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The Evolution and Function of Melanopsin in Craniates

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Book cover Evolution of Visual and Non-visual Pigments

Abstract

In addition to well-characterised visual systems, many organisms, including the craniates, possess a complex sensory system of non-visual photoreceptors that detect light for a diverse array of non-image-forming tasks. Like the photoreceptors of image-forming systems, the pigments contained within non-visual photoreceptive cells comprise a protein component (opsin) linked to a light-sensitive retinal chromophore derived from vitamin A. In mammals, one of the most important of these non-visual pigments is melanopsin (encoded by the OPN4 gene, specifically that of the “mammal-like” or “m-class”), which is restricted in expression to a subset of retinal ganglion cells and has been shown to be the conduit through which light regulates many physiological activities, including the photoentrainment of circadian systems (e.g. the sleep cycle) and the pupillary reflex response. In non-mammals, melanopsin exists as two distinct gene lineages, namely the m-class and x-class (“Xenopus-like”), and both are expressed in many different tissues, including the eyes, skin, fins, gills, brain and pineal gland; however, the functional roles mediated by melanopsin in these “lower” vertebrates remain to be fully elucidated. In this review, we discuss the evolutionary history of the melanopsin gene, its diverse patterns of expression and transcriptional output, the functional roles so far determined, and the clinical significance of this critical and phylogenetically most ancient opsin-based system of irradiance detection.

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References

  • Adamski FM, Timms KM, Shieh BH. A unique isoform of phospholipase Cbeta4 highly expressed in the cerebellum and eye. Biochim Biophys Acta. 1999;1444:55–60.

    PubMed  CAS  Google Scholar 

  • Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH. Zebrafish hox clusters and vertebrate genome evolution. Science. 1998;282:1711–4.

    PubMed  CAS  Google Scholar 

  • Archibald NK, Clarke MP, Mosimann UP, Burn DJ. The retina in Parkinson’s disease. Brain. 2009;132:1128–45.

    PubMed  Google Scholar 

  • Arendt D. Evolution of eyes and photoreceptor cell types. Int J Dev Biol. 2003;47:563–71.

    PubMed  Google Scholar 

  • Arendt D, Wittbrodt J. Reconstructing the eyes of Urbilateria. Philos Trans R Soc Lond B Biol Sci. 2001;356:1545–63.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science. 2004;306:869–71.

    PubMed  CAS  Google Scholar 

  • Arendt D, Hausen H, Purschke G. The ‘division of labour’ model of eye evolution. Philos Trans R Soc Lond B Biol Sci. 2009;364:2809–17.

    PubMed  PubMed Central  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, Obika M. Light sensitivity of melanophores in neural crest explants. Experientia. 1967;23:155–7.

    PubMed  CAS  Google Scholar 

  • Bailes HJ, Lucas RJ. Melanopsin and inner retinal photoreception. Cell Mol Life Sci. 2010;67:99–111.

    PubMed  CAS  Google Scholar 

  • Bailes HJ, Lucas RJ. Human melanopsin forms a pigment maximally sensitive to blue light (λ max ≈ 479 nm) supporting activation of Gq/11 and Gi/o signalling cascades. Proc Biol Sci. 2013;280:20122987.

    PubMed  PubMed Central  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. Brain Res Mol Brain Res. 2002;107:128–36.

    PubMed  CAS  Google Scholar 

  • Bellingham J, Tarttelin EE, Foster RG, Wells DJ. Structure and evolution of the teleost extraretinal rod-like opsin (errlo) and ocular rod opsin (rho) genes: is teleost rho a retrogene? J Exp Zool B Mol Dev Evol. 2003a;297:1–10.

    PubMed  Google Scholar 

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

  • Benarroch EE. The melanopsin system: Phototransduction, projections, functions, and clinical implications. Neurology. 2011;76:1422–7.

    PubMed  Google Scholar 

  • Berisha F, Feke GT, Trempe CL, McMeel JW, Schepens CL. Retinal abnormalities in early Alzheimer’s disease. Invest Ophthalmol Vis Sci. 2007;48:2285–9.

    PubMed  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 

  • Berson DM, Castrucci AM, Provencio I. Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J Comp Neurol. 2010;518:2405–22.

    PubMed  PubMed Central  Google Scholar 

  • Biel M, Seeliger M, Pfeifer A, Kohler K, Gerstner A, Ludwig A, Jaissle G, Fauser S, Zrenner E, Hofmann F. Selective loss of cone function in mice lacking the cyclic nucleotide-gated channel CNG3. Proc Natl Acad Sci U S A. 1999;96:7553–7.

    PubMed  CAS  PubMed Central  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 

  • Blasic Jr JR, Brown RL, Robinson PR. Phosphorylation of mouse melanopsin by protein kinase A. PLoS One. 2012a;7:e45387.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Blasic Jr JR, Lane Brown R, Robinson PR. Light-dependent phosphorylation of the carboxy tail of mouse melanopsin. Cell Mol Life Sci. 2012b;69:1551–62.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bodis-Wollner I. Retinopathy in parkinson disease. J Neural Transm. 2009;116:1493–501.

    PubMed  Google Scholar 

  • Borges R, Johnson WE, O’Brien SJ, Vasconcelos V, Antunes A. The role of gene duplication and unconstrained selective pressures in the melanopsin gene family evolution and vertebrate circadian rhythm regulation. PLoS One. 2012;7:e52413.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bowes C, Li T, Danciger M, Baxter LC, Applebury ML, Farber DB. Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature. 1990;347:677–80.

    PubMed  CAS  Google Scholar 

  • Bowmaker JK. Evolution of vertebrate visual pigments. Vision Res. 2008;48:2022–41.

    PubMed  CAS  Google Scholar 

  • Briggs WR, Spudich JL. Handbook of photosensory receptors. Weinheim: Wiley VCH; 2005.

