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Abstract

Circadian rhythms are self-sustained, approximately 24-h rhythms of physiology and behavior. These rhythms are entrained to an exactly 24-h period by the daily light-dark cycle. Remarkably, mice lacking all rod and cone photoreceptors still demonstrate photic entrainment, an effect mediated by intrinsically photosensitive retinal ganglion cells (ipRGCs). These cells utilize melanopsin (OPN4) as their photopigment. Distinct from the ciliary rod and cone opsins, melanopsin appears to function as a stable photopigment utilizing sequential photon absorption for its photocycle; this photocycle, in turn, confers properties on ipRGCs such as sustained signaling and resistance from photic bleaching critical for an irradiance detection system. The retina itself also functions as a circadian pacemaker that can be autonomously entrained to light-dark cycles. Recent experiments have demonstrated that another novel opsin, neuropsin (OPN5), is required for this entrainment, which appears to be mediated by a separate population of ipRGCs. Surprisingly, the circadian clock of the mammalian cornea is also light entrainable and is also neuropsin-dependent for this effect. The retina thus utilizes a surprisingly broad array of opsins for mediation of different light-detection tasks.

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2016-10-14
2024-06-20
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Literature Cited

  1. Barnard AR, Hattar S, Hankins MW, Lucas RJ. 2006. Melanopsin regulates visual processing in the mouse retina. Curr. Biol. 16:389–95 [Google Scholar]
  2. Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–73 [Google Scholar]
  3. Besharse JC, Iuvone PM. 1983. Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature 305:133–35 [Google Scholar]
  4. Blackshaw S, Snyder SH. 1999. Encephalopsin: a novel mammalian extraretinal opsin discretely localized in the brain. J. Neurosci. 19:3681–90 [Google Scholar]
  5. Blasic JR Jr., Brown RL, Robinson PR. 2012. Light-dependent phosphorylation of the carboxy tail of mouse melanopsin. Cell. Mol. Life Sci. 69:1551–62 [Google Scholar]
  6. Blasic JR Jr., Matos-Cruz V, Ujla D, Cameron EG, Hattar S. et al. 2014. Identification of critical phosphorylation sites on the carboxy tail of melanopsin. Biochemistry 53:2644–49 [Google Scholar]
  7. Brzezinski JA IV, Brown NL, Tanikawa A, Bush RA, Sieving PA. et al. 2005. Loss of circadian photoentrainment and abnormal retinal electrophysiology in Math5 mutant mice. Investig. Ophthalmol. Vis. Sci. 46:2540–51 [Google Scholar]
  8. Buhr ED, Takahashi JS. 2013. Molecular components of the mammalian circadian clock. Handb. Exp. Pharmacol. 217:3–27 [Google Scholar]
  9. Buhr ED, Van Gelder RN. 2014. Local photic entrainment of the retinal circadian oscillator in the absence of rods, cones, and melanopsin. PNAS 111:8625–30 [Google Scholar]
  10. Buhr ED, Yue WWS, Ren X, Jiang Z, Liao H-WR. et al. 2015. Neuropsin (OPN5)-mediated photoentrainment of local circadian oscillators in mammalian retina and cornea. PNAS 112:13093–98 [Google Scholar]
  11. Cavallari N, Frigato E, Vallone D, Fröhlich N, Lopez-Olmeda JF. et al. 2011. A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception. PLOS Biol. 9:e1001142 [Google Scholar]
  12. Chen S-K, Badea TC, Hattar S. 2011. Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature 476:92–95 [Google Scholar]
  13. Chew KS, Schmidt TM, Rupp AC, Kofuji P, Trimarchi JM. 2014. Loss of Gq/11 genes does not abolish melanopsin phototransduction. PLOS ONE 9:e98356 [Google Scholar]
