1932

Abstract

We live on a planet that is bathed in daily and seasonal sunlight cycles. In this context, terrestrial life forms have evolved mechanisms that directly harness light energy (plants) or decode light information for adaptive advantage. In animals, the main light sensors are a family of G protein–coupled receptors called opsins. Opsin function is best described for the visual sense. However, most animals also use opsins for extraocular light sensing for seasonal behavior and camouflage. While it has long been believed that mammals do not have an extraocular light sensing capacity, recent evidence suggests otherwise. Notably, encephalopsin (OPN3) and neuropsin (OPN5) are both known to mediate extraocular light sensing in mice. Examples of this mediation include photoentrainment of circadian clocks in skin (by OPN5) and acute light-dependent regulation of metabolic pathways (by OPN3 and OPN5). This review summarizes current findings in the expanding field of extraocular photoreception and their relevance for human physiology.

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2023-09-15
2024-04-27
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Literature Cited

  1. Al-Juboori SI, Dondzillo A, Stubblefield EA, Felsen G, Lei TC, Klug A. 2013. Light scattering properties vary across different regions of the adult mouse brain. PLOS ONE 8:7e67626
    [Google Scholar]
  2. Ashton A, Foster RG, Jagannath A. 2022. Photic entrainment of the circadian system. Int. J. Mol. Sci. 23:2729
    [Google Scholar]
  3. Barreto Ortiz S, Hori D, Nomura Y, Yun X, Jiang H et al. 2018. Opsin 3 and 4 mediate light-induced pulmonary vasorelaxation that is potentiated by G protein-coupled receptor kinase 2 inhibition. Am. J. Physiol. Lung Cell. Mol. Physiol. 314:1L93–106
    [Google Scholar]
  4. Baumann C. 1977. Boll's phenomenon. Vis. Res. 17:11–121325–27
    [Google Scholar]
  5. Beaudry FEG, Iwanicki TW, Mariluz BRZ, Darnet S, Brinkmann H et al. 2017. The non-visual opsins: eighteen in the ancestor of vertebrates, astonishing increase in ray-finned fish, and loss in amniotes. J. Exp Zool. B 328:7685–96
    [Google Scholar]
  6. Bellingham J, Wells DJ, Foster RG. 2003. In silico characterisation and chromosomal localisation of human RRH (peropsin)—implications for opsin evolution. BMC Genom. 4:3
    [Google Scholar]
  7. Bertolesi GE, Atkinson-Leadbeater K, Mackey EM, Song YN, Heyne B, McFarlane S. 2020. The regulation of skin pigmentation in response to environmental light by pineal Type II opsins and skin melanophore melatonin receptors. J. Photochem. Photobiol. B 212:112024
    [Google Scholar]
  8. Bertolesi GE, McFarlane S. 2018. Seeing the light to change colour: an evolutionary perspective on the role of melanopsin in neuroendocrine circuits regulating light-mediated skin pigmentation. Pigment Cell Melanoma Res. 31:3354–73
    [Google Scholar]
  9. Blackshaw S, Snyder SH. 1999. Encephalopsin: a novel mammalian extraretinal opsin discretely localized in the brain. J. Neurosci. 19:103681–90
    [Google Scholar]
  10. Brown DM, Mazade R, Clarkson-Townsend D, Hogan K, Datta Roy PM, Pardue MT 2022. Candidate pathways for retina to scleral signaling in refractive eye growth. Exp. Eye Res. 219:109071
    [Google Scholar]
  11. Buhr ED, van Gelder RN. 2014. Local photic entrainment of the retinal circadian oscillator in the absence of rods, cones, and melanopsin. PNAS 111:238625–30
    [Google Scholar]
  12. Buhr ED, Vemaraju S, Diaz N, Lang RA, van Gelder RN. 2019. Neuropsin (OPN5) mediates local light-dependent induction of circadian clock genes and circadian photoentrainment in exposed murine skin. Curr. Biol. 29:203478–87.e4
    [Google Scholar]
  13. 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 112:4213093–98
    [Google Scholar]
  14. Buscone S, Mardaryev AN, Raafs B, Bikker JW, Sticht C et al. 2017. A new path in defining light parameters for hair growth: discovery and modulation of photoreceptors in human hair follicle. Lasers Surg. Med. 49:7705–18