    Google Scholar 

  • Brown RL, Robinson PR. Melanopsin–shedding light on the elusive circadian photopigment. Chronobiol Int. 2004;21:189–204.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Burns A, Allen H, Tomenson B, Duignan D, Byrne J. Bright light therapy for agitation in dementia: a randomized controlled trial. Int Psychogeriatr. 2009;21:711–21.

    PubMed  Google Scholar 

  • Cajochen C, Munch M, Knoblauch V, Blatter K, Wirz-Justice A. Age-related changes in the circadian and homeostatic regulation of human sleep. Chronobiol Int. 2006;23:461–74.

    PubMed  Google Scholar 

  • Carrier J, Paquet J, Morettini J, Touchette E. Phase advance of sleep and temperature circadian rhythms in the middle years of life in humans. Neurosci Lett. 2002;320:1–4.

    PubMed  CAS  Google Scholar 

  • Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R, Natesan A, Zatz M, Tosini G, Liu C, Korf HW, Iuvone PM, Provencio I. Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J Neurochem. 2005;92:158–70.

    PubMed  CAS  Google Scholar 

  • Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GT, Batschauer A, Ahmad M. The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol. 2011;62:335–64.

    PubMed  CAS  Google Scholar 

  • Chen SK, Badea TC, Hattar S. Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature. 2011;476:92–5.

    PubMed  CAS  PubMed Central  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 

  • Chuang AT, Margo CE, Greenberg PB (2014) Retinal implants: a systematic review. Br J Ophthalmol

    Google Scholar 

  • Chyb S, Hevers W, Forte M, Wolfgang WJ, Selinger Z, Hardie RC. Modulation of the light response by cAMP in Drosophila photoreceptors. J Neurosci. 1999a;19:8799–807.

    PubMed  CAS  Google Scholar 

  • Chyb S, Raghu P, Hardie RC. Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature. 1999b;397:255–9.

    PubMed  CAS  Google Scholar 

  • Collin SP, Knight MA, Davies WL, Potter IC, Hunt DM, Trezise AE. Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol. 2003;13:R864–5.

    PubMed  CAS  Google Scholar 

  • Collin SP, Davies WL, Hart NS, Hunt DM. The evolution of early vertebrate photoreceptors. Philos Trans R Soc Lond B Biol Sci. 2009;364:2925–40.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Contin MA, Verra DM, Guido ME. An invertebrate-like phototransduction cascade mediates light detection in the chicken retinal ganglion cells. FASEB J. 2006;20:2648–50.

    PubMed  CAS  Google Scholar 

  • Dacey DM, Liao HW, Peterson BB, Robinson FR, Smith VC, Pokorny 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 

  • David-Gray ZK, Janssen JW, DeGrip WJ, Nevo E, Foster RG. Light detection in a ‘blind’ mammal. Nat Neurosci. 1998;1:655–6.

    PubMed  CAS  Google Scholar 

  • Davies WL (2011) Adaptive gene loss in vertebrates: photosensitivity as a model case. Encyclopedia of Life Sciences. http://www.els.net/WileyCDA/ElsArticle/refId-a0022890.html

  • Davies WL, Cowing JA, Carvalho LS, Potter IC, Trezise AE, Hunt DM, Collin SP. Functional characterization, tuning, and regulation of visual pigment gene expression in an anadromous lamprey. FASEB J. 2007;21:2713–24.

    PubMed  CAS  Google Scholar 

  • Davies WL, Carvalho LS, Tay BH, Brenner S, Hunt DM, Venkatesh B. Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res. 2009a;19:415–26.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Davies WL, Collin SP, Hunt DM. Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. Mol Biol Evol. 2009b;26:1803–9.

    PubMed  CAS  Google Scholar 

  • Davies WL, Cowing JA, Bowmaker JK, Carvalho LS, Gower DJ, Hunt DM. Shedding light on serpent sight: the visual pigments of Henophidian snakes. J Neurosci. 2009c;29:7519–25.

    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, 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. 2012a;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. 2012b;7:e51276.

    PubMed  CAS  PubMed Central  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. 2012c;8:291–4.

    PubMed  PubMed Central  Google Scholar 

  • Davies WL, Foster RG, Hankins MW. Focus on molecules: Melanopsin. Exp Eye Res. 2012d;97:161–2.

    PubMed  CAS  Google Scholar 

  • Davignon I, Barnard M, Gavrilova O, Sweet K, Wilkie TM. Gene structure of murine Gna11 and Gna15: tandemly duplicated Gq class G protein alpha subunit genes. Genomics. 1996;31: 359–66.

    PubMed  CAS  Google Scholar 

  • Dearworth Jr JR, Selvarajah BP, Kalman RA, Lanzone AJ, Goch AM, Boyd AB, Goldberg LA, Cooper LJ. A mammalian melanopsin in the retina of a fresh water turtle, the red-eared slider (Trachemys scripta elegans). Vision Res. 2011;51(2):288–95.

    PubMed  CAS  Google Scholar 

  • Devlin PF, Kay SA. Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. Plant Cell. 2000;12:2499–510.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Do MT, Yau KW. Intrinsically photosensitive retinal ganglion cells. Physiol Rev. 2010;90: 1547–81.

    PubMed  CAS  Google Scholar 

  • Do MT, Kang SH, Xue T, Zhong H, Liao HW, Bergles DE, Yau KW. Photon capture and signalling by melanopsin retinal ganglion cells. Nature. 2009;457:281–7.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dong C, Zhang J, Qiao J, He G. Positive selection and functional divergence after melanopsin gene duplication. Biochem Genet. 2012;50:235–48.