  14. Dinet V, Ansari N, Torres-Farfan C, Korf H-W. 2007. Clock gene expression in the retina of melatonin-proficient (C3H) and melatonin-deficient (C57BL) mice. J. Pineal Res. 42:83–91 [Google Scholar]
  15. Dinet V, Korf H-W. 2007. Impact of melatonin receptors on pCREB and clock-gene protein levels in the murine retina. Cell Tissue Res. 330:29–34 [Google Scholar]
  16. Dkhissi-Benyahya O, Coutanson C, Knoblauch K, Lahouaoui H, Leviel V. et al. 2013. The absence of melanopsin alters retinal clock function and dopamine regulation by light. Cell. Mol. Life Sci. 70:3435–47 [Google Scholar]
  17. Do MTH, Kang SH, Xue T, Zhong H, Liao H-W. et al. 2009. Photon capture and signalling by melanopsin retinal ganglion cells. Nature 457:281–87 [Google Scholar]
  18. Doyle SE, Castrucci AM, McCall M, Provencio I, Menaker M. 2006. Nonvisual light responses in the Rpe65 knockout mouse: Rod loss restores sensitivity to the melanopsin system. PNAS 103:10432–37 [Google Scholar]
  19. Doyle SE, Grace MS, McIvor W, Menaker M. 2002a. Circadian rhythms of dopamine in mouse retina: the role of melatonin. Vis. Neurosci. 19:593–601 [Google Scholar]
  20. Doyle SE, McIvor WE, Menaker M. 2002b. Circadian rhythmicity in dopamine content of mammalian retina: role of the photoreceptors. J. Neurochem. 83:211–19 [Google Scholar]
  21. Ebihara S, Tsuji K. 1980. Entrainment of the circadian activity rhythm to the light cycle: effective light intensity for a Zeitgeber in the retinal degenerate C3H mouse and the normal C57BL mouse. Physiol. Behav. 24:523–27 [Google Scholar]
  22. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK. et al. 2010. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67:49–60 [Google Scholar]
  23. Emanuel AJ, Do MTH. 2015. Melanopsin tristability for sustained and broadband phototransduction. Neuron 85:1043–55 [Google Scholar]
  24. Emery P, Stanewsky R, Helfrich-Förster C, Emery-Le M, Hall JC, Rosbash M. 2000. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26:493–504 [Google Scholar]
  25. Faradji-Prevautel H, Cespuglio R, Jouvet M. 1990. Circadian rest-activity rhythms in the anophthalmic, monocular and binocular ZRDCT/An mice. Retinal and serotoninergic (raphe) influences. Brain Res. 526:207–16 [Google Scholar]
  26. Fischer RM, Fontinha BM, Kirchmaier S, Steger J, Bloch S. et al. 2013. Co-expression of VAL- and TMT-opsins uncovers ancient photosensory interneurons and motorneurons in the vertebrate brain. PLOS Biol. 11:e1001585 [Google Scholar]
  27. Fogle KJ, Parson KG, Dahm NA, Holmes TC. 2011. CRYPTOCHROME is a blue-light sensor that regulates neuronal firing rate. Science 331:1409–13 [Google Scholar]
  28. Freedman MS, Lucas RJ, Soni B, von Schantz M, Muñoz M. et al. 1999. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science 284:502–4 [Google Scholar]
  29. Fu Y, Zhong H, Wang M-HH, Luo D-G, Liao H-W. et al. 2005. Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. PNAS 102:10339–44 [Google Scholar]
  30. Gaub BM, Berry MH, Holt AE, Isacoff EY, Flannery JG. 2015. Optogenetic vision restoration using rhodopsin for enhanced sensitivity. Mol. Ther. 23:1562–71 [Google Scholar]
  31. Goldman AI, Teirstein PS, O'Brien PJ. 1980. The role of ambient lighting in circadian disc shedding in the rod outer segment of the rat retina. Investig. Ophthalmol. Vis. Sci. 19:1257–67 [Google Scholar]
  32. Göz D, Studholme K, Lappi DA, Rollag MD, Provencio I, Morin LP. 2008. Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PLOS ONE 3:e3153 [Google Scholar]
