Peng J, Bok D, Mata NL, Travis GH. 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. J Biol Chem. 2008;283: 19730–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rivolta C, Berson EL, Dryja TP. Mutation screening of the peropsin gene, a retinal pigment epithelium specific rhodopsin homolog, in patients with retinitis pigmentosa and allied diseases. Mol Vis. 2006;12:1511–5.

    PubMed  CAS  Google Scholar 

  • Rollag MD, Provencio I, Sugden D, Green CB. Cultured amphibian melanophores: a model system to study melanopsin photobiology. Methods Enzymol. 2000;316:291–309.

    PubMed  CAS  Google Scholar 

  • Romer AS. The vertebrate body. Philadelphia: W.B. Saunders; 1970.

    Google Scholar 

  • Ruby NF, Brennan TJ, Xie X, Cao V, Franken P, Heller HC, O’Hara BF. Role of melanopsin in circadian responses to light. Science. 2002;298:2211–3.

    PubMed  CAS  Google Scholar 

  • Sakai K, Imamoto Y, Su CY, Tsukamoto H, Yamashita T, Terakita A, Yau KW, Shichida Y. Photochemical nature of parietopsin. Biochemistry. 2012;51:1933–41.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sato K, Yamashita T, Ohuchi H, Shichida Y. Vertebrate ancient-long opsin has molecular properties intermediate between those of vertebrate and invertebrate visual pigments. Biochemistry. 2011;50:10484–90.

    PubMed  CAS  Google Scholar 

  • Schertler GF. Structure of rhodopsin and the metarhodopsin I photointermediate. Curr Opin Struct Biol. 2005;15:408–15.

    PubMed  CAS  Google Scholar 

  • Sekaran S, Foster RG, Lucas RJ, Hankins MW. Calcium imaging reveals a network of intrinsically light-sensitive inner-retinal neurons. Curr Biol. 2003;13:1290–8.

    PubMed  CAS  Google Scholar 

  • Sekaran S, Lupi D, Jones SL, Sheely CJ, Hattar S, Yau KW, Lucas RJ, Foster RG, Hankins MW. Melanopsin-dependent photoreception provides earliest light detection in the mammalian retina. Curr Biol. 2005;15:1099–107.

    PubMed  CAS  Google Scholar 

  • Semyonov J, Park JI, Chang CL, Hsu SY. GPCR genes are preferentially retained after whole genome duplication. PLoS One. 2008;3:e1903.

    PubMed  PubMed Central  Google Scholar 

  • Shand J, Foster RG. The extraretinal photoreceptors of non-mammalian vertebrates. In: Archer SN, Djamgoz MBA, Leow ER, Partridge JC, Vallerga S, editors. Adaptive mechanisms in the ecology of vision. Forlag: Kluwer; 1999. p. 197–222.

    Google Scholar 

  • Shand J, Lythgoe JN. The isolated iridescent cornea of the sand goby is photoresponsive. Photochem Photobiol. 1990;51:737–9.

    PubMed  CAS  Google Scholar 

  • Silver R, Witkovsky P, Horvath P, Alones V, Barnstable CJ, Lehman MN. Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res. 1988;253:189–98.

    PubMed  CAS  Google Scholar 

  • Solessio E, Engbretson GA. Antagonistic chromatic mechanisms in photoreceptors of the parietal eye of lizards. Nature. 1993;364:442–5.

    PubMed  CAS  Google Scholar 

  • Sollars PJ, Smeraski CA, Kaufman JD, Ogilvie MD, Provencio I, Pickard GE. Melanopsin and non-melanopsin expressing retinal ganglion cells innervate the hypothalamic suprachiasmatic nucleus. Vis Neurosci. 2003;20:601–10.

    PubMed  Google Scholar 

  • Soni BG, Foster RG. A novel and ancient vertebrate opsin. FEBS Lett. 1997;406:279–83.

    PubMed  CAS  Google Scholar 

  • Soni BG, Philp AR, Foster RG, Knox BE. Novel retinal photoreceptors. Nature. 1998;394:27–8.

    PubMed  CAS  Google Scholar 

  • Starace DM, Knox BE. Cloning and expression of a Xenopus short wavelength cone pigment. Exp Eye Res. 1998;67:209–20.

    PubMed  CAS  Google Scholar 

  • Su CY, Luo DG, Terakita A, Shichida Y, Liao HW, Kazmi MA, Sakmar TP, Yau KW. Parietal-eye phototransduction components and their potential evolutionary implications. Science. 2006;311:1617–21.