    [Google Scholar]
  15. Byun J-H, Hyeon J-Y, Kim E-S, Kim B-H, Miyanishi H et al. 2020. Gene expression patterns of novel visual and non-visual opsin families in immature and mature Japanese eel males. PeerJ 8:e8326
    [Google Scholar]
  16. Castellano-Pellicena I, Uzunbajakava NE, Mignon C, Raafs B, Botchkarev VA, Thornton MJ 2019. Does blue light restore human epidermal barrier function via activation of opsin during cutaneous wound healing?. Lasers Surg. Med. 51:4370–82
    [Google Scholar]
  17. 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. 9:9e1001142
    [Google Scholar]
  18. Chen P, Hao W, Rife L, Wang XP, Shen D et al. 2001. A photic visual cycle of rhodopsin regeneration is dependent on Rgr. Nat. Genet. 28:3256–60
    [Google Scholar]
  19. Chen S-C, Robertson RM, Hawryshyn CW. 2013. Possible involvement of cone opsins in distinct photoresponses of intrinsically photosensitive dermal chromatophores in tilapia Oreochromis niloticus. PLOS ONE 8:8e70342
    [Google Scholar]
  20. Clothier J, Lythgoe JN. 1987. Light-induced colour changes by the iridophores of the neon tetra, Paracheirodon innesi. J. Cell Sci. 88:Part 5663–68
    [Google Scholar]
  21. Contreras E, Nobleman AP, Robinson PR, Schmidt TM. 2021. Melanopsin phototransduction: beyond canonical cascades. J. Exp. Biol. 224:23jeb226522
    [Google Scholar]
  22. Crescitelli F. 1977. Friedrich Wilhelm Kühne. The centennial of rhodopsin. Arch. Ophthalmol. 95:101766
    [Google Scholar]
  23. Crowe-Riddell JM, Simões BF, Partridge JC, Hunt DM, Delean S et al. 2019. Phototactic tails: evolution and molecular basis of a novel sensory trait in sea snakes. Mol. Ecol. 28:82013–28
    [Google Scholar]
  24. Currie SP, Doherty GH, Sillar KT. 2016. Deep-brain photoreception links luminance detection to motor output in Xenopus frog tadpoles. PNAS 113:216053–58
    [Google Scholar]
  25. Dan W, Park GH, Vemaraju S, Wu AD, Perez K et al. 2021. Light-mediated inhibition of colonic smooth muscle constriction and colonic motility via Opsin 3. Front. Physiol. 12:744294
    [Google Scholar]
  26. Dardente H, Simonneaux V. 2022. GnRH and the photoperiodic control of seasonal reproduction: delegating the task to kisspeptin and RFRP-3. J. Neuroendocrinol. 34:5e13124
    [Google Scholar]
  27. Dardente H, Wood S, Ebling F, Sáenz de Miera C. 2019. An integrative view of mammalian seasonal neuroendocrinology. J. Neuroendocrinol. 31:5e12729
    [Google Scholar]
  28. Davies WIL, Sghari S, Upton BA, Nord C, Hahn M et al. 2021. Distinct Opsin 3 (Opn3) expression in the developing nervous system during mammalian embryogenesis. eNeuro 8:5ENEURO.0141-21.2021
    [Google Scholar]
  29. Davies WIL, Tamai TK, Zheng L, Fu JK, Rihel J et al. 2015. An extended family of novel vertebrate photopigments is widely expressed and displays a diversity of function. Genome Res. 25:111666–79
    [Google Scholar]
  30. Davies WIL, Turton M, Peirson SN, Follett BK, Halford S et al. 2012. Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response. Biol. Lett. 8:2291–94
    [Google Scholar]
  31. de Assis LVM, Lacerda JT, Moraes MN, Domínguez-Amorocho OA, Kinker GS et al. 2022. Melanopsin (Opn4) is an oncogene in cutaneous melanoma. Commun. Biol. 5:461
    [Google Scholar]
  32. de Assis LVM, Moraes MN, Magalhães-Marques KK, de Lauro Castrucci AM. 2018. Melanopsin and rhodopsin mediate UVA-induced immediate pigment darkening: unravelling the photosensitive system of the skin. Eur. J. Cell Biol. 97:3150–62
    [Google Scholar]
  33. de Assis LVM, Moraes MN, Mendes D, Silva MM, Menck CFM, de Lauro Castrucci AM. 2021a. Loss of melanopsin (OPN4) leads to a faster cell cycle progression and growth in murine melanocytes. Curr. Issues Mol. Biol. 43:31436–50
    [Google Scholar]
  34. de Assis LVM, Tonolli PN, Moraes MN, Baptista MS, de Lauro Castrucci AM. 2021b. How does the skin sense sun light? An integrative view of light sensing molecules. J. Photochem. Photobiol. C 47:100403
    [Google Scholar]