  33. Güler AD, Ecker JL, Lall GS, Haq S, Altimus CM. et al. 2008. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453:102–5 [Google Scholar]
  34. Haltaufderhyde K, Ozdeslik RN, Wicks NL, Najera JA, Oancea E. 2015. Opsin expression in human epidermal skin. Photochem. Photobiol. 91:117–23 [Google Scholar]
  35. Hatori M, Le H, Vollmers C, Keding SR, Tanaka N. et al. 2008. Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLOS ONE 3:e2451 [Google Scholar]
  36. Hattar S, Kumar M, Park A, Tong P, Tung J. et al. 2006. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J. Comp. Neurol. 497:326–49 [Google Scholar]
  37. Hattar S, Liao H, Takao M, Berson D, Yau K. 2002. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065–70 [Google Scholar]
  38. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH. et al. 2003. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424:76–81 [Google Scholar]
  39. Helfrich-Förster C, Winter C, Hofbauer A, Hall JC, Stanewsky R. 2001. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30:249–61 [Google Scholar]
  40. Herzog ED, Huckfeldt RM. 2003. Circadian entrainment to temperature, but not light, in the isolated suprachiasmatic nucleus. J. Neurophysiol. 90:763–70 [Google Scholar]
  41. Hiragaki S, Baba K, Coulson E, Kunst S, Spessert R, Tosini G. 2014. Melatonin signaling modulates clock genes expression in the mouse retina. PLOS ONE 9:e106819 [Google Scholar]
  42. Ibuka N. 1987. Circadian rhythms in sleep-wakefulness and wheel-running activity in a congenitally anophthalmic rat mutant. Physiol. Behav. 39:321–26 [Google Scholar]
  43. Jackson CR, Ruan G-X, Aseem F, Abey J, Gamble K. et al. 2012. Retinal dopamine mediates multiple dimensions of light-adapted vision. J. Neurosci. 32:9359–68 [Google Scholar]
  44. Jin NG, Chuang AZ, Masson PJ, Ribelayga CP. 2015. Rod electrical coupling is controlled by a circadian clock and dopamine in mouse retina. J. Physiol. 593:1597–631 [Google Scholar]
  45. Johnson J, Wu V, Donovan M, Majumdar S, Rentería RC. et al. 2010. Melanopsin-dependent light avoidance in neonatal mice. PNAS 107:17374–78 [Google Scholar]
  46. Keeler CE. 1927. Iris movements in blind mice. Am. J. Physiol. 81:107–12 [Google Scholar]
  47. Kikkawa Y. 1973. Diurnal variation in corneal thickness. Exp. Eye Res. 15:1–9 [Google Scholar]
  48. Kiser PD, Golczak M, Palczewski K. 2014. Chemistry of the retinoid (visual) cycle. Chem. Rev. 114:194–232 [Google Scholar]
  49. Koh K, Zheng X, Sehgal A. 2006. JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science 312:1809–12 [Google Scholar]
  50. Kojima D, Mori S, Torii M, Wada A, Morishita R, Fukada Y. 2011. UV-sensitive photoreceptor protein OPN5 in humans and mice. PLOS ONE 6:e26388 [Google Scholar]
  51. Konopka RJ, Benzer S. 1971. Clock mutants of Drosophila melanogaster. PNAS 68:2112–16 [Google Scholar]
  52. Koyanagi M, Terakita A. 2008. Gq-coupled rhodopsin subfamily composed of invertebrate visual pigment and melanopsin. Photochem. Photobiol. 84:1024–30 [Google Scholar]
  53. Krieger DT. 1973. Effect of ocular enucleation and altered lighting regimens at various ages on the circadian periodicity of plasma corticosteroid levels in the rat. Endocrinology 93:1077–91 [Google Scholar]
  54. Kumbalasiri T, Provencio I. 2005. Melanopsin and other novel mammalian opsins. Exp. Eye Res. 81:368–75 [Google Scholar]
  55. Kumbalasiri T, Rollag MD, Isoldi MC, Castrucci AMDL, Provencio I. 2007. Melanopsin triggers the release of internal calcium stores in response to light. Photochem. Photobiol. 83:273–79 [Google Scholar]