    PubMed  CAS  Google Scholar 

  • Drivenes O, Soviknes AM, Ebbesson LO, Fjose A, Seo HC, Helvik JV. Isolation and characterization of two teleost melanopsin genes and their differential expression within the inner retina and brain. J Comp Neurol. 2003;456:84–93.

    PubMed  CAS  Google Scholar 

  • Drouyer E, Dkhissi-Benyahya O, Chiquet C, WoldeMussie E, Ruiz G, Wheeler LA, Denis P, Cooper HM. Glaucoma alters the circadian timing system. PLoS One. 2008;3:e3931.

    PubMed  PubMed Central  Google Scholar 

  • Ebrey T, Koutalos Y. Vertebrate photoreceptors. Prog Retin Eye Res. 2001;20:49–94.

    PubMed  CAS  Google Scholar 

  • Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T, Renna JM, Prusky GT, Berson DM, Hattar S. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron. 2010;67:49–60.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Emery P, So WV, Kaneko M, Hall JC, Rosbash M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell. 1998;95:669–79.

    PubMed  CAS  Google Scholar 

  • Fahrenkrug J, Falktoft B, Georg B, Rask L. N-linked deglycosylated melanopsin retains its responsiveness to light. Biochemistry. 2009;48:5142–8.

    PubMed  CAS  Google Scholar 

  • Feigl B, Mattes D, Thomas R, Zele AJ. Intrinsically photosensitive (melanopsin) retinal ganglion cell function in glaucoma. Invest Ophthalmol Vis Sci. 2011;52:4362–7.

    PubMed  CAS  Google Scholar 

  • Ferreira PA, Pak WL. Bovine phospholipase C highly homologous to the norpA protein of Drosophila is expressed specifically in cones. J Biol Chem. 1994;269:3129–31.

    PubMed  CAS  Google Scholar 

  • Ferreira PA, Shortridge RD, Pak WL. Distinctive subtypes of bovine phospholipase C that have preferential expression in the retina and high homology to the norpA gene product of Drosophila. Proc Natl Acad Sci U S A. 1993;90:6042–6.

    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 

  • Foster R, Bellingham J. Opsins and melanopsins. Curr Biol. 2002;12:R543–4.

    PubMed  CAS  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, Hankins MW, Peirson SN. Light, photoreceptors, and circadian clocks. Methods Mol Biol. 2007;362:3–28.

    PubMed  CAS  Google Scholar 

  • Foster RG, Peirson SN, Wulff K, Winnebeck E, Vetter C, Roenneberg T. Sleep and circadian rhythm disruption in social jetlag and mental illness. Prog Mol Biol Transl Sci. 2013;119: 325–46.

    PubMed  Google Scholar 

  • Franke RR, Sakmar TP, Oprian DD, Khorana HG. A single amino acid substitution in rhodopsin (lysine 248 to leucine) prevents activation of transducin. J Biol Chem. 1988;263:2119–22.

    PubMed  CAS  Google Scholar 

  • Franke RR, Sakmar TP, Graham RM, Khorana HG. Structure and function in rhodopsin. Studies of the interaction between the rhodopsin cytoplasmic domain and transducin. J Biol Chem. 1992;267:14767–74.

    PubMed  CAS  Google Scholar 

  • Freedman MS, Lucas RJ, Soni B, von Schantz M, Munoz 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 

  • Garg SJ, Federman J. Optogenetics, visual prosthesis and electrostimulation for retinal dystrophies. Curr Opin Ophthalmol. 2013;24:407–14.

    PubMed  Google Scholar 

  • Glickman G, Byrne B, Pineda C, Hauck WW, Brainard GC. Light therapy for seasonal affective disorder with blue narrow-band light-emitting diodes (LEDs). Biol Psychiatry. 2006;59:502–7.

    PubMed  Google Scholar 

  • Gooley JJ, Lu J, Chou TC, Scammell TE, Saper CB. Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci. 2001;4:1165.

    PubMed  CAS  Google Scholar 

  • Graham DM, Wong KY, Shapiro P, Frederick C, Pattabiraman K, Berson DM. Melanopsin ganglion cells use a membrane-associated rhabdomeric phototransduction cascade. J Neurophysiol. 2008;99:2522–32.

    PubMed  CAS  Google Scholar 

  • Grone BP, Sheng Z, Chen CC, Fernald RD. Localization and diurnal expression of melanopsin, vertebrate ancient opsin, and pituitary adenylate cyclase-activating peptide mRNA in a teleost retina. J Biol Rhythms. 2007;22:558–61.

    PubMed  PubMed Central  Google Scholar 

  • Guler 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 

  • Hankins MW, Peirson SN, Foster RG. Melanopsin: an exciting photopigment. Trends Neurosci. 2008;31:27–36.

    PubMed  CAS  Google Scholar 

  • Hannibal J, Fahrenkrug J. Melanopsin: a novel photopigment involved in the photoentrainment of the brain’s biological clock? Ann Med. 2002;34:401–7.

    PubMed  CAS  Google Scholar 

  • Hannibal J, Hindersson P, Nevo E, Fahrenkrug J. The circadian photopigment melanopsin is expressed in the blind subterranean mole rat, Spalax. Neuroreport. 2002;13:1411–4.

    PubMed  CAS  Google Scholar 

  • Hardie RC. Phototransduction in Drosophila melanogaster. J Exp Biol. 2001;204:3403–9.

    PubMed  CAS  Google Scholar 

  • Hardie RC. Phototransduction: shedding light on translocation. Curr Biol. 2003;13:R775–7.

    PubMed  CAS  Google Scholar 

  • Hardie RC. TRP channels and lipids: from Drosophila to mammalian physiology. J Physiol. 2007;578:9–24.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hardie RC, Raghu P. Visual transduction in Drosophila. Nature. 2001;413:186–93.

