Abstract
The variety of experimental approaches possible in amphibians, in particular, in the anuran species Xenopus laevis, have been crucial in discovering key regulators of circadian rhythms, such as melatonin and melanopsin. Differently from mammals, amphibians are characterized by the peculiar presence of multiple anatomical structures and cell types that feature photosensitive and self-sustained circadian activities. In particular, in amphibians, both the retina and the pineal complex are photosensitive and display circadian melatonin secretion. Furthermore, skin melanophores are light responsive and represent an exclusive model to study a peripheral circadian clock. In this chapter, we will review (1) the cellular and molecular mechanisms regulating circadian rhythms in amphibian retina, (2) the molecular bases of pineal circadian rhythms and its link to cell differentiation and cell proliferation, and (3) the Xenopus melanophore system as an example of a well-described peripheral, light-sensitive, clock.
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References
Alvarez-Viejo M, Cernuda-Cernuda R, DeGrip WJ, Alvarez-López C, García-Fernández JM (2003) Co-localization of mesotocin and opsin immunoreactivity in the hypothalamic preoptic nucleus of Xenopus laevis. Brain Res 969:36–43
Anderson KD (1986) Role of the eyes, frontal organ and pineal organ in the generation of the circadian activity rhythm and its entrainment by light in the South African clawed frog, Xenopus laevis. Ph.D. thesis, Northwestern University
Harada Y, Goto M, Ebihara S, Fujisawa H, Kegasawa K, Oishi T (1998) Circadian locomotor activity rhythms in the african clawed frog, Xenopus laevis: the role of the eye and the hypothalamus. Biol Rhythm Res 29:30–48
Gurdon JB (2014) A view of amphibian embryology during the last century. Int J Dev Biol 58:723–725
Andreazzoli M (2009) Molecular regulation of vertebrate retina cell fate. Birth Defects Res C Embryo Today 87:284–295
Besharse JC, Iuvone PM, Pierce ME (1988) Regulation of rhythmic photoreceptor metabolism: a role for post-receptoral neurons. Prog Retin Res 17:21–61
Anderson FE, Green CB (2000) Symphony of rhythms in Xenopus laevisretina. Microsc Res Tech 50:360–372
Besharse JC, Iuvone PM (1983) Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature 305:133–135
Green CB, Cahill GM, Besharse JC (1995) Regulation of tryptophan hydroxylase expression by a retinal circadian oscillator in vitro. Brain Res 677:283–290
Zhu H, LaRue S, Whiteley A, Steeves TD, Takahashi JS, Green CB (2000) The Xenopus clock gene is constitutively expressed in retinal photoreceptors. Brain Res Mol Brain Res 75:303–308
Zhuang M, Wang Y, Steenhard BM, Besharse JC (2000) Differential regulation of two period genes in the Xenopus eye. Brain Res Mol Brain Res 82:52–64
Curran KL, LaRue S, Bronson B, Solis J, Trow A, Sarver N, Zhu H (2008) Circadian genes are expressed during early development in Xenopus laevis. PLoS One 3, e2749
Cahill GM, Besharse JC (1993) Circadian clock functions localized in Xenopus retinal photoreceptors. Neuron 10:573–577
Cahill GM, Besharse JC (1995) Circadian rhythmicity in vertebrate retinas: regulation by a photoreceptor oscillator. Prog Retin Eye Res 14:267–291
Steenhard BM, Besharse JC (2000) Phase shifting the retinal circadian clock: xPer2 mRNA induction by light and dopamine. J Neurochem 20:8572–8577
Hasegawa M, Cahill GM (1998) Cyclic AMP resets the circadian clock in cultured Xenopus retinal photoreceptor layers. J Neurochem 70:1523–1531
Hasegawa M, Cahill GM (1999) A role for cyclicAMP in entrainment of the circadian oscillator in Xenopus retinal photoreceptors by dopamine but not by light. J Neurochem 72:1812–1820
Green CB, Besharse JC (2004) Retinal circadian clocks and control of retinal physiology. J Biol Rhythm 19:91–102
Hayasaka N, LaRue SI, Green CB (2002) In vivo disruption of Xenopus CLOCK in the retinal photoreceptor cells abolishes circadian melatonin rhythmicity without affecting its production levels. J Neurosci 22:1600–1607
Hayasaka N, LaRue SI, Green CB (2010) Differential contribution of rod and cone circadian clocks in driving retinal melatonin rhythms in Xenopus. PLoS One 5, e15599
Ebisawa T, Karne S, Lerner MR, Reppert SM (1994) Expression cloning of a high-affinity melatonin receptor from Xenopus dermal melanophores. Proc Natl Acad Sci U S A 91:6133–6137
Wiechmann AF, Campbell LD, Defoe DM (1999) Melatonin receptor RNA expression in Xenopus retina. Mol Brain Res 63:297–303
Dufourny L, Levasseur A, Migaud M, Callebaut I, Pontarotti P, Malpaux B, Monget P (2008) GPR50 is the mammalian ortholog of Mel1c: evidence of rapid evolution in mammals. BMC Evol Biol 8:105
Wiechmann AF, Sherry DM (2012) Melatonin receptors are anatomically organized to modulate transmission specifically to cone pathways in the retina of Xenopus laevis. J Comp Neurol 520:1115–1122