  56. Levin SR. 1966. The persistance of a circadian rhythm in the cell division rate of corneal epithelium in rats maintained under constant illumination. Chic. Med. Sch. Q. 26:123–24 [Google Scholar]
  57. Liu JH. 1998. Circadian rhythm of intraocular pressure. J. Glaucoma 7:141–47 [Google Scholar]
  58. Liu X, Zhang Z, Ribelayga CP. 2012. Heterogeneous expression of the core circadian clock proteins among neuronal cell types in mouse retina. PLOS ONE 7:e50602 [Google Scholar]
  59. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau K-W. 2003. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299:245–47 [Google Scholar]
  60. Mandell RB, Fatt I. 1965. Thinning of the human cornea on awakening. Nature 208:292–93 [Google Scholar]
  61. Matsuyama T, Yamashita T, Imamoto Y, Shichida Y. 2012. Photochemical properties of mammalian melanopsin. Biochemistry 51:5454–62 [Google Scholar]
  62. McMahon DG, Iuvone PM, Tosini G. 2014. Circadian organization of the mammalian retina: from gene regulation to physiology and diseases. Prog. Retin. Eye Res. 39:58–76 [Google Scholar]
  63. Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW. 2005. Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433:741–45 [Google Scholar]
  64. Moore RY, Lenn NJ. 1972. A retinohypothalamic projection in the rat. J. Comp. Neurol. 146:1–14 [Google Scholar]
  65. Mrosovsky N, Hattar S. 2003. Impaired masking responses to light in melanopsin-knockout mice. Chronobiol. Int. 20:989–99 [Google Scholar]
  66. Mrosovsky N, Hattar S. 2005. Diurnal mice (Mus musculus) and other examples of temporal niche switching. J. Comp. Physiol. A 191:1011–24 [Google Scholar]
  67. Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S. et al. 2010. A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. PNAS 107:15264–68 [Google Scholar]
  68. Nakane Y, Shimmura T, Abe H, Yoshimura T. 2014. Intrinsic photosensitivity of a deep brain photoreceptor. Curr. Biol. 24:R596–97 [Google Scholar]
  69. Nieto PS, Valdez DJ, Acosta-Rodríguez VA, Guido ME. 2011. 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 6:e26417 [Google Scholar]
  70. Nissilä J, Mänttäri S, Särkioja T, Tuominen H, Takala T. et al. 2012. Encephalopsin (OPN3) protein abundance in the adult mouse brain. J. Comp. Physiol. A 198:833–39 [Google Scholar]
  71. Organisciak DT, Darrow RM, Barsalou L, Kutty RK, Wiggert B. 2000. Circadian-dependent retinal light damage in rats. Investig. Ophthalmol. Vis. Sci. 41:3694–701 [Google Scholar]
  72. Owens L, Buhr E, Tu DC, Lamprecht TL, Lee J, Van Gelder RN. 2012. Effect of circadian clock gene mutations on nonvisual photoreception in the mouse. Investig. Ophthalmol. Vis. Sci. 53:454–60 [Google Scholar]
  73. Öztürk N, Song S-H, Özgür S, Selby CP, Morrison L. et al. 2007. Structure and function of animal cryptochromes. Cold Spring Harb. Symp. Quant. Biol. 72:119–31 [Google Scholar]
  74. Ozturk N, VanVickle-Chavez SJ, Akileswaran L, Van Gelder RN, Sancar A. 2013. Ramshackle (Brwd3) promotes light-induced ubiquitylation of Drosophila Cryptochrome by DDB1-CUL4-ROC1 E3 ligase complex. PNAS 110:4980–85 [Google Scholar]
  75. Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T. 2005. Illumination of the melanopsin signaling pathway. Science 307:600–4 [Google Scholar]
  76. Panda S, Provencio I, Tu DC, Pires SP, Rollag MD. et al. 2003. Melanopsin is required for non-image-forming photic responses in blind mice. Science 301:525–27 [Google Scholar]