  35. Díaz NM, Lang RA, van Gelder RN, Buhr ED. 2020. Wounding induces facultative Opn5- dependent circadian photoreception in the murine cornea. Investig. Opthalmol. Vis. Sci. 61:637
    [Google Scholar]
  36. Eilertsen M, Clokie BGJ, Ebbesson LOE, Tanase C, Migaud H, Helvik JV. 2021. Neural activation in photosensitive brain regions of Atlantic salmon (Salmo salar) after light stimulation. PLOS ONE 16:9e0258007
    [Google Scholar]
  37. Eppenberger LS, Sturm V. 2020. The role of time exposed to outdoor light for myopia prevalence and progression: a literature review. Clin. Ophthalmol. 14:1875–90
    [Google Scholar]
  38. Fernandes AM, Fero K, Arrenberg AB, Bergeron SA, Driever W, Burgess HA. 2012. Deep brain photoreceptors control light-seeking behavior in zebrafish larvae. Curr. Biol. 22:212042–47
    [Google Scholar]
  39. Fernandes AM, Fero K, Driever W, Burgess HA. 2013. Enlightening the brain: linking deep brain photoreception with behavior and physiology. Bioessays 35:9775–79
    [Google Scholar]
  40. Fernandez DC, Fogerson PM, Lazzerini Ospri L, Thomsen MB, Layne RM et al. 2018. Light affects mood and learning through distinct retina-brain pathways. Cell 175:171–84.e18
    [Google Scholar]
  41. Feuda R, Hamilton SC, McInerney JO, Pisani D. 2012. Metazoan opsin evolution reveals a simple route to animal vision. PNAS 109:4618868–72
    [Google Scholar]
  42. Feuda R, Menon AK, Göpfert MC. 2022. Rethinking opsins. Mol. Biol. Evol. 39:3msac033
    [Google Scholar]
  43. Filipek S, Stenkamp RE, Teller DC, Palczewski K. 2003. G protein-coupled receptor rhodopsin: a prospectus. Annu. Rev. Physiol. 65:851–79
    [Google Scholar]
  44. Finger A-M, Kramer A. 2021. Peripheral clocks tick independently of their master. Genes Dev. 35:5–6304–6
    [Google Scholar]
  45. 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. 11:6e1001585
    [Google Scholar]
  46. Fleury G, Masís-Vargas A, Kalsbeek A. 2020. Metabolic implications of exposure to light at night: lessons from animal and human studies. Obesity 28:Suppl. 1S18–28
    [Google Scholar]
  47. Flyktman A, Jernfors T, Manttari S, Nissila J, Timonen M, Saarela S. 2017. Transcranial light alters melanopsin and monoamine production in mouse (Mus musculus) brain. J. Neurol. Res. 7:339–45
    [Google Scholar]
  48. Fontinha BM, Zekoll T, Al-Rawi M, Gallach M, Reithofer F et al. 2021. TMT-Opsins differentially modulate medaka brain function in a context-dependent manner. PLOS Biol. 19:1e3001012
    [Google Scholar]
  49. Foster RG, Roenneberg T. 2008. Human responses to the geophysical daily, annual and lunar cycles. Curr. Biol. 18:17R784–94
    [Google Scholar]
  50. Friedmann D, Hoagland A, Berlin S, Isacoff EY. 2015. A spinal opsin controls early neural activity and drives a behavioral light response. Curr. Biol. 25:169–74
    [Google Scholar]
  51. Fulgione D, Trapanese M, Maselli V, Rippa D, Itri F et al. 2014. Seeing through the skin: Dermal light sensitivity provides cryptism in Moorish gecko. J. Zool. 294:2122–28
    [Google Scholar]
  52. Ganong WF, Shepherd MD, Wall JR, van Brunt EE, Clegg MT. 1963. Penetration of light into the brain of mammals. Endocrinology 72:6962–63
    [Google Scholar]
  53. García-Fernández JM, Cernuda-Cernuda R, Davies WIL, Rodgers J, Turton M et al. 2015. The hypothalamic photoreceptors regulating seasonal reproduction in birds: a prime role for VA opsin. Front. Neuroendocrinol. 37:13–28
    [Google Scholar]
  54. Haltaufderhyde K, Ozdeslik RN, Wicks NL, Najera JA, Oancea E. 2015. Opsin expression in human epidermal skin. Photochem. Photobiol. 91:1117–23
    [Google Scholar]
  55. Hang CY, Kitahashi T, Parhar IS. 2016. Neuronal organization of deep brain opsin photoreceptors in adult teleosts. Front. Neuroanat. 10:48
    [Google Scholar]
  56. 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. 497:3326–49
    [Google Scholar]
  57. Hrvatin S, Sun S, Wilcox OF, Yao H, Lavin-Peter AJ et al. 2020. Neurons that regulate mouse torpor. Nature 583:7814115–21
    [Google Scholar]
