From blue light to clock genes in zebrafish ZEM-2S cells

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Ramos, Bruno C R ^a   Moraes, Maria Nathália C M ^a   Poletini, Maristela O ^a,b   Lima, Leonardo H R G ^a   Castrucci, Ana Maria L ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

MELANOPSIN; MITOGEN ACTIVATED PROTEIN KINASE; NEUROPSIN; NITRIC OXIDE; OPSIN; PHOSPHATIDYLINOSITIDE; CIRCADIAN RHYTHM SIGNALING PROTEIN; CRY1A PROTEIN, ZEBRAFISH; CRYPTOCHROME; EYE PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; PER1B PROTEIN, ZEBRAFISH; PER2 PROTEIN, ZEBRAFISH; PHOSPHATIDYLINOSITOL; SCOTOPSIN; ZEBRAFISH PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BLUE LIGHT; CELL SYNCHRONIZATION; CELL TYPE; CIRCADIAN RHYTHM; CONTROLLED STUDY; CRY1A GENE; CRY1B GENE; EMBRYO; ENZYME ACTIVATION; GENE; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PER1B GENE; PER2 GENE; PHOTOSTIMULATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ZEBRA FISH; ZEM 2S CELL; ANIMAL; ANIMAL EMBRYO; CELL LINE; CYTOLOGY; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; MOLECULAR GENETICS; RADIATION RESPONSE; RETINA; SUPRACHIASMATIC NUCLEUS;

DANIO RERIO;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CIRCADIAN CLOCKS; CRYPTOCHROMES; EMBRYO, NONMAMMALIAN; EYE PROTEINS; FIBROBLASTS; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; LIGHT; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; PERIOD CIRCADIAN PROTEINS; PHOSPHATIDYLINOSITOLS; PHOTIC STIMULATION; RETINA; ROD OPSINS; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84906971470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106252     Document Type: Article

References (103)

1. Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD (1998) Melanopsin: An opsin in melanophores, brain, and eye. Proc Natl Acad Sci USA 95:340-345.
2. Jenkins A, Munoz M, Tarttelin EE, Bellingham J, Foster RG, et al. (2003) VA opsin, melanopsin, and an inherent light response within retinal interneurons. Curr Biol 13:1269-1278.
3. Bailey MJ, Cassone VM (2005) Melanopsin expression in the chick retina and pineal gland. Brain Res Mol Brain Res 134:345-348.
4. Chaurasia SS, Rollag MD, Jiang G, Hayes WP, Haque R, et al. (2005) Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J Neurochem 92:158-170.
5. Bellingham J, Chaurasia SS, Melyan Z, Liu C, Cameron MA, et al. (2006) Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. PLoS Biol 4:e254.
6. Tomonari S, Takagi A, Noji S, Ohuchi H (2007) Expression pattern of the melanopsin-like (cOpn4m) and VA opsin-like genes in the developing chicken retina and neural tissues. Gene Expr Patterns 7:746-753.
7. Davies WI, Zheng L, Hughes S, Tamai TK, Turton M, et al. (2011) Functional diversity of melanopsins and their global expression in the teleost retina. Cell Mol Life Sci 68:4115-4132.
8. Davies WI, Tay BH, Zheng L, Danks JA, Brenner S, et al. (2012) Evolution and functional characterisation of melanopsins in a deep-sea chimaera (elephant shark, Callorhinchus milii). PLoS One 7(12):e51276.
9. Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070-1073.
10. 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.
11. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, et al. (2003) Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299:245-247.
12. Ruby NF, Brennan TJ, Xie X, Cao V, Franken P, et al. (2002) Role of melanopsin in circadian responses to light. Science 298:2211-2213.
13. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, et al. (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307-320.
14. 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 301:525-527.
15. Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413:186-193.
16. Newman LA, Walker MT, Brown RL, Cronin TW, Robinson PR (2003) Melanopsin forms a functional short-wavelength photopigment. Biochemistry 42(44):12734-12738.
17. Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, et al. (2005) Illumination of the melanopsin signaling pathway. Science 307:600-604.
18. Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW (2005) Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433:741-745.
19. Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, et al. (2005) Induction of photosensitivity by heterologous expression of melanopsin. Nature 433:745-749.
20. Isoldi MC, Rollag MD, Castrucci AM, Provencio I (2005) Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin. Proc Natl Acad Sci USA 102:1217-1221.
21. Contin MA, Verra DM, Guido ME (2006) An invertebrate-like phototransduction cascade mediates light detection in the chicken retinal ganglion cells. FASEB J 20(14):2648-2650.
22. Peirson SN, Oster H, Jones SL, Leitges M, Hankins MW, et al. (2007) Microarray analysis and functional genomics identify novel components of melanopsin signaling. Curr Biol 17(16):1363-1372.