  77. Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ. et al. 2002. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298:2213–16 [Google Scholar]
  78. Partch CL, Green CB, Takahashi JS. 2014. Molecular architecture of the mammalian circadian clock. Trends Cell Biol. 24:90–99 [Google Scholar]
  79. Perez-Leighton CE, Schmidt TM, Abramowitz J, Birnbaumer L, Kofuji P. 2011. Intrinsic phototransduction persists in melanopsin-expressing ganglion cells lacking diacylglycerol-sensitive TRPC subunits. Eur. J. Neurosci. 33:856–67 [Google Scholar]
  80. Peschel N, Veleri S, Stanewsky R. 2006. Veela defines a molecular link between Cryptochrome and Timeless in the light-input pathway to Drosophila's circadian clock. PNAS 103:17313–18 [Google Scholar]
  81. Pezük P, Mohawk JA, Wang LA, Menaker M. 2012. Glucocorticoids as entraining signals for peripheral circadian oscillators. Endocrinology 153:4775–83 [Google Scholar]
  82. Pierce ME, Sheshberadaran H, Zhang Z, Fox LE, Applebury ML, Takahashi JS. 1993. Circadian regulation of iodopsin gene expression in embryonic photoreceptors in retinal cell culture. Neuron 10:579–84 [Google Scholar]
  83. Pittendrigh CS. 1993. Temporal organization: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55:17–54 [Google Scholar]
  84. Pittler SJ, Keeler CE, Sidman RL, Baehr W. 1993. PCR analysis of DNA from 70-year-old sections of rodless retina demonstrates identity with the mouse rd defect. PNAS 90:9616–19 [Google Scholar]
  85. Polosukhina A, Litt J, Tochitsky I, Nemargut J, Sychev Y. et al. 2012. Photochemical restoration of visual responses in blind mice. Neuron 75:271–82 [Google Scholar]
  86. Provencio I. 2002. Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 415:493 [Google Scholar]
  87. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD. 1998. Melanopsin: an opsin in melanophores, brain, and eye. PNAS 95:340–45 [Google Scholar]
  88. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. 2000. A novel human opsin in the inner retina. J. Neurosci. 20:600–5 [Google Scholar]
  89. Provencio I, Rollag MD, Castrucci AM. 2002. Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 415:493 [Google Scholar]
  90. Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V. et al. 2005. Induction of photosensitivity by heterologous expression of melanopsin. Nature 433:745–49 [Google Scholar]
  91. Ralph MR, Foster RG, Davis FC, Menaker M. 1990. Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975–78 [Google Scholar]
  92. Rao S, Chun C, Fan J, Kofron JM, Yang MB. et al. 2013. A direct and melanopsin-dependent fetal light response regulates mouse eye development. Nature 494:243–46 [Google Scholar]
  93. Ribelayga C, Cao Y, Mangel SC. 2008. The circadian clock in the retina controls rod-cone coupling. Neuron 59:790–801 [Google Scholar]
  94. Rosbash M, Bradley S, Kadener S, Li Y, Luo W. et al. 2007. Transcriptional feedback and definition of the circadian pacemaker in Drosophila and animals. Cold Spring Harb. Symp. Quant. Biol. 72:75–83 [Google Scholar]
  95. Ruan G-X, Allen GC, Yamazaki S, McMahon D-G. 2008. An autonomous circadian clock in the inner mouse retina regulated by dopamine and GABA. PLOS Biol. 6:e249 [Google Scholar]
  96. Ruan G-X, Zhang D-Q, Zhou T, Yamazaki S, McMahon DG. 2006. Circadian organization of the mammalian retina. PNAS 103:9703–8 [Google Scholar]
  97. Ruby NF, Brennan TJ, Xie X, Cao V, Franken P. et al. 2002. Role of melanopsin in circadian responses to light. Science 298:2211–13 [Google Scholar]