  58. Hu J, Shi Y, Zhang J, Huang X, Wang Q et al. 2022. Melanopsin retinal ganglion cells mediate light-promoted brain development. Cell 185:173124–37.e15
    [Google Scholar]
  59. Hubbard R. 1976. 100 years of rhodopsin. Trends Biochem. Sci. 1:7154–58
    [Google Scholar]
  60. Isoldi MC, Rollag MD, de Lauro Castrucci AM, Provencio I. 2005. Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin. PNAS 102:41217–21
    [Google Scholar]
  61. Ito C, Tomioka K. 2016. Heterogeneity of the peripheral circadian systems in Drosophila melanogaster: a review. Front. Physiol. 7:8
    [Google Scholar]
  62. Jastroch M, Giroud S, Barrett P, Geiser F, Heldmaier G, Herwig A. 2016. Seasonal control of mammalian energy balance: recent advances in the understanding of daily torpor and hibernation. J Neuroendocrinol. 28:11 https://doi.org/10.1111/jne.12437
    [Google Scholar]
  63. Jiang X, Kurihara T, Kunimi H, Miyauchi M, Ikeda SI et al. 2018. A highly efficient murine model of experimental myopia. Sci. Rep. 8:2026
    [Google Scholar]
  64. Jiang X, Pardue MT, Mori K, Ikeda SI, Torii H et al. 2021. Violet light suppresses lens-induced myopia via neuropsin (OPN5) in mice. PNAS 118:22e2018840118
    [Google Scholar]
  65. Jiao J, Hong S, Zhang J, Ma L, Sun Y et al. 2012. Opsin3 sensitizes hepatocellular carcinoma cells to 5-fluorouracil treatment by regulating the apoptotic pathway. Cancer Lett. 320:196–103
    [Google Scholar]
  66. Johnson J, Wu V, Donovan M, Majumdar S, Rentería RC et al. 2010. Melanopsin-dependent light avoidance in neonatal mice. PNAS 107:4017374–78
    [Google Scholar]
  67. Kang SW, Leclerc B, Kosonsiriluk S, Mauro LJ, Iwasawa A, el Halawani ME. 2010. Melanopsin expression in dopamine-melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds. Neuroscience 170:1200–13
    [Google Scholar]
  68. Kato M, Sugiyama T, Sakai K, Yamashita T, Fujita H et al. 2016. Two Opsin 3-related proteins in the chicken retina and brain: A TMT-type Opsin 3 is a blue-light sensor in retinal horizontal cells, hypothalamus, and cerebellum. PLOS ONE 11:11e0163925
    [Google Scholar]
  69. Kojima D, Mori S, Torii M, Wada A, Morishita R, Fukada Y. 2011. UV-sensitive photoreceptor protein OPN5 in humans and mice. PLOS ONE 6:10e26388
    [Google Scholar]
  70. Kokel D, Dunn TW, Ahrens MB, Alshut R, Cheung CYJ et al. 2013. Identification of nonvisual photomotor response cells in the vertebrate hindbrain. J. Neurosci. 33:93834–43
    [Google Scholar]
  71. Koyanagi M, Takada E, Nagata T, Tsukamoto H, Terakita A. 2013. Homologs of vertebrate Opn3 potentially serve as a light sensor in nonphotoreceptive tissue. PNAS 110:134998–5003
    [Google Scholar]
  72. Koyanagi M, Terakita A. 2014. Diversity of animal opsin-based pigments and their optogenetic potential. Biochim. Biophys. Acta Bioenerg. 1837:5710–16
    [Google Scholar]
  73. Kusumoto J, Takeo M, Hashikawa K, Komori T, Tsuji T et al. 2020. OPN4 belongs to the photosensitive system of the human skin. Genes Cells 25:3215–25
    [Google Scholar]
  74. Labbé SM, Caron A, Lanfray D, Monge-Rofarello B, Bartness TJ, Richard D. 2015. Hypothalamic control of brown adipose tissue thermogenesis. Front. Syst. Neurosci. 9:150
    [Google Scholar]
  75. Lan Y, Wang Y, Lu H. 2020. Opsin 3 is a key regulator of ultraviolet A-induced photoageing in human dermal fibroblast cells. Br. J. Dermatol. 182:51228–44
    [Google Scholar]
  76. Lan Y, Zeng W, Dong X, Lu H. 2021. Opsin 5 is a key regulator of ultraviolet radiation-induced melanogenesis in human epidermal melanocytes. Br. J. Dermatol. 185:2391–404
    [Google Scholar]
  77. Leung NY, Montell C. 2017. Unconventional roles of opsins. Annu. Rev. Cell Dev. Biol. 33:241–64
    [Google Scholar]
  78. Leung NY, Thakur DP, Gurav AS, Kim SH, di Pizio A et al. 2020. Functions of opsins in Drosophila taste. Curr. Biol. 30:81367–79.e6
    [Google Scholar]
  79. Ma H, Yang MS, Zhang YT, Qiu HT, You XX et al. 2022. Expressions of melanopsins in telencephalon imply their function in synchronizing semilunar spawning rhythm in the mudskipper Boleophthalmus pectinirostris. Gen. Comp. Endocrinol. 315:113926