    PubMed  CAS  Google Scholar 

  • Sun H, Gilbert DJ, Copeland NG, Jenkins NA, Nathans J. Peropsin, a novel visual pigment-like protein located in the apical microvilli of the retinal pigment epithelium. Proc Natl Acad Sci U S A. 1997;94:9893–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Takashima N, Fujioka A, Hayasaka N, Matsuo A, Takasaki J, Shigeyoshi Y. Gq/11-induced intracellular calcium mobilization mediates Per2 acute induction in Rat-1 fibroblasts. Genes Cells. 2006;11:1039–49.

    PubMed  CAS  Google Scholar 

  • Tang WJ, Gilman AG. Type-specific regulation of adenylyl cyclase by G protein beta gamma subunits. Science. 1991;254:1500–3.

    PubMed  CAS  Google Scholar 

  • Taniguchi Y, Hisatomi O, Yoshida M, Tokunaga F. Pinopsin expressed in the retinal photoreceptors of a diurnal gecko. FEBS Lett. 2001;496:69–74.

    PubMed  CAS  Google Scholar 

  • Tarttelin EE, Bellingham J, Hankins MW, Foster RG, Lucas RJ. Neuropsin (Opn5): a novel opsin identified in mammalian neural tissue. FEBS Lett. 2003;554:410–6.

    PubMed  CAS  Google Scholar 

  • Tarttelin EE, Fransen MP, Edwards PC, Hankins MW, Schertler GF, Vogel R, Lucas RJ, Bellingham J. Adaptation of pineal expressed teleost exo-rod opsin to non-image forming photoreception through enhanced Meta II decay. Cell Mol Life Sci. 2011;68:3713–23.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Terakita A, Yamashita T, Shichida Y. Highly conserved glutamic acid in the extracellular IV-V loop in rhodopsins acts as the counterion in retinochrome, a member of the rhodopsin family. Proc Natl Acad Sci U S A. 2000;97:14263–7.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Terakita A, Koyanagi M, Tsukamoto H, Yamashita T, Miyata T, Shichida Y. Counterion displacement in the molecular evolution of the rhodopsin family. Nat Struct Mol Biol. 2004;11:284–9.

    PubMed  CAS  Google Scholar 

  • Terakita A, Kawano-Yamashita E, Koyanagi M. Evolution and diversity of opsins. WIREs Membr Transp Signal. 2012;1:104–11.

    CAS  Google Scholar 

  • Tomonari S, Takagi A, Akamatsu S, Noji S, Ohuchi H. A non-canonical photopigment, melanopsin, is expressed in the differentiating ganglion, horizontal, and bipolar cells of the chicken retina. Dev Dyn. 2005;234:783–90.

    PubMed  CAS  Google Scholar 

  • Tosini G, Menaker M. The pineal complex and melatonin affect the expression of the daily rhythm of behavioral thermoregulation in the green iguana. J Comp Physiol A. 1996;179:135–42.

    PubMed  CAS  Google Scholar 

  • van Veen T, Hartwig HG, Müller K. Light-dependent motor activity and photonegative behavior in the eel (Anguilla anguilla L.)—evidence for extraretinal and extrapineal photoreception. J Comp Physiol A. 1976;111:209–19.

    Google Scholar 

  • Vigh B, Vigh-Teichmann I. Comparitive neurohistology and immunohistochemistry of the pineal complex with special reference to CSF-contacting neuronal structures. Pineal Res Rev. 1988;6:1–65.

    Google Scholar 

  • Vigh-Teichmann I, Korf HW, Oksche A, Vigh B. Opsin-immunoreactive outer segments and acetylcholinesterase-positive neurons in the pineal complex of Phoxinus phoxinus (Teleostei, Cyprinidae). Cell Tissue Res. 1982;227:351–69.

    PubMed  CAS  Google Scholar 

  • Vigh-Teichmann I, Korf HW, Nürnberger F, Oksche A, Vigh B, Olsson R. Opsin-immunoreactive outer segments in the pineal and parapineal organs of the lamprey (Lampetra fluviatilis), the eel (Anguilla anguilla), and the rainbow trout (Salmo gairdneri). Cell Tissue Res. 1983;230: 289–307.

    PubMed  CAS  Google Scholar 

  • Vollrath L. The pineal organ. In: Oksche A, Vollrath L, editors. Handbuch der mikroskopischen Anatomie Des meschen. Berlin: Springer; 1981.

    Google Scholar 

  • Vought BW, Dukkipatti A, Max M, Knox BE, Birge RR. Photochemistry of the primary event in short-wavelength visual opsins at low temperature. Biochemistry. 1999;38:11287–97.