    PubMed  CAS  Google Scholar 

  • Hargrave PA, McDowell JH, Curtis DR, Wang JK, Juszczak E, Fong SL, Rao JK, Argos P. The structure of bovine rhodopsin. Biophys Struct Mech. 1983;9:235–44.

    PubMed  CAS  Google Scholar 

  • Hartwick AT, Bramley JR, Yu J, Stevens KT, Allen CN, Baldridge WH, Sollars PJ, Pickard GE. Light-evoked calcium responses of isolated melanopsin-expressing retinal ganglion cells. J Neurosci. 2007;27:13468–80.

    PubMed  CAS  Google Scholar 

  • Hatori M, Panda S. The emerging roles of melanopsin in behavioral adaptation to light. Trends Mol Med. 2010;16:435–46.

    PubMed  CAS  PubMed Central  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 

  • Hebert M, Dumont M, Paquet J. Seasonal and diurnal patterns of human illumination under natural conditions. Chronobiol Int. 1998;15:59–70.

    PubMed  CAS  Google Scholar 

  • Hermann R, Poppe L, Pilbak S, Boden C, Maurer J, Weber S, Lerchl A. Predicted 3D-structure of melanopsin, the non-rod, non-cone photopigment of the mammalian circadian clock, from Djungarian hamsters (Phodopus sungorus). Neurosci Lett. 2005;376:76–80.

    PubMed  CAS  Google Scholar 

  • Hillman P, Hochstein S, Minke B. Transduction in invertebrate photoreceptors: role of pigment bistability. Physiol Rev. 1983;63:668–772.

    PubMed  CAS  Google Scholar 

  • Hinton DR, Sadun AA, Blanks JC, Miller CA. Optic-nerve degeneration in Alzheimer’s disease. N Engl J Med. 1986;315:485–7.

    PubMed  CAS  Google Scholar 

  • Hisatomi O, Tokunaga F. Molecular evolution of proteins involved in vertebrate phototransduction. Comp Biochem Physiol B Biochem Mol Biol. 2002;133:509–22.

    PubMed  Google Scholar 

  • Hubbard KB, Hepler JR. Cell signalling diversity of the Gqalpha family of heterotrimeric G proteins. Cell Signal. 2006;18:135–50.

    PubMed  CAS  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 

  • Hughes S, Watson TS, Foster RG, Peirson SN, Hankins MW. Nonuniform distribution and spectral tuning of photosensitive retinal ganglion cells of the mouse retina. Curr Biol. 2013;23:1696–701.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hunt DM, Carvalho LS, Cowing JA, Parry JW, Wilkie SE, Davies WL, Bowmaker JK. Spectral tuning of shortwave-sensitive visual pigments in vertebrates. Photochem Photobiol. 2007;83: 303–10.

    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, 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 

  • Jagannath A, Peirson SN, Foster RG. Sleep and circadian rhythm disruption in neuropsychiatric illness. Curr Opin Neurobiol. 2013;23:888–94.

    PubMed  CAS  Google Scholar 

  • Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, De Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau JP, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff JN, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature. 2004;431:946–57.

    PubMed  Google Scholar 

  • Jakobs TC, Libby RT, Ben Y, John SW, Masland RH. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J Cell Biol. 2005;171:313–25.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jenkins A, Munoz 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 

  • Jewett ME, Kronauer RE, Czeisler CA. Light-induced suppression of endogenous circadian amplitude in humans. Nature. 1991;350:59–62.

    PubMed  CAS  Google Scholar 

  • Jones KA, Hatori M, Mure LS, Bramley JR, Artymyshyn R, Hong SP, Marzabadi M, Zhong H, Sprouse J, Zhu Q, Hartwick AT, Sollars PJ, Pickard GE, Panda S. Small-molecule antagonists of melanopsin-mediated phototransduction. Nat Chem Biol. 2013;9:630–5.

    PubMed  CAS  Google Scholar 

  • Karnik SS, Khorana HG. Assembly of functional rhodopsin requires a disulfide bond between cysteine residues 110 and 187. J Biol Chem. 1990;265:17520–4.

    PubMed  CAS  Google Scholar 

  • Karnik SS, Sakmar TP, Chen HB, Khorana HG. Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin. Proc Natl Acad Sci U S A. 1988;85:8459–63.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Karnik SS, Ridge KD, Bhattacharya S, Khorana HG. Palmitoylation of bovine opsin and its cysteine mutants in COS cells. Proc Natl Acad Sci U S A. 1993;90:40–4.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kaushal S, Ridge KD, Khorana HG. Structure and function in rhodopsin: the role of asparagine-linked glycosylation. Proc Natl Acad Sci U S A. 1994;91:4024–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kawamura S, Tachibanaki S. Rod and cone photoreceptors: molecular basis of the difference in their physiology. Comp Biochem Physiol A Mol Integr Physiol. 2008;150:369–77.

    PubMed  Google Scholar 

  • Keeler CE. The Inheritance of a Retinal Abnormality in White Mice. Proc Natl Acad Sci U S A. 1924;10:329–33.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kessel L, Lundeman JH, Herbst K, Andersen TV, Larsen M. Age-related changes in the transmission properties of the human lens and their relevance to circadian entrainment. J Cataract Refract Surg. 2010;36:308–12.

    PubMed  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 

  • Konig B, Arendt A, McDowell JH, Kahlert M, Hargrave PA, Hofmann KP. Three cytoplasmic loops of rhodopsin interact with transducin. Proc Natl Acad Sci U S A. 1989;86:6878–82.

    PubMed  CAS  PubMed Central  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, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A. Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr Biol. 2005;15:1065–9.

    PubMed  CAS  Google Scholar 

  • La Morgia C, Ross-Cisneros FN, Hannibal J, Montagna P, Sadun AA, Carelli V. Melanopsin-expressing retinal ganglion cells: implications for human diseases. Vision Res. 2011;51:296–302.