  98. Sakamoto K, Liu C, Kasamatsu M, Iuvone PM, Tosini G. 2006. Intraocular injection of kainic acid does not abolish the circadian rhythm of arylalkylamine N-acetyltransferase mRNA in rat photoreceptors. Mol. Vis. 12:117–24 [Google Scholar]
  99. Sakamoto K, Liu C, Tosini G. 2004a. Circadian rhythms in the retina of rats with photoreceptor degeneration. J. Neurochem. 90:1019–24 [Google Scholar]
  100. Sakamoto K, Liu C, Tosini G. 2004b. Classical photoreceptors regulate melanopsin mRNA levels in the rat retina. J. Neurosci. 24:9693–97 [Google Scholar]
  101. Schlichting M, Helfrich-Förster C. 2015. Photic entrainment in Drosophila assessed by locomotor activity recordings. Methods Enzymol. 552:105–23 [Google Scholar]
  102. Schmidt TM, Chen S-K, Hattar S. 2011a. Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions. Trends Neurosci. 34:572–80 [Google Scholar]
  103. Schmidt TM, Do MTH, Dacey D, Lucas R, Hattar S, Matynia A. 2011b. Melanopsin-positive intrinsically photosensitive retinal ganglion cells: from form to function. J. Neurosci. 31:16094–101 [Google Scholar]
  104. Schmidt TM, Kofuji P. 2009. Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J. Neurosci. 29:476–82 [Google Scholar]
  105. Schmidt TM, Kofuji P. 2011. Structure and function of bistratified intrinsically photosensitive retinal ganglion cells in the mouse. J. Comp. Neurol. 519:1492–504 [Google Scholar]
  106. Semo M, Gias C, Ahmado A, Vugler A. 2014. A role for the ciliary marginal zone in the melanopsin-dependent intrinsic pupillary light reflex. Exp. Eye Res. 119:8–18 [Google Scholar]
  107. Sexton TJ, Bleckert A, Turner MH, Van Gelder RN. 2015. Type I intrinsically photosensitive retinal ganglion cells of early post-natal development correspond to the M4 subtype. Neural Dev. 10:17 [Google Scholar]
  108. Sexton TJ, Buhr E, Van Gelder RN. 2012a. Melanopsin and mechanisms of non-visual ocular photoreception. J. Biol. Chem. 287:1649–56 [Google Scholar]
  109. Sexton TJ, Golczak M, Palczewski K, Van Gelder RN. 2012b. Melanopsin is highly resistant to light and chemical bleaching in vivo. J. Biol. Chem. 287:20888–97 [Google Scholar]
  110. Sexton TJ, Van Gelder RN. 2015. G-protein coupled receptor kinase 2 minimally regulates melanopsin activity in intrinsically photosensitive retinal ganglion cells. PLOS ONE 10:e0128690 [Google Scholar]
  111. Sikka G, Hussmann GP, Pandey D, Cao S, Hori D. et al. 2014. Melanopsin mediates light-dependent relaxation in blood vessels. PNAS 111:17977–82 [Google Scholar]
  112. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B. et al. 2007. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130:730–41 [Google Scholar]
  113. Tarttelin EE, Bellingham J, Hankins MW, Foster RG, Lucas RJ. 2003. Neuropsin (Opn5): a novel opsin identified in mammalian neural tissue. FEBS Lett. 554:410–16 [Google Scholar]
  114. Tataroglu O, Emery P. 2015. The molecular ticks of the Drosophila circadian clock. Curr. Opin. Insect Sci. 7:51–57 [Google Scholar]
  115. Teirstein PS, Goldman AI, O'Brien PJ. 1980. Evidence for both local and central regulation of rat rod outer segment disc shedding. Investig. Ophthalmol. Vis. Sci. 19:1268–73 [Google Scholar]
  116. Terakita A, Tsukamoto H, Koyanagi M, Sugahara M, Yamashita T, Shichida Y. 2008. Expression and comparative characterization of Gq-coupled invertebrate visual pigments and melanopsin. J. Neurochem. 105:883–90 [Google Scholar]
  117. Thompson CL, Blaner WS, Van Gelder RN, Lai K, Quadro L. et al. 2001. Preservation of light-signaling to the suprachiasmatic nucleus in vitamin-A deficient mice. PNAS 98:11708–13 [Google Scholar]
