The light-induced transcriptome of the zebrafish pineal gland reveals complex regulation of the circadian clockwork by light

Nucleic Acids Research

Volumn 42, Issue 6, 2014, Pages 3750-3767

  Ben Moshe, Zohar ^a   Alon, Shahar ^a   Mracek, Philipp ^b   Faigenbloom, Lior ^a   Tovin, Adi ^a   Vatine, Gad D ^a   Eisenberg, Eli ^a   Foulkes, Nicholas S ^b   Gothilf, Yoav ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3' UNTRANSLATED REGIONS; ANIMALS; CIRCADIAN CLOCKS; HEK293 CELLS; HUMANS; LIGHT; LOCOMOTION; METABOLIC NETWORKS AND PATHWAYS; MICRORNAS; PINEAL GLAND; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSCRIPTOME; ZEBRAFISH;

EID: 84899004316     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1359     Document Type: Article

References (69)

1. Pittendrigh, C. S. (1993) Temporal organization: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol., 55, 16-54.
2. Dunlap, J. C. (1999) Molecular bases for circadian clocks. Cell, 96, 271-290.
3. Ko, C. H. and Takahashi, J. S. (2006) Molecular components of the mammalian circadian clock. Hum. Mol. Genet., 15, R271-R277. (Pubitemid 44446803)
4. Mehra, A., Baker, C. L., Loros, J. J. and Dunlap, J. C. (2009) Posttranslational modifications in circadian rhythms. Trends Biochem. Sci., 34, 483-490.
5. Doyle, S. and Menaker, M. (2007) Circadian photoreception in vertebrates. Cold Spring Harb. Symp. Quant. Biol., 72, 499-508.
6. Vatine, G., Vallone, D., Gothilf, Y. and Foulkes, N. S. (2011) It's time to swim! zebrafish and the circadian clock. FEBS Lett., 585, 1485-1494.
7. Falcon, J., Besseau, L., Fuentes, M., Sauzet, S., Magnanou, E. and Boeuf, G. (2009) Structural and functional evolution of the pineal melatonin system in vertebrates. Ann. N. Y. Acad. Sci., 1163, 101-111.
8. Whitmore, D., Foulkes, N. S. and Sassone-Corsi, P. (2000) Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature, 404, 87-91.
9. Devlin, P. F. and Kay, S. A. (2001) Circadian photoperception. Annu. Rev. Physiol., 63, 677-694.
10. Tamai, T. K., Young, L. C. and Whitmore, D. (2007) Light signaling to the zebrafish circadian clock by Cryptochrome 1a. Proc. Natl Acad. Sci. USA, 104, 14712-14717.
11. Ziv, L., Levkovitz, S., Toyama, R., Falcon, J. and Gothilf, Y. (2005) Functional development of the zebrafish pineal gland: lightinduced expression of period2 is required for onset of the circadian clock. J. Neuroendocrinol., 17, 314-320.
12. Mracek, P., Santoriello, C., Idda, M. L., Pagano, C., Ben-Moshe, Z., Gothilf, Y., Vallone, D. and Foulkes, N. S. (2012) Regulation of per and cry genes reveals a central role for the D-Box enhancer in light-dependent gene expression. PLoS One, 7, e51278.
13. Vatine, G., Vallone, D., Appelbaum, L., Mracek, P., Ben-Moshe, Z., Lahiri, K., Gothilf, Y. and Foulkes, N. S. (2009) Light directs zebrafish period2 expression via conserved D and E boxes. PLoS Biol., 7, e1000223.
14. Gavriouchkina, D., Fischer, S., Ivacevic, T., Stolte, J., Benes, V. and Dekens, M. P. (2010) Thyrotroph embryonic factor regulates light-induced transcription of repair genes in zebrafish embryonic cells. PLoS One, 5, e12542.
15. Weger, B. D., Sahinbas, M., Otto, G. W., Mracek, P., Armant, O., Dolle, D., Lahiri, K., Vallone, D., Ettwiller, L., Geisler, R. et al. (2011) The light responsive transcriptome of the zebrafish: function and regulation. PLoS One, 6, e17080.
16. Wang, Z., Gerstein, M. and Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet., 10, 57-63.
17. Gothilf, Y., Toyama, R., Coon, S. L., Du, S. J., Dawid, I. B. and Klein, D. C. (2002) Pineal-specific expression of green fluorescent protein under the control of the serotonin-N-acetyltransferase gene regulatory regions in transgenic zebrafish. Dev. Dyn., 225, 241-249.
18. Trapnell, C., Pachter, L. and Salzberg, S. L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
19. Levin, J. Z., Yassour, M., Adiconis, X., Nusbaum, C., Thompson, D. A., Friedman, N., Gnirke, A. and Regev, A. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat. Methods, 7, 709-715.
20. Alon, S., Vigneault, F., Eminaga, S., Christodoulou, D. C., Seidman, J. G., Church, G. M. and Eisenberg, E. (2011) Barcoding bias in high-throughput multiplex sequencing of miRN A. Genome Res., 21, 1506-1511.
21. Robinson, M. D. and Oshlack, A. (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol., 11, R25.
22. Alon, S., Mor, E., Vigneault, F., Church, G. M., Locatelli, F., Galeano, F., Gallo, A., Shomron, N. and Eisenberg, E. (2012) Systematic identification of edited microRNAs in the human brain. Genome Res., 22, 1533-1540.
23. Kozomara, A. and Griffiths-Jones, S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res., 39, D152-D157.
24. Bolstad, B. M., Irizarry, R. A., Astrand, M. and Speed, T. P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics, 19, 185-193.
25. Rocke, D. M. and Durbin, B. (2001) A model for measurement error for gene expression arrays. J. Comput. Biol., 8, 557-569.
26. Huang da, W., Sherman, B. T. and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
27. Ben-Moshe, Z., Vatine, G., Alon, S., Tovin, A., Mracek, P., Foulkes, N. S. and Gothilf, Y. (2010) Multiple PAR and E4BP4 bZIP transcription factors in zebrafish: diverse spatial and temporal expression patterns. Chronobiol. Int., 27, 1509-1531.
28. Lin, S., Gaiano, N., Culp, P., Burns, J. C., Friedmann, T., Yee, J. K. and Hopkins, N. (1994) Integration and germ-line transmission of a pseudotyped retroviral vector in zebrafish. Science, 265, 666-669.
29. Vallone, D., Santoriello, C., Gondi, S. B. and Foulkes, N. S. (2007) Basic protocols for zebrafish cell lines: maintenance and transfection. Methods Mol. Biol., 362, 429-441.
30. Vallone, D., Gondi, S. B., Whitmore, D. and Foulkes, N. S. (2004) E-box function in a period gene repressed by light. Proc. Natl Acad. Sci. USA, 101, 4106-4111.
31. Travnickova-Bendova, Z., Cermakian, N., Reppert, S. M. and Sassone-Corsi, P. (2002) Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc. Natl Acad. Sci. USA, 99, 7728-7733.
32. Abe, M., Herzog, E. D., Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M. and Block, G. D. (2002) Circadian rhythms in isolated brain regions. J. Neurosci., 22, 350-356.
33. Ziv, L. and Gothilf, Y. (2006) Circadian time-keeping during early stages of development. Proc. Natl Acad. Sci. USA, 103, 4146-4151.
34. Smadja