    PubMed  Google Scholar 

  • Lall GS, Revell VL, Momiji H, Al Enezi J, Altimus CM, Guler AD, Aguilar C, Cameron MA, Allender S, Hankins MW, Lucas RJ. Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron. 2010;66:417–28.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lamb TD. Evolution of vertebrate retinal photoreception. Philos Trans R Soc Lond B Biol Sci. 2009;364:2911–24.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lamb TD. Evolution of phototransduction, vertebrate photoreceptors and retina. Prog Retin Eye Res. 2013;36:52–119.

    PubMed  CAS  Google Scholar 

  • Lamb TD, Collin SP, Pugh Jr EN. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci. 2007;8:960–76.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lamb TD, Arendt D, Collin SP. The evolution of phototransduction and eyes. Philos Trans R Soc Lond B Biol Sci. 2009;364:2791–3.

    PubMed  PubMed Central  Google Scholar 

  • Larhammar D, Nordstrom K, Larsson TA. Evolution of vertebrate rod and cone phototransduction genes. Philos Trans R Soc Lond B Biol Sci. 2009;364:2867–80.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lee RD, Thomas CF, Marietta RG, Stark WS. Vitamin A, visual pigments, and visual receptors in Drosophila. Microsc Res Tech. 1996;35:418–30.

    PubMed  CAS  Google Scholar 

  • Lerea CL, Somers DE, Hurley JB, Klock IB, Bunt-Milam AH. Identification of specific transducin alpha subunits in retinal rod and cone photoreceptors. Science. 1986;234:77–80.

    PubMed  CAS  Google Scholar 

  • Lewy AJ. Circadian misalignment in mood disturbances. Curr Psychiatry Rep. 2009;11:459–65.

    PubMed  Google Scholar 

  • Lewy AJ, Sack RL, Miller LS, Hoban TM. Antidepressant and circadian phase-shifting effects of light. Science. 1987;235:352–4.

    PubMed  CAS  Google Scholar 

  • Lewy AJ, Emens JS, Songer JB, Sims N, Laurie AL, Fiala SC, Buti AL. Winter depression: integrating mood, circadian rhythms, and the sleep/wake and light/dark cycles into a bio-psycho-social-environmental model. Sleep Med Clin. 2009;4:285–99.

    PubMed  PubMed Central  Google Scholar 

  • Li RS, Chen BY, Tay DK, Chan HH, Pu ML, So KF. Melanopsin-expressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model. Invest Ophthalmol Vis Sci. 2006;47:2951–8.

    PubMed  Google Scholar 

  • Li SY, Yau SY, Chen BY, Tay DK, Lee VW, Pu ML, Chan HH, So KF. Enhanced survival of melanopsin-expressing retinal ganglion cells after injury is associated with the PI3 K/Akt pathway. Cell Mol Neurobiol. 2008;28:1095–107.

    PubMed  CAS  Google Scholar 

  • Lin B, Koizumi A, Tanaka N, Panda S, Masland RH. Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc Natl Acad Sci U S A. 2008;105:16009–14.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lipinski DM, Thake M, MacLaren RE. Clinical applications of retinal gene therapy. Prog Retin Eye Res. 2013;32:22–47.

    PubMed  CAS  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 

  • Lucas RJ, Lall GS, Allen AE, Brown TM. How rod, cone, and melanopsin photoreceptors come together to enlighten the mammalian circadian clock. Prog Brain Res. 2012;199:1–18.

    PubMed  CAS  Google Scholar 

  • Mainster MA, Turner PL. Blue-blocking IOLs decrease photoreception without providing significant photoprotection. Surv Ophthalmol. 2010;55:272–89.

    PubMed  Google Scholar 

  • Makino CL, Wen XH, Lem J. Piecing together the timetable for visual transduction with transgenic animals. Curr Opin Neurobiol. 2003;13:404–12.

    PubMed  CAS  Google Scholar 

  • Markwell EL, Feigl B, Zele AJ. Intrinsically photosensitive melanopsin retinal ganglion cell contributions to the pupillary light reflex and circadian rhythm. Clin Exp Optom. 2010;93: 137–49.

    PubMed  Google Scholar 

  • Matos-Cruz V, Blasic J, Nickle B, Robinson PR, Hattar S, Halpern ME. Unexpected diversity and photoperiod dependence of the zebrafish melanopsin system. PLoS One. 2011;6:e25111.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Matsuyama T, Yamashita T, Imamoto Y, Shichida Y. Photochemical properties of mammalian melanopsin. Biochemistry. 2012;51:5454–62.

    PubMed  CAS  Google Scholar 

  • Mellor H, Parker PJ. The extended protein kinase C superfamily. Biochem J. 1998;332(Pt 2):281–92.

    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 

  • Meyer A, Van de Peer Y. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays. 2005;27:937–45.

    PubMed  CAS  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 

  • Mizuno N, Itoh H. Functions and regulatory mechanisms of Gq-signaling pathways. Neurosignals. 2009;17:42–54.

    PubMed  CAS  Google Scholar 

  • Mohawk JA, Green CB, Takahashi JS. Central and peripheral circadian clocks in mammals. Annu Rev Neurosci. 2012;35:445–62.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Montell C. Drosophila visual transduction. Trends Neurosci. 2012;35:356–63.

    PubMed  CAS  PubMed Central  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? Brain Res Mol Brain Res. 2003;112:135–45.

    PubMed  CAS  Google Scholar 

  • Mure LS, Rieux C, Hattar S, Cooper HM. Melanopsin-dependent nonvisual responses: evidence for photopigment bistability in vivo. J Biol Rhythms. 2007;22:411–24.