    [Google Scholar]
  80. Martemyanov KA. 2014. G protein signaling in the retina and beyond: the Cogan Lecture. Investig. Ophthalmol. Vis. Sci. 55:128201–7
    [Google Scholar]
  81. Matsunaga N, Itcho K, Hamamura K, Ikeda E, Ikeyama H et al. 2014. 24-hour rhythm of aquaporin-3 function in the epidermis is regulated by molecular clocks. J. Investig. Dermatol. 134:61636–44
    [Google Scholar]
  82. McDowell RJ, Rodgers J, Milosavljevic N, Lucas RJ. 2022. Divergent G-protein selectivity across melanopsins from mice and humans. J. Cell Sci. 135:6jcs258474
    [Google Scholar]
  83. Mohawk JA, Green CB, Takahashi JS. 2012. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35:445–62
    [Google Scholar]
  84. Morris CJ, Yang JN, Scheer FAJL. 2012. The impact of the circadian timing system on cardiovascular and metabolic function. Prog. Brain Res. 199:337–58
    [Google Scholar]
  85. Morrison SF, Madden CJ, Tupone D. 2012. Central control of brown adipose tissue thermogenesis. Front. Endocrinol. 3:5
    [Google Scholar]
  86. Moutsaki P, Whitmore D, Bellingham J, Sakamoto K, David-Gray ZK, Foster RG. 2003. Teleost multiple tissue (tmt) opsin: a candidate photopigment regulating the peripheral clocks of zebrafish?. Brain Res. Mol. Brain Res. 112:1–2135–45
    [Google Scholar]
  87. Mure LS, Hatori M, Zhu Q, Demas J, Kim IM et al. 2016. Melanopsin-encoded response properties of intrinsically photosensitive retinal ganglion cells. Neuron 90:51016–27
    [Google Scholar]
  88. Musilova Z, Cortesi F, Matschiner M, Davies WIL, Patel JS et al. 2019. Vision using multiple distinct rod opsins in deep-sea fishes. Science 364:6440588–92
    [Google Scholar]
  89. Nakane Y, Ikegami K, Iigo M, Ono H, Takeda K et al. 2013. The saccus vasculosus of fish is a sensor of seasonal changes in day length. Nat. Commun. 4:2108
    [Google Scholar]
  90. 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 107:3415264–68
    [Google Scholar]
  91. Nakane Y, Shimmura T, Abe H, Yoshimura T. 2014. Intrinsic photosensitivity of a deep brain photoreceptor. Curr. Biol. 24:13R596–97
    [Google Scholar]
  92. Nakane Y, Shinomiya A, Ota W, Ikegami K, Shimmura T et al. 2019. Action spectrum for photoperiodic control of thyroid-stimulating hormone in Japanese quail (Coturnix japonica). PLOS ONE 14:9e0222106
    [Google Scholar]
  93. Nakane Y, Yoshimura T. 2014. Universality and diversity in the signal transduction pathway that regulates seasonal reproduction in vertebrates. Front. Neurosci. 8:115
    [Google Scholar]
  94. Nayak G, Zhang KX, Vemaraju S, Odaka Y, Buhr ED et al. 2020. Adaptive thermogenesis in mice is enhanced by Opsin 3-dependent adipocyte light sensing. Cell Rep. 30:3672–86.e8
    [Google Scholar]
  95. Nelson RJ, Chbeir S. 2018. Dark matters: effects of light at night on metabolism. Proc. Nutr. Soc. 77:3223–29
    [Google Scholar]
  96. Nguyen MTT, Vemaraju S, Nayak G, Odaka Y, Buhr ED et al. 2019. An Opsin 5-dopamine pathway mediates light-dependent vascular development in the eye. Nat. Cell Biol. 21:4420–29
    [Google Scholar]
  97. 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 198:11833–39
    [Google Scholar]
  98. Ohuchi H, Yamashita T, Tomonari S, Fujita-Yanagibayashi S, Sakai K et al. 2012. A non-mammalian type opsin 5 functions dually in the photoreceptive and non-photoreceptive organs of birds. PLOS ONE 7:2e31534
    [Google Scholar]
  99. Olinski LE, Lin EM, Oancea E. 2020a. Illuminating insights into opsin 3 function in the skin. Adv. Biol. Regul. 75:100668
    [Google Scholar]
  100. Olinski LE, Tsuda AC, Kauer JA, Oancea E. 2020b. Endogenous Opsin 3 (OPN3) protein expression in the adult brain using a novel OPN3-mCherry knock-in mouse model. eNeuro 7:5ENEURO.0107-20.2020
    [Google Scholar]
  101. Ondrusova K, Fatehi M, Barr A, Czarnecka Z, Long W et al. 2017. Subcutaneous white adipocytes express a light sensitive signaling pathway mediated via a melanopsin/TRPC channel axis. Sci. Rep. 7:16332