Cahill GM, Besharse JC (1989) Retinal melatonin is metabolized within the eye of Xenopus laevis. Proc Natl Acad Sci U S A 86:1098–1102
Kojima S, Sher-Chen EL, Green CB (2012) Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev 26:2724–2736
Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD (1998) Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci U S A 95:340–345
Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065–1070
Bertolesi GE, Hehr CL, McFarlane S (2014) Wiring the retinal circuits activated by light during early development. Neural Dev 9:3
Eakin RM (1961) Photoreceptor in the amphibian frontal organ. Proc Natl Acad Sci U S A 47:1084–1088
Mano H, Fukada Y (2007) A median third eye: pineal gland retraces evolution of vertebrate photoreceptive organs. Photochem Photobiol 83:11–18
Green CB, Liang MY, Steenhard BM, Besharse JC (1999) Ontogeny of circadian and light regulation of melatonin release in Xenopus laevis embryos. Brain Res Dev Brain Res 117:109–116
Chiba A, Kikuchi M, Aoki K (1993) The effects of pinealectomy and blinding on the circadian locomotor activity rhythm in the Japanese newt, Cynops pyrrhogaster. J Comp Physiol A 172:683–691
Chiba A, Kikuchi M, Aoki K (2003) Dissociation between the circadian rhythm of locomotor activity and the pineal clock in the Japanese newt. J Comp Physiol A 189:655–659
Hunt T, Sassone-Corsi P (2007) Riding tandem: circadian clocks and the cell cycle. Cell 129:461–464
Brown SA (2014) Circadian clock-mediated control of stem cell division and differentiation: beyond night and day. Development 141:3105–3111
Dekens MPS, Santoriello C, Vallone D, Grassi G, Whitmore D, Foulkes NS (2003) Light regulates the cell cycle in zebrafish. Curr Biol 13:2051–2057
Laranjeiro R, Tamai TK, Peyric E, Krusche P, Ott S, Whitmore D (2013) Cyclin-dependent kinase inhibitor p20 controls circadian cell-cycle timing. Proc Natl Acad Sci U S A 110:6835–6840
D’Autilia S, Broccoli V, Barsacchi G, Andreazzoli M (2010) Xenopus Bsx links daily cell cycle rhythms and pineal photoreceptor fate. Proc Natl Acad Sci U S A 107:6352–6357
Coon SL, Munson PJ, Cherukuri PF, Sugden D, Rath MF, Møller M, Clokie SJ, Fu C, Olanich ME, Rangel Z, Werner T, NISC Comparative Sequencing Program, Mullikin JC, Klein DC (2012) Circadian changes in long noncoding RNAs in the pineal gland. Proc Natl Acad Sci U S A 109:13319–13324
Oshima N (2001) Direct reception of light by chromatophores of lower vertebrates. Pigment Cell Res 14:312–319
Roubos EW, Van Wijk DC, Kozicz T, Scheenen WJ, Jenks BG (2010) Plasticity of melanotrope cell regulations in Xenopus laevis. Eur J Neurosci 32:2082–2086
Bagnara JT (1957) Hypophysectomy and the tail darkening reaction in Xenopus. Proc Soc Exp Biol Med 94:572–575
Lythgoe JN, Thompson M (1984) A porphyropsin-like action spectrum from Xenopus melanophores. Photochem Photobiol 40:411–412
Moriya T, Miyashita Y, Arai J, Kusunoki S, Abe M, Asami K (1996) Light-sensitive response in melanophores of Xenopus laevis: I Spectral characteristics of melanophore response in isolated tail fin of Xenopus tadpole. J Exp Zool 276:11–18
Miyashita Y, Moriya T, Yamada K, Kubota T, Shirakawa S, Fujii N, Asami K (2001) The photoreceptor molecules in Xenopus tadpole tail fin, in which melanophores exist. Zool Sci 18:671–674
Daniolos A, Lerner AB, Lerner MR (1990) Action of light on frog pigment cells in culture. Pigment Cell Res 3:38–43
McCord CP, Allen FP (1917) Evidences associating pineal gland function with alterations in pigmentation. J Exp Zool 23:207–224
Lerner AB, Case JD, Takahashi Y, Lee TH, Mori W (1958) Isolation of melatonin, the pineal gland factor that lightens melanocytes. J Am Chem Soc 80:2587–2592
Isoldi MC, Rollag MD, Castrucci AM (2005) I. Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin. Proc Natl Acad Sci U S A 102:1217–1221
Rollag MD, Provencio I, Sugden D, Green CB (2000) Cultured amphibian melanophores: a model system to study melanopsin photobiology. Methods Enzymol 316:291–309
Bluhm AP, Obeid NN, Castrucci AM, Visconti MA (2012) The expression of melanopsin and clock genes in Xenopus laevis melanophores and their modulation by melatonin. Braz J Med Biol Res 45:730–736
Moraes MN, dos Santos LR, Mezzalira N, Poletini MO, Castrucci AM (2014) Regulation of melanopsins and Per1 by α -MSH and melatonin in photosensitive Xenopus laevis melanophores. Biomed Res Int 2014:654710
Bertolesi GE, Hehr CL, McFarlane S (2015) Melanopsin photoreception in the eye regulates light-induced skin colour changes through the production of α-MSH in the pituitary gland. Pigment Cell Melanoma Res 28:559–571
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Andreazzoli, M., Angeloni, D. (2017). The Amphibian Clock System. In: Kumar, V. (eds) Biological Timekeeping: Clocks, Rhythms and Behaviour. Springer, New Delhi. https://doi.org/10.1007/978-81-322-3688-7_9
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DOI: https://doi.org/10.1007/978-81-322-3688-7_9
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