    PubMed  CAS  Google Scholar 

  • Wada S, Kawano-Yamashita E, Koyanagi M, Terakita A. Expression of UV-sensitive parapinopsin in the iguana parietal eyes and its implication in UV-sensitivity in vertebrate pineal-related organs. PLoS One. 2012;7:e39003.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Walls GD. The vertebrate eye and its adaptive radiation. New York: Hafner; 1942.

    Google Scholar 

  • Wang G, Wingfield JC. Immunocytochemical study of rhodopsin-containing putative encephalic photoreceptors in house sparrow, Passer domesticus. Gen Comp Endocrinol. 2011;170: 589–96.

    PubMed  CAS  Google Scholar 

  • Weber W. Photosensitivity of chromatophores. Integr Comp Biol. 1983;23:495–506.

    Google Scholar 

  • White JH, Chiano M, Wigglesworth M, Geske R, Riley J, White N, Hall S, Zhu G, Maurio F, Savage T, Anderson W, Cordy J, Ducceschi M, Vestbo J, Pillai SG, Barnes KC, Carlsen K, Gerritsen J, Lenney W, Silverman M, Sly P, Sundy J, Tsanakas J, von Berg A, Whyte M, Helms PJ. Identification of a novel asthma susceptibility gene on chromosome 1qter and its functional evaluation. Hum Mol Genet. 2008;17:1890–903.

    PubMed  CAS  Google Scholar 

  • Whitmore D, Foulkes NS, Sassone-Corsi P. Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature. 2000;404:87–91.

    PubMed  CAS  Google Scholar 

  • Wolken JJ, Mogus MA. Extraocular photosensitivity. Photochem Photobiol. 1979;29:189–90.

    Google Scholar 

  • Wong KY. A retinal ganglion cell that can signal irradiance continuously for 10 hours. J Neurosci. 2012;32:11478–85.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yamashita T, Ohuchi H, Tomonari S, Ikeda K, Sakai K, Shichida Y. Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. Proc Natl Acad Sci U S A. 2010;107: 22084–9.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yan EC, Kazmi MA, Ganim Z, Hou JM, Pan D, Chang BS, Sakmar TP, Mathies RA. Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc Natl Acad Sci U S A. 2003;100:9262–7.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yau KW, Hardie RC. Phototransduction Motifs and Variations. Cell. 2009;139:246–64.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yokoyama S, Zhang H. Cloning and characterization of the pineal gland-specific opsin gene of marine lamprey (Petromyzon marinus). Gene. 1997;202:89–93.

    PubMed  CAS  Google Scholar 

  • Yoshikawa T, Okano T, Oishi T, Fukada Y. A deep brain photoreceptive molecule in the toad hypothalamus. FEBS Lett. 1998;424:69–72.

    PubMed  Google Scholar 

  • Young JZ. The life of vertebrates. Oxford: Clarendon Press; 1981.

    Google Scholar 

  • Zhu L, Imanishi Y, Filipek S, Alekseev A, Jastrzebska B, Sun W, Saperstein DA, Palczewski K. Autosomal recessive retinitis pigmentosa and E150K mutation in the opsin gene. J Biol Chem. 2006;281:22289–98.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Zhukovsky EA, Oprian DD. Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science. 1989;246:928–30.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neurosciences, Levels 5-6 West Wing, University of Oxford, John Radcliffe Hospital, Oxford, OX3 9DU, UK

    Mark W. Hankins B.Sc. Hons., Ph.D. & Russell G. Foster B.Sc., Ph.D.

  2. School of Animal Biology and the University of Western Australia Oceans Institute, University of Western Australia, Perth, WA, Australia

    Wayne I. L. Davies B.A. (Hons.), M.A., Ph.D. (Cantab.)

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  1. Mark W. Hankins B.Sc. Hons., Ph.D.
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  2. Wayne I. L. Davies B.A. (Hons.), M.A., Ph.D. (Cantab.)
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  3. Russell G. Foster B.Sc., Ph.D.
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Correspondence to Mark W. Hankins B.Sc. Hons., Ph.D. .

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  1. School of Animal Biology, The University of Western Australia, Crawley, Australia

    David M. Hunt

  2. Department of Ophthalmology, University of Oxford, Oxford, United Kingdom

    Mark W. Hankins

  3. School of Animal Biology, The University of Western Australia, Crawley, West Australia, Australia

    Shaun P Collin

  4. Queensland Brain Institute, The University of Queensland, Brisbane, Australia

    N. Justin Marshall

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Hankins, M.W., Davies, W.I.L., Foster, R.G. (2014). The Evolution of Non-visual Photopigments in the Central Nervous System of Vertebrates. In: Hunt, D., Hankins, M., Collin, S., Marshall, N. (eds) Evolution of Visual and Non-visual Pigments. Springer Series in Vision Research, vol 4. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-4355-1_3

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