    [Google Scholar]
  102. Ozdeslik RN, Olinski LE, Trieu MM, Oprian DD, Oancea E. 2019. Human nonvisual opsin 3 regulates pigmentation of epidermal melanocytes through functional interaction with melanocortin 1 receptor. PNAS 116:2311508–17
    [Google Scholar]
  103. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H et al. 2000. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:5480739–45
    [Google Scholar]
  104. Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T. 2005. Illumination of the melanopsin signaling pathway. Science 307:5709600–4
    [Google Scholar]
  105. Panda S, Provencio I, Tu DC, Pires SS, Rollag MD et al. 2003. Melanopsin is required for non-image-forming photic responses in blind mice. Science 301:5632525–27
    [Google Scholar]
  106. Pasqualetti M, Bertolucci C, Ori M, Innocenti A, Magnone MC et al. 2003. Identification of circadian brain photoreceptors mediating photic entrainment of behavioural rhythms in lizards. Eur. J. Neurosci. 18:2364–72
    [Google Scholar]
  107. Pérez JH. 2022. Light receptors in the avian brain and seasonal reproduction. J. Exp. Zool. A 337:9–10985–93
    [Google Scholar]
  108. Pérez JH, Tolla E, Dunn IC, Meddle SL, Stevenson TJ. 2019. A comparative perspective on extra-retinal photoreception. Trends Endocrinol. Metab. 30:139–53
    [Google Scholar]
  109. Pérez-Cerezales S, Boryshpolets S, Afanzar O, Brandis A, Nevo R et al. 2015. Involvement of opsins in mammalian sperm thermotaxis. Sci. Rep. 5:16146
    [Google Scholar]
  110. Persinger MA, Dotta BT, Saroka KS. 2013. Bright light transmits through the brain: measurement of photon emissions and frequency-dependent modulation of spectral electroencephalographic power. World J. Neurosci. 3:110–16
    [Google Scholar]
  111. Pizarro A, Hayer K, Lahens NF, Hogenesch JB. 2012. CircaDB: a database of mammalian circadian gene expression profiles. Nucleic Acids Res. 41:D1D1009–13
    [Google Scholar]
  112. Plikus MV, van Spyk EN, Pham K, Geyfman M, Kumar V et al. 2015. The circadian clock in skin. J. Biol. Rhythms 30:3163–82
    [Google Scholar]
  113. Potter H, Alenciks E, Frazier K, Porter A, Fraley GS. 2018. Immunolesion of melanopsin neurons causes gonadal regression in Pekin drakes (Anas platyrhynchos domesticus). Gen. Comp. Endocrinol. 256:16–22
    [Google Scholar]
  114. Provencio I, Jiang G, de Grip WJ, Hayes WP, Rollag MD. 1998. Melanopsin: an opsin in melanophores, brain, and eye. PNAS 95:1340–45
    [Google Scholar]
  115. 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 494:7436243–46
    [Google Scholar]
  116. Roy D, Levi K, Kiss V, Nevo R, Eisenbach M. 2020. Rhodopsin and melanopsin coexist in mammalian sperm cells and activate different signaling pathways for thermotaxis. Sci. Rep. 10:112
    [Google Scholar]
  117. Regazzetti C, Sormani L, Debayle D, Bernerd F, Tulic MK et al. 2018. Melanocytes sense blue light and regulate pigmentation through Opsin-3. J. Investig. Dermatol. 138:1171–78
    [Google Scholar]
  118. Sandbakken M, Ebbesson L, Stefansson S, Helvik JV. 2012. Isolation and characterization of melanopsin photoreceptors of Atlantic salmon (Salmo salar). J. Comp. Neurol. 520:163727–44
    [Google Scholar]
  119. Sato K, Yamashita T, Ohuchi H, Takeuchi A, Gotoh H et al. 2018. Opn5L1 is a retinal receptor that behaves as a reverse and self-regenerating photoreceptor. Nat. Commun. 9:1255
    [Google Scholar]
  120. Sato M, Tsuji T, Yang K, Ren X, Dreyfuss JM et al. 2020. Cell-autonomous light sensitivity via Opsin3 regulates fuel utilization in brown adipocytes. PLOS Biol. 18:2e3000630
    [Google Scholar]
  121. Schilperoort M, Rensen PCN, Kooijman S. 2020. Time for novel strategies to mitigate cardiometabolic risk in shift workers. Trends Endocrinol. Metab. 31:12952–64
    [Google Scholar]
  122. Shen WL, Kwon Y, Adegbola AA, Luo J, Chess A, Montell C. 2011. Function of rhodopsin in temperature discrimination in Drosophila. Science 331:60221333–36
    [Google Scholar]