23. Graham DM, Wong KY, Shapiro P, Frederick C, Pattabiraman K, et al. (2008) Melanopsin ganglion cells use a membrane-associated rhabdomeric phototransduction cascade. J Neurophysiol 99(5):2522-2532.
24. Kumbalasiri T, Rollag MD, Isoldi MC, Castrucci AM, Provencio I (2007) Melanopsin triggers the release of internal calcium stores in response to light. Photochem Photobiol 83:273-279.
25. Moutsaki P, Whitmore D, Bellingham J, Sakamoto K, David-Gray ZK, et al. (2003) Teleost multiple tissue (tmt) opsin: a candidate photopigment regulating the peripheral clocks of zebrafish? Brain Res Mol Brain Res 112:135-145.
26. 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(9):e1001142.
27. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271-290.
28. Shearman LP, Sriram S, Weaver DR, Maywood ES, Chaves I, et al. (2000) Interacting molecular loops in the mammalian circadian clock. Science 288:1013-1019.
29. Okamura H, Yamaguchi S, Yagita K (2002) Molecular machinery of the circadian clock in mammals. Cell Tissue Res 309:47-56.
30. Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330:1349-1354.
31. Zhang EE, Kay SA (2010) Clocks not winding down: unravelling circadian networks. Nat Rev Mol Cell Biol 11:764-776.
32. Huang W, Ramsey KM, Marcheva B, Bass J (2011) Circadian rhythms, sleep, and metabolism. J Clin Invest 121:2133-2141.
33. Emery P, So WV, Kaneko M, Hall JC, Rosbash M (1998) CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95:669-679.
34. Plautz JD, Kaneko M, Hall JC, Kay SA (1997) Independent photoreceptive circadian clocks throughout Drosophila. Science 278(5343):1632-1635.
35. Ceriani MF, Darlington TK, Staknis D, Mas P, Petti AA, et al. (1999) Lightdependent sequestration of TIMELESS by CRYPTOCHROME. Science 285:553-556.
36. Whitmore D, Foulkes NS, Sassone-Corsi P (2000) Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404:87-91.
37. Pando MP, Morse D, Cermakian N, Sassone-Corsi P (2002) Phenotypic rescue of a peripheral clock genetic defect via SCN hierarchical dominance. Cell 110:107-117.
38. Farhat FP, Martins CB, De Lima LH, Isoldi MC, Castrucci AM (2009) Melanopsin and clock genes: regulation by light and endothelin in the zebrafish ZEM-2S cell line. Chronobiol Int 26:1090-1119.
39. Buhr ED, Yoo SH, Takahashi JS (2010) Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330:379-385.
40. Balsalobre A, Damiola F, Schibler U (1998) A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:929-937.
41. Drivenes Ø1, Søviknes AM, Ebbesson LO, Fjose A, Seo HC, et al. (2003) Isolation and characterization of two teleost melanopsins and their differential expression within the inner retina. J Comp Neurol 456(1):84-93.
42. Lima LHRG, Scarparo AC, Isoldi MC, Visconti MA, Castrucci AML (2006) Melanopsin in chicken melanocytes and retina. Biol Rhythm Res 37:393-404.
43. Bilotta J, Saszik S (2001) The zebrafish as a model visual system. Int J Dev Neurosci 19:621-629.
44. Gonzalez-Nunez V, Rodriguez RE (2009) The zebrafish: a model to study the endogenous mechanisms of pain. ILAR J 50:373-386.
45. Chakraborty C, Hsu CH, Wen ZH, Lin CS, Agoramoorthy G (2009) Zebrafish: a complete animal model for in vivo drug discovery and development. Curr Drug Metab 10:116-124.
46. Cahill GM (2002) Clock mechanisms in zebrafish. Cell Tissue Res 309(1):27-34.
47. Tamai TK, Carr AJ, Whitmore D (2005) Zebrafish circadian clocks: cells that see light. Biochem Soc Trans 33(Pt 5):962-966.
48. Idda ML, Bertolucci C, Vallone D, Gothilf Y, Sánchez-Vázquez FJ, et al. (2012) Circadian clocks: lessons from fish. Prog Brain Res 199:41-57.
49. Vatine G, Vallone D, Gothilf Y, Foulkes NF (2011) It's time to swim! Zebrafish and the circadian clock. FEBS lett 585(10):1485-1494.
50. Goidin D, Mamessier A, Staquet MJ, Schmitt D, Berthier-Vergnes O (2001) Ribosomal 18S RNA prevails over glyceraldehyde-3-phosphate dehydrogenase and beta-actin genes as internal standard for quantitative comparison of mRNA levels in invasive and noninvasive human melanoma cell subpopulations. Anal Biochem 295:17-21.