    PubMed  PubMed Central  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 

  • Nasi E, del Pilar Gomez M. Melanopsin-mediated light-sensing in amphioxus: a glimpse of the microvillar photoreceptor lineage within the deuterostomia. Commun Integr Biol. 2009;2:441–3.

    PubMed  CAS  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nathans J. Determinants of visual pigment absorbance: role of charged amino acids in the putative transmembrane segments. Biochemistry. 1990b;29:937–42.

    PubMed  CAS  Google Scholar 

  • Nathans J, Hogness DS. Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin. Cell. 1983;34:807–14.

    PubMed  CAS  Google Scholar 

  • Newman LA, Walker MT, Brown RL, Cronin TW, Robinson PR. Melanopsin forms a functional short-wavelength photopigment. Biochemistry. 2003;42:12734–8.

    PubMed  CAS  Google Scholar 

  • Nilsson DE. Eye evolution and its functional basis. Vis Neurosci. 2013;30:5–20.

    PubMed  PubMed Central  Google Scholar 

  • Noseda R, Kainz V, Jakubowski M, Gooley JJ, Saper CB, Digre K, Burstein R. A neural mechanism for exacerbation of headache by light. Nat Neurosci. 2010;13:239–45.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Okano T, Fukada Y. Phototransduction cascade and circadian oscillator in chicken pineal gland. J Pineal Res. 1997;22:145–51.

    PubMed  CAS  Google Scholar 

  • Okano T, Kojima D, Fukada Y, Shichida Y, Yoshizawa T. Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. Proc Natl Acad Sci U S A. 1992;89:5932–6.

    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 

  • Ovchinnikov Yu A. Rhodopsin and bacteriorhodopsin: structure-function relationships. FEBS Lett. 1982;148:179–91.

    PubMed  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 

  • Peirson S, Foster RG. Melanopsin: another way of signaling light. Neuron. 2006;49:331–9.

    PubMed  CAS  Google Scholar 

  • Peirson SN, Thompson S, Hankins MW, Foster RG. Mammalian photoentrainment: results, methods, and approaches. Methods Enzymol. 2005;393:697–726.

    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 

  • Peirson SN, Halford S, Foster RG. The evolution of irradiance detection: melanopsin and the non-visual opsins. Philos Trans R Soc Lond B Biol Sci. 2009;364:2849–65.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pepe IM. Rhodopsin and phototransduction. J Photochem Photobiol B. 1999;48:1–10.

    PubMed  CAS  Google Scholar 

  • Perez-Leighton CE, Schmidt TM, Abramowitz J, Birnbaumer L, Kofuji P. Intrinsic phototransduction persists in melanopsin-expressing ganglion cells lacking diacylglycerol-sensitive TRPC subunits. Eur J Neurosci. 2011;33:856–67.

    PubMed  PubMed Central  Google Scholar 

  • Philp AR, Bellingham J, Garcia-Fernandez J, 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 

  • Pickard GE, Sollars PJ. Intrinsically photosensitive retinal ganglion cells. Rev Physiol Biochem Pharmacol. 2012;162:59–90.

    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 

  • Pritchett D, Wulff K, Oliver PL, Bannerman DM, Davies KE, Harrison PJ, Peirson SN, Foster RG. Evaluating the links between schizophrenia and sleep and circadian rhythm disruption. J Neural Transm. 2012;119:1061–75.

    PubMed  Google Scholar 

  • Provencio I. The hidden organ in your eyes. Sci Am. 2011;304:54–9.

    PubMed  Google Scholar 

  • Provencio I, Foster RG. Circadian rhythms in mice can be regulated by photoreceptors with cone-like characteristics. Brain Res. 1995;694:183–90.

    PubMed  CAS  Google Scholar 

  • Provencio I, Warthen DM. Melanopsin, the photopigment of intrinsically photosensitive retinal ganglion cells. WIREs Membr Transp Signal. 2012;1:228–37.

    CAS  Google Scholar 

  • Provencio I, Wong S, Lederman AB, Argamaso SM, Foster RG. Visual and circadian responses to light in aged retinally degenerate mice. Vision Res. 1994;34:1799–806.

    PubMed  CAS  Google Scholar 

  • Provencio I, Cooper HM, Foster RG. Retinal projections in mice with inherited retinal degeneration: implications for circadian photoentrainment. J Comp Neurol. 1998a;395:417–39.

    PubMed  CAS  Google Scholar 

  • Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD. Melanopsin: An opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A. 1998b;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 

  • Provencio I, Rollag MD, Castrucci AM. Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature. 2002;415:493.

    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 

  • Raghu P. Regulation of Drosophila TRPC channels by protein and lipid interactions. Semin Cell Dev Biol. 2006;17:646–53.

    PubMed  CAS  Google Scholar 

  • Roecklein KA, Rohan KJ, Duncan WC, Rollag MD, Rosenthal NE, Lipsky RH, Provencio I. A missense variant (P10L) of the melanopsin (OPN4) gene in seasonal affective disorder. J Affect Disord. 2009;114:279–85.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Roecklein KA, Wong PM, Miller MA, Donofry SD, Kamarck ML, Brainard GC. Melanopsin, photosensitive ganglion cells, and seasonal affective disorder. Neurosci Biobehav Rev. 2013;37:229–39.

    PubMed  CAS  PubMed Central  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 

  • Rollag MD, Berson DM, Provencio I. Melanopsin, ganglion-cell photoreceptors, and mammalian photoentrainment. J Biol Rhythms. 2003;18:227–34.

    PubMed  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 

  • Ruprecht JJ, Mielke T, Vogel R, Villa C, Schertler GF. Electron crystallography reveals the structure of metarhodopsin I. EMBO J. 2004;23:3609–20.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.