  123. Shichida Y, Matsuyama T. 2009. Evolution of opsins and phototransduction. Philos. Trans. R. Soc. B 364:15312881–95
    [Google Scholar]
  124. Shinojima A, Negishi K, Tsubota K, Kurihara T. 2022. Multiple factors causing myopia and the possible treatments: a mini review. Front. Public Health 10:897600
    [Google Scholar]
  125. Sikka G, Hussmann GP, Pandey D, Cao S, Hori D et al. 2014. Melanopsin mediates light-dependent relaxation in blood vessels. PNAS 111:5017977–82
    [Google Scholar]
  126. Starck T, Nissilä J, Aunio A, Abou-Elseoud A, Remes J et al. 2012. Stimulating brain tissue with bright light alters functional connectivity in brain at the resting state. World J. Neurosci. 2:281–90
    [Google Scholar]
  127. Sugiyama T, Suzuki H, Takahashi T. 2014. Light-induced rapid Ca2+ response and MAPK phosphorylation in the cells heterologously expressing human OPN5. Sci. Rep. 4:5352
    [Google Scholar]
  128. Suh S, Choi EH, Atanaskova Mesinkovska N. 2020. The expression of opsins in the human skin and its implications for photobiomodulation: a systematic review. Photodermatol. Photoimmunol. Photomed. 36:5329–38
    [Google Scholar]
  129. Sun H, Gilbert DJ, Copeland NG, Jenkins NA, Nathans J. 1997. Peropsin, a novel visual pigment-like protein located in the apical microvilli of the retinal pigmentepithelium. PNAS 94:189893–98
    [Google Scholar]
  130. Sun L, Peräkylä J, Kovalainen A, Ogawa KH, Karhunen PJ, Hartikainen KM. 2016. Human brain reacts to transcranial extraocular light. PLOS ONE 11:2e0149525
    [Google Scholar]
  131. Tarttelin EE, Bellingham J, Hankins MW, Foster RG, Lucas RJ. 2003. Neuropsin (Opn5): a novel opsin identified in mammalian neural tissue. FEBS Lett. 554:3410–16
    [Google Scholar]
  132. Tarttelin EE, Frigato E, Bellingham J, di Rosa V, Berti R et al. 2012. Encephalic photoreception and phototactic response in the troglobiont Somalian blind cavefish Phreatichthys andruzzii. J. Exp. Biol. 215:Part 162898–903
    [Google Scholar]
  133. Teng S, Zhen F, Wang L, Schalchli JC, Simko J et al. 2022. Control of non-REM sleep by ventrolateral medulla glutamatergic neurons projecting to the preoptic area. Nat. Commun. 13:4748
    [Google Scholar]
  134. Terakita A. 2005. The opsins. Genome Biol. 6:3213
    [Google Scholar]
  135. Tran LT, Park S, Kim SK, Lee JS, Kim KW, Kwon O. 2022. Hypothalamic control of energy expenditure and thermogenesis. Exp. Mol. Med. 54:4358–69
    [Google Scholar]
  136. Tsuchiya S, Buhr ED, Higashide T, Sugiyama K, van Gelder RN. 2017. Light entrainment of the murine intraocular pressure circadian rhythm utilizes non-local mechanisms. PLOS ONE 12:9e0184790
    [Google Scholar]
  137. Underwood H, Menaker M. 1970. Extraretinal light perception: entrainment of the biological clock controlling lizard locomotor activity. Science 170:3954190–93
    [Google Scholar]
  138. Upton B. 2021. Hypothalamic opsins: evolution and functions PhD Thesis Dept. Med. Univ. Cincinnati, OH: https://etd.ohiolink.edu/apexprod/rws_olink/r/1501/10?clear=10&p10_accession_num=ucin1627659750139728
  139. Upton BA, Díaz NM, Gordon SA, van Gelder RN, Buhr ED, Lang RA. 2021a. Evolutionary constraint on visual and nonvisual mammalian opsins. J. Biol. Rhythms 36:2109–26
    [Google Scholar]
  140. Upton BA, D'Souza SP, Lang RA 2021b. QPLOT neurons—converging on a thermoregulatory preoptic neuronal population. Front. Neurosci. 15:665762
    [Google Scholar]
  141. Upton BA, Nayak G, Schweinzger I, D'Souza SP, Vorhees CV et al. 2022. Comprehensive behavioral analysis of Opsin 3 (encephalopsin)-deficient mice identifies role in modulation of acoustic startle reflex. eNeuro 9:5ENEURO.0202-22.2022
    [Google Scholar]
  142. Vaiserman A. 2021. Season-of-birth phenomenon in health and longevity: epidemiologic evidence and mechanistic considerations. J. Dev. Orig. Health Dis. 12:6849–58
    [Google Scholar]
  143. van Veen T, Andersson M. 1982. Threshold for synchronization of locomotor activity to visible radiation in the eel Anguilla anguilla. Oikos 38:121–26