  118. Thompson CL, Selby CP, Partch CL, Plante DT, Thresher RJ. et al. 2004a. Further evidence for the role of cryptochromes in retinohypothalamic photoreception/phototransduction. Mol. Brain Res. 122:158–66 [Google Scholar]
  119. Thompson CL, Selby CP, Van Gelder RN, Blaner WS, Lee J. et al. 2004b. Effect of vitamin A depletion on nonvisual phototransduction pathways in cryptochromeless mice. J. Biol. Rhythms 19:504–17 [Google Scholar]
  120. Thresher RJ, Vitaterna MH, Miyamoto Y, Kazantsev A, Hsu DS. et al. 1998. Role of mouse cryptochrome blue-light photoreceptor in circadian photoresponses. Science 282:1490–94 [Google Scholar]
  121. Tosini G, Davidson AJ, Fukuhara C, Kasamatsu M, Castanon-Cervantes O. 2007. Localization of a circadian clock in mammalian photoreceptors. FASEB J. 21:3866–71 [Google Scholar]
  122. Tosini G, Menaker M. 1996. Circadian rhythms in cultured mammalian retina. Science 272:419–21 [Google Scholar]
  123. Tosini G, Menaker M. 1998. The clock in the mouse retina: melatonin synthesis and photoreceptor degeneration. Brain Res. 789:221–28 [Google Scholar]
  124. Tu DC, Batten ML, Palczewski K, Van Gelder RN. 2004. Nonvisual photoreception in the chick iris. Science 306:129–31 [Google Scholar]
  125. Tu DC, Owens LA, Anderson L, Golczak M, Doyle SE. et al. 2006. Inner retinal photoreception independent of the visual retinoid cycle. PNAS 103:10426–31 [Google Scholar]
  126. Tu DC, Zhang D, Demas J, Slutsky EB, Provencio I. et al. 2005. Physiologic diversity and development of intrinsically photosensitive retinal ganglion cells. Neuron 48:987–99 [Google Scholar]
  127. Van Gelder RN, Wee R, Lee JA, Tu DC. 2003. Reduced pupillary light responses in mice lacking cryptochromes. Science 299:222 [Google Scholar]
  128. Walker MT, Brown RL, Cronin TW, Robinson PR. 2008. Photochemistry of retinal chromophore in mouse melanopsin. PNAS 105:8861–65 [Google Scholar]
  129. Wee R, Castrucci AM, Provencio I, Gan L, Van Gelder RN. 2002. Loss of photic entrainment and altered free-running circadian rhythms in math5−/− mice. J. Neurosci. 22:10427–33 [Google Scholar]
  130. Weng S, Wong KY, Berson DM. 2009. Circadian modulation of melanopsin-driven light response in rat ganglion-cell photoreceptors. J. Biol. Rhythms 24:391–402 [Google Scholar]
  131. Wong KY. 2012. A retinal ganglion cell that can signal irradiance continuously for 10 hours. J. Neurosci. 32:11478–85 [Google Scholar]
  132. Xue T, Do MTH, Riccio A, Jiang Z, Hsieh J. et al. 2011. Melanopsin signalling in mammalian iris and retina. Nature 479:67–73 [Google Scholar]
  133. Yoo S-H, Yamazaki S, Lowrey PL, Shimomura K, Ko CH. et al. 2004. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. PNAS 101:5339–46 [Google Scholar]
  134. Zhang D-Q, Belenky MA, Sollars PJ, Pickard GE, McMahon DG. 2012. Melanopsin mediates retrograde visual signaling in the retina. PLOS ONE 7:e42647 [Google Scholar]
  135. Zhang D-Q, Wong KY, Sollars PJ, Berson DM, Pickard GE, McMahon DG. 2008. Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. PNAS 105:14181–86 [Google Scholar]
  136. Zhao X, Stafford BK, Godin AL, King WM, Wong KY. 2014. Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells. J. Physiol. 592:1619–36 [Google Scholar]
  137. Zhu Y, Tu DC, Denner D, Shane T, Fitzgerald CM, Van Gelder RN. 2007. Melanopsin-dependent persistence and photopotentiation of murine pupillary light responses. Investig. Ophthalmol. Vis. Sci. 48:1268–75 [Google Scholar]
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  • Article Type: Review Article
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