    PubMed  CAS  Google Scholar 

  • Sakmar TP, Franke RR, Khorana HG. Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc Natl Acad Sci U S A. 1989;86:8309–13.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sakmar TP, Franke RR, Khorana HG. The role of the retinylidene Schiff base counterion in rhodopsin in determining wavelength absorbance and Schiff base pKa. Proc Natl Acad Sci U S A. 1991;88:3079–83.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sakmar TP, Menon ST, Marin EP, Awad ES. Rhodopsin: insights from recent structural studies. Annu Rev Biophys Biomol Struct. 2002;31:443–84.

    PubMed  CAS  Google Scholar 

  • Sandbakken M, Ebbesson L, Stefansson S, Helvik JV. Isolation and characterization of melanopsin photoreceptors of Atlantic salmon (Salmo salar). J Comp Neurol. 2012;520:3727–44.

    PubMed  CAS  Google Scholar 

  • Sansom IJ, Smith MP, Smith MM. Scales of thelodont and shark-like fishes from the Ordovician. Nature. 1996;379:628–30.

    CAS  Google Scholar 

  • Schaefer M. Homo- and heteromeric assembly of TRP channel subunits. Pflugers Arch. 2005;451:35–42.

    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 

  • Schmidt TM, Kofuji P. Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci. 2009;29:476–82.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Schmidt TM, Kofuji P. Structure and function of bistratified intrinsically photosensitive retinal ganglion cells in the mouse. J Comp Neurol. 2011;519:1492–504.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Schmidt TM, Chen SK, Hattar S. Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions. Trends Neurosci. 2011a;34:572–80.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Schmidt TM, Do MT, Dacey D, Lucas R, Hattar S, Matynia A. Melanopsin-positive intrinsically photosensitive retinal ganglion cells: from form to function. J Neurosci. 2011b;31:16094–101.

    PubMed  CAS  PubMed Central  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, Lall GS, Ralphs KL, Wolstenholme AJ, Lucas RJ, Foster RG, Hankins MW. 2-Aminoethoxydiphenylborane is an acute inhibitor of directly photosensitive retinal ganglion cell activity in vitro and in vivo. J Neurosci. 2007;27:3981–6.

    PubMed  CAS  Google Scholar 

  • Sekharan S, Wei JN, Batista VS. The active site of melanopsin: the biological clock photoreceptor. J Am Chem Soc. 2012;134:19536–9.

    PubMed  CAS  Google Scholar 

  • Semo M, Peirson S, Lupi D, Lucas RJ, Jeffery G, Foster RG. Melanopsin retinal ganglion cells and the maintenance of circadian and pupillary responses to light in aged rodless/coneless (rd/rd cl) mice. Eur J Neurosci. 2003;17:1793–801.

    PubMed  Google Scholar 

  • Semo M, Munoz Llamosas M, Foster RG, Jeffery G. Melanopsin (Opn4) positive cells in the cat retina are randomly distributed across the ganglion cell layer. Vis Neurosci. 2005;22:111–6.

    PubMed  Google Scholar 

  • Sexton TJ, Golczak M, Palczewski K, Van Gelder RN. Melanopsin is highly resistant to light and chemical bleaching in vivo. J Biol Chem. 2012;287:20888–97.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Shen D, Jiang M, Hao W, Tao L, Salazar M, Fong HK. A human opsin-related gene that encodes a retinaldehyde-binding protein. Biochemistry. 1994;33:13117–25.

    PubMed  CAS  Google Scholar 

  • Shichida Y, Matsuyama T. Evolution of opsins and phototransduction. Philos Trans R Soc Lond B Biol Sci. 2009;364:2881–95.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Somers DE, Devlin PF, Kay SA. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science. 1998;282:1488–90.

    PubMed  CAS  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 

  • Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, Rosbash M, Hall JC. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell. 1998;95:681–92.

    PubMed  CAS  Google Scholar 

  • Strader CD, Sigal IS, Dixon RA. Genetic approaches to the determination of structure-function relationships of G protein-coupled receptors. Trends Pharmacol Sci. 1989;Suppl:26–30.

    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 

  • Suh BC, Hille B. PIP2 is a necessary cofactor for ion channel function: how and why? Annu Rev Biophys. 2008;37:175–95.

    PubMed  CAS  PubMed Central  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 

  • Swalla BJ, Smith AB. Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos Trans R Soc Lond B Biol Sci. 2008;363:1557–68.

    PubMed  PubMed Central  Google Scholar 

  • Swalla BJ, Xavier-Neto J. Chordate origins and evolution. Genesis. 2008;46:575–9.

    PubMed  Google Scholar 

  • Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10:512–26.

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007;24:1596–9.

    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 

  • Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y. Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res. 2003;13:382–90.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Terakita A. The opsins. Genome Biol. 2005;6:213.

    PubMed  PubMed Central  Google Scholar 

  • Terakita A, Yamashita T, Nimbari N, Kojima D, Shichida Y. Functional interaction between bovine rhodopsin and G protein transducin. J Biol Chem. 2002;277:40–6.

    PubMed  CAS  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, Tsukamoto H, Koyanagi M, Sugahara M, Yamashita T, Shichida Y. Expression and comparative characterization of Gq-coupled invertebrate visual pigments and melanopsin. J Neurochem. 2008;105:883–90.

    PubMed  CAS  Google Scholar 

  • Thorne HC, Jones KH, Peters SP, Archer SN, Dijk DJ. Daily and seasonal variation in the spectral composition of light exposure in humans. Chronobiol Int. 2009;26:854–66.

    PubMed  Google Scholar 

  • Todo T. Functional diversity of the DNA photolyase/blue light receptor family. Mutat Res. 1999;434:89–97.

    PubMed  CAS  Google Scholar 

  • Tomioka K, Matsumoto A. A comparative view of insect circadian clock systems. Cell Mol Life Sci. 2010;67:1397–406.