51. McCurley TA, Callard GV (2008) Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Biol 9:102-119.
52. Aerts JL, Gonzales MI, Topalian LS (2004) Selection of appropriate control genes to assess expression of tumor antigens using real-time RT-PCR. Biotechniques 36:84-86, 88, 90-91.
53. Zhu LJ, Altmann SW (2005) mRNA and 18S-RNA coapplication-reverse transcription for quantitative gene expression analysis. Anal Biochem 345:102-109.
54. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 25:402-408.
55. Ziv L, Gothilf Y (2006) Period2 expression pattern and its role in the development of the pineal circadian clock in zebrafish. Chronobiol Int 23(1-2):101-112.
56. Tamai TK, Young LC, Whitmore D (2007) Light signaling to the zebrafish circadian clock by Cryptochrome 1a. Proc Natl Acad Sci USA 104(37):14712-14717.
57. Golombek DA, Rosenstein RE (2010) Physiology of circadian entrainment. Physiol Rev 90:1063-1102.
58. Hayashi Y, Nishio M, Naito Y, Yokokura H, Nimura Y, et al. (1999) Regulation of neuronal nitric-oxide synthase by calmodulin kinases. J Biol Chem 274(29):20597-20602.
59. Cermakian N, Pando MP, Thompson CL, Pinchak AB, Selby CP, et al. (2002) Light induction of a vertebrate clock gene involves signaling through blue-light receptors and MAP kinases. Curr Biol 12(10):844-848.
60. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291:490-493.
61. Blum ID, Lamont EW, Abizaid A (2012) Competing clocks: metabolic status moderates signals from the master circadian pacemaker. Neurosci Biobehav Rev 36:254-270.
62. Rollag MD, Provencio I, Sugden D, Green CB (2000) Cultured amphibian melanophores: A model system to study melanopsin photobiology. Methods Enzymol 316:291-309.
63. Tamai TK, Carr AJ, Whitmore D (2005) Zebrafish circadian clocks: cells that see light. Biochem Soc Trans 33(5):962-966.
64. Hirayama J, Cho S, Sassone-Corsi P (2007) Circadian control by the reduction/oxidation pathway: catalase represses light-dependent clock gene expression in the zebrafish. Proc Natl Acad Sci USA 104(40):15747-15752.
65. Mracek P, Pagano C, Fröhlich N, Idda ML, Cuesta IH, et al. (2013) ERK signaling regulates light-induced gene expression via D-Box enhancers in a differential, wavelength-dependent manner. PLoS One 8(6):e67858.
66. Hughes S, Hankins MW, Foster RG, Peirson SN (2012) Melanopsin phototransduction: Slowly emerging from the dark. Progress in Brain Res 199:19-40.
67. Sekaran S, Foster RG, Lucas RJ, Hankins MW (2003) Calcium imaging reveals a network of intrinsically light-sensitive inner-retinal neurons. Curr Biol 13:1290-1298.
68. 2+-dependent phosphatase. Biochem J 365:295-301.
69. Nishizuka Y (1988) The heterogeneity and differential expression of multiple species of the protein kinase C family. Biofactors 1:17-20.
70. Patten SA, Sihra RK, Dhami KS, Coutts CA, Ali DW (2007) Differential expression of PKC isoforms in developing zebrafish. Int J Dev Neurosci 25:155-164.
71. Koyanagi M, Terakita A (2014) Diversity of animal opsin-based pigments and their optogenetic potential. Biochim Biophys Acta 1837:710-716.
72. Davies WL, Hankins MW, Foster RG (2010) Vertebrate ancient opsin and melanopsin: divergent irradiance detectors. Photochem Photobiol Sci 9:1444-1457.
73. Koyanagi M, Takada E, Nagata T, Tsukamoto H, Terakita A (2013) Homologs of vertebrate Opn3 potentially serve as a light sensor in nonphotoreceptive tissue. Proc Natl Acad Sci USA 110(13):4998-5003.
74. Ozturk N, Selby CP, Zhong D, Sancar A (2014) Mechanism of photosignaling by Drosophila cryptochrome: role of the redox status of the flavin chromophore. J Biol Chem 289(8):4634-4642.
75. Pittendrigh CS (1993) Temporal organization: reflections of a Darwinian clockwatcher. Annu Rev Physiol 55:16-54.
76. Hankins MW, Peirson SN, Foster RG (2008) Melanopsin: an exciting photopigment. Trends Neurosci 31:27-36.
77. Prosser RA, Gillette MU (1991) Cyclic changes in cAMP concentration and phosphodiesterase activity in a mammalian circadian clock studied in vitro. Brain Res 568:185-192.
78. Ferreyra GA, Golombek DA (2000) Cyclic AMP and protein kinase A rhythmicity in the mammalian suprachiasmatic nuclei. Brain Res 858:33-39.