    [Google Scholar]
  144. Wade PD, Taylor J, Siekevitz P. 1988. Mammalian cerebral cortical tissue responds to low-intensity visible light. PNAS 85:239322–26
    [Google Scholar]
  145. Wagdi A, Malan D, Sathyanarayanan U, Beauchamp JS, Vogt M et al. 2022. Selective optogenetic control of Gq signaling using human Neuropsin. Nat. Commun. 13:1765
    [Google Scholar]
  146. Wang Y, Lan Y, Lu H. 2020. Opsin3 downregulation induces apoptosis of human epidermal melanocytes via mitochondrial pathway. Photochem Photobiol. 96:183–93
    [Google Scholar]
  147. Weaver DR, Reppert SM. 1989. Direct in utero perception of light by the mammalian fetus. Brain Res. Dev. Brain Res. 47:1151–55
    [Google Scholar]
  148. Weil T, Daly KM, Yarur Castillo H, Thomsen MB, Wang H et al. 2022. Daily changes in light influence mood via inhibitory networks within the thalamic perihabenular nucleus. Sci. Adv. 8:23eabn3567
    [Google Scholar]
  149. White JH, Chiano M, Wigglesworth M, Geske R, Riley J et al. 2008. Identification of a novel asthma susceptibility gene on chromosome 1qter and its functional evaluation. Hum. Mol. Genet. 17:131890–903
    [Google Scholar]
  150. Whitmore D, Foulkes NS, Sassone-Corsi P. 2000. Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404:677387–91
    [Google Scholar]
  151. Wong KY. 2012. A retinal ganglion cell that can signal irradiance continuously for 10 hours. J. Neurosci. 32:3311478–85
    [Google Scholar]
  152. Wood S, Loudon A. 2018. The pars tuberalis: the site of the circannual clock in mammals?. Gen. Comp. Endocrinol. 258:222–35
    [Google Scholar]
  153. Wu AD, Dan W, Zhang Y, Vemaraju S, Upton BA et al. 2021. Opsin 3-Gαs promotes airway smooth muscle relaxation modulated by G protein receptor kinase 2. Am. J. Respir. Cell Mol. Biol. 64:159–68
    [Google Scholar]
  154. Yamashita T, Ohuchi H, Tomonari S, Ikeda K, Sakai K, Shichida Y. 2010. Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. PNAS 107:5122084–89
    [Google Scholar]
  155. Yamashita T, Ono K, Ohuchi H, Yumoto A, Gotoh H et al. 2014. Evolution of mammalian Opn5 as a specialized UV-absorbing pigment by a single amino acid mutation. J. Biol. Chem. 289:73991–4000
    [Google Scholar]
  156. Yang MB, Rao S, Copenhagen DR, Lang RA. 2013. Length of day during early gestation as a predictor of risk for severe retinopathy of prematurity. Ophthalmology 120:122706–13
    [Google Scholar]
  157. Yim PD, Gallos G, Perez-Zoghbi JF, Zhang Y, Xu D et al. 2019. Airway smooth muscle photorelaxation via opsin receptor activation. Am. J. Physiol. Lung Cell. Mol. Physiol. 316:1L82–93
    [Google Scholar]
  158. Yim PD, Hyuga S, Wu AD, Dan W, Vink JY, Gallos G. 2020. Activation of an endogenous Opsin 3 light receptor mediates photo-relaxation of pre-contracting late gestation human uterine smooth muscle ex vivo. Reprod. Sci. 27:91791–801
    [Google Scholar]
  159. 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 101:155339–46
    [Google Scholar]
  160. Yoshimoto T, Morine Y, Takasu C, Feng R, Ikemoto T et al. 2018. Blue light-emitting diodes induce autophagy in colon cancer cells by Opsin 3. Ann. Gastroenterol. Surg. 2:2154–61
    [Google Scholar]
  161. Yoshimoto T, Shimada M, Tokunaga T, Nakao T, Nishi M et al. 2022. Blue light irradiation inhibits the growth of colon cancer and activation of cancer-associated fibroblasts. Oncol. Rep. 47:5104
    [Google Scholar]
  162. Yu S, Cheng H, François M, Qualls-Creekmore E, Huesing C et al. 2018. Preoptic leptin signaling modulates energy balance independent of body temperature regulation. eLife 7:e33505
    [Google Scholar]
  163. Zhang KX, D'Souza S, Upton BA, Kernodle S, Vemaraju S et al. 2020. Violet-light suppression of thermogenesis by opsin 5 hypothalamic neurons. Nature 585:7825420–25
    [Google Scholar]
  164. Zhang W, Feng J, Zeng W, He Z, Yang W, Lu H. 2022. Integrated analysis of the prognostic and oncogenic roles of OPN3 in human cancers. BMC Cancer 22:1187
    [Google Scholar]
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