    PubMed  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 

  • Tomonari S, Takagi A, Noji S, Ohuchi H. Expression pattern of the melanopsin-like (cOpn4m) and VA opsin-like genes in the developing chicken retina and neural tissues. Gene Expr Patterns. 2007;7:746–53.

    PubMed  CAS  Google Scholar 

  • Torii M, Kojima D, Okano T, Nakamura A, Terakita A, Shichida Y, Wada A, Fukada Y. Two isoforms of chicken melanopsins show blue light sensitivity. FEBS Lett. 2007;581:5327–31.

    PubMed  CAS  Google Scholar 

  • Tsukamoto H, Terakita A. Diversity and functional properties of bistable pigments. Photochem Photobiol Sci. 2010;9:1435–43.

    PubMed  CAS  Google Scholar 

  • Tsukamoto H, Terakita A, Shichida Y. A rhodopsin exhibiting binding ability to agonist all-trans-retinal. Proc Natl Acad Sci U S A. 2005;102:6303–8.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Turner PL, Van Someren EJ, Mainster MA. The role of environmental light in sleep and health: effects of ocular aging and cataract surgery. Sleep Med Rev. 2010;14:269–80.

    PubMed  Google Scholar 

  • Vandewalle G, Schmidt C, Albouy G, Sterpenich V, Darsaud A, Rauchs G, Berken PY, Balteau E, Degueldre C, Luxen A, Maquet P, Dijk DJ. Brain responses to violet, blue, and green monochromatic light exposures in humans: prominent role of blue light and the brainstem. PLoS One. 2007;2:e1247.

    PubMed  PubMed Central  Google Scholar 

  • Walker MT, Brown RL, Cronin TW, Robinson PR. Photochemistry of retinal chromophore in mouse melanopsin. Proc Natl Acad Sci U S A. 2008;105:8861–5.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Walls GL. The vertebrate eye and its adaptive radiation. Bloomfield Hills: Cranbrook Institute of Science; 1942.

    Google Scholar 

  • Wang HZ, Lu QJ, Wang NL, Liu H, Zhang L, Zhan GL. Loss of melanopsin-containing retinal ganglion cells in a rat glaucoma model. Chin Med J (Engl). 2008;121:1015–9.

    Google Scholar 

  • Warren EJ, Allen CN, Brown RL, Robinson DW. The light-activated signaling pathway in SCN-projecting rat retinal ganglion cells. Eur J Neurosci. 2006;23:2477–87.

    PubMed  PubMed Central  Google Scholar 

  • Weng S, Wong KY, Berson DM. Circadian modulation of melanopsin-driven light response in rat ganglion-cell photoreceptors. J Biol Rhythms. 2009;24:391–402.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wilkie TM, Gilbert DJ, Olsen AS, Chen XN, Amatruda TT, Korenberg JR, Trask BJ, de Jong P, Reed RR, Simon MI, et al. Evolution of the mammalian G protein alpha subunit multigene family. Nat Genet. 1992;1:85–91.

    PubMed  CAS  Google Scholar 

  • Willis GL. Parkinson’s disease as a neuroendocrine disorder of circadian function: dopamine-melatonin imbalance and the visual system in the genesis and progression of the degenerative process. Rev Neurosci. 2008;19:245–316.

    PubMed  CAS  Google Scholar 

  • Willis GL, Kelly AM, Kennedy GA. Compromised circadian function in Parkinson’s disease: enucleation augments disease severity in the unilateral model. Behav Brain Res. 2008;193: 37–47.

    PubMed  CAS  Google Scholar 

  • Wu YH, Swaab DF. Disturbance and strategies for reactivation of the circadian rhythm system in aging and Alzheimer’s disease. Sleep Med. 2007;8:623–36.

    PubMed  Google Scholar 

  • Wulff K, Porcheret K, Cussans E, Foster RG. Sleep and circadian rhythm disturbances: multiple genes and multiple phenotypes. Curr Opin Genet Dev. 2009;19:237–46.

    PubMed  CAS  Google Scholar 

  • Wulff K, Gatti S, Wettstein JG, Foster RG. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat Rev Neurosci. 2010;11:589–99.

    PubMed  CAS  Google Scholar 

  • Wulff K, Dijk DJ, Middleton B, Foster RG, Joyce EM. Sleep and circadian rhythm disruption in schizophrenia. Br J Psychiatry. 2012;200:308–16.

    PubMed  PubMed Central  Google Scholar 

  • Xue T, Do MT, Riccio A, Jiang Z, Hsieh J, Wang HC, Merbs SL, Welsbie DS, Yoshioka T, Weissgerber P, Stolz S, Flockerzi V, Freichel M, Simon MI, Clapham DE, Yau KW. Melanopsin signalling in mammalian iris and retina. Nature. 2011;479:67–73.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yamashita T, Terakita A, Shichida Y. Distinct roles of the second and third cytoplasmic loops of bovine rhodopsin in G protein activation. J Biol Chem. 2000;275:34272–9.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res. 2000;19: 385–419.

    PubMed  CAS  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 

  • Yokoyama S, Tada T, Yamato T. Modulation of the absorption maximum of rhodopsin by amino acids in the C-terminus. Photochem Photobiol. 2007;83:236–41.

    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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Acknowledgements

We thank those who have collectively produced much of the data discussed in this review. Particularly noteworthy are Professor David Whitmore, Doctor Katherine Tamai, Professor Venkatesh, Professor David Hunt and Professor Shaun Collin, amongst many others. This work was supported by grants awarded by the Australian Research Council (ARC) to WILD in the form of a Future Fellowship, and the UK Biotechnology and Biological Sciences Research Council (BBSRC) and the Wellcome Trust to MWH and RGR.

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

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Davies, W.I.L., Foster, R.G., Hankins, M.W. (2014). The Evolution and Function of Melanopsin in Craniates. 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_2

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