79. Prosser RA, Gillette MU (1989) The mammalian circadian clock in the suprachiasmatic nuclei is reset in vitro by cAMP. J Neurosci 9:1073-1081.
80. O'Neill JS, Maywood ES, Chesham JE, Takahashi JS, Hastings MH (2008) cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320:949-953.
81. 2+/calmodulin kinase II, attenuates circadian responses to light. Neuroreport 5:1638-1640.
82. Golombek DA, Ralph MR (1995) Circadian responses to light: the calmodulin connection. Neurosci Lett 192:101-104.
83. Ding JM, Chen D, Weber ET, Faiman LE, Rea MA, et al. (1994) Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science 266:1713-1717.
84. Watanabe A, Ono M, Shibata S, Watanabe S (1995) Effect of a nitric oxide synthase inhibitor, N-nitro-L-arginine methylester, on light-induced phase delay of circadian rhythm of wheel-running activity in golden hamsters. Neurosci Lett 192:25-28.
85. 2+/calmodulin-dependent protein kinase II in the circadian rhythms controlled by the suprachiasmatic nucleus. Neurosci Lett 227:45-48.
86. Melo L, Golombek DA, Ralph MR (1997) Regulation of circadian photic responses by nitric oxide. J Biol Rhythms 12:319-326.
87. Ferreyra GA, Cammarota MP, Golombek DA (1998) Photic control of nitric oxide synthase activity in the hamster suprachiasmatic nuclei. Brain Res 797:190-196.
88. Agostino PV, Ferreyra GA, Murad AD, Watanabe Y, Golombek DA (2004) Diurnal, circadian and photic regulation of calcium/calmodulin-dependent kinase II and neuronal nitric oxide synthase in the hamster suprachiasmatic nuclei. Neurochem Int 44:617-625.
89. Yun HY, Gonzalez-Zulueta M, Dawson VL, Dawson TM (1998) Nitric oxide mediates N-methyl-D-aspartate receptor-induced activation of p21ras. Proc Natl Acad Sci USA 95:5773-5778.
90. Obrietan K, Impey S, Smith D, Athos J, Storm DR (1999) Circadian regulation of cAMP response element-mediated gene expression in the suprachiasmatic nuclei. J Biol Chem 274:17748-17756.
91. Krishna M, Narang H (2008) The complexity of mitogen-activated protein kinases (MAPKs) made simple. Cell Mol Life Sci 65:3525-3544.
92. Chansard M, Molyneux P, Nomura K, Harrington ME, Fukuhara C (2007) c-Jun. N-terminal kinase inhibitor SP600125 modulates the period of mammalian circadian rhythms. Neuroscience 145:812-823.
93. Akashi M, Hayasaka N, Yamazaki S, Node K (2008) Mitogen-activated protein kinase is a functional component of the autonomous circadian system in the suprachiasmatic nucleus. J Neurosci 28:4619-4623.
94. Obrietan K, Impey S, Storm DR (1998) Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat Neurosci 1:693-700.
95. Butcher GQ, Doner J, Dziema H, Collamore M, Burgoon PW, et al. (2002) The p42/44 mitogen-activated protein kinase pathway couples photic input to circadian clock entrainment. J Biol Chem 277:29519-29525.
96. Butcher GQ, Lee B, Obrietan K (2003) Temporal regulation of light-induced extracellular signal-regulated kinase activation in the suprachiasmatic nucleus. J Neurophysiol 90:3854-3863.
97. Dziema H, Oatis B, Butcher GQ, Yates R, Hoyt KR, et al. (2003) The ERK/MAP kinase pathway couples light to immediate-early gene expression in the suprachiasmatic nucleus. Eur J Neurosci 17:1617-1627.
98. Pizzio GA, Hainich EC, Ferreyra GA, Coso OA, Golombek DA (2003) Circadian and photic regulation of ERK, JNK and p38 in the hamster SCN. Neuroreport 14:1417-1419.
99. Hirayama J, Miyamura N, Uchida Y, Asaoka Y, Honda R, et al. (2009) Common light signaling pathways controlling DNA repair and circadian clock entrainment in zebrafish. Cell Cycle 8(17):2794-2801.
100. Ding JM, Faiman LE, Hurst WJ, Kuriashkina LR, Gillette MU (1997) Resetting the biological clock: mediation of nocturnal CREB phosphorylation via light, glutamate, and nitric oxide. J Neurosci 17:667-675.
101. Uchida Y, Hirayama J, Nishina H (2010) A common origin: signaling similarities in the regulation of the circadian clock and DNA damage responses. Biol Pharm Bull 33(4):535-544.
102. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6(2):150-166.
103. Martínez-Ruiz A, Cadenas S, Lamas S (2011) Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic Biol Med 51(1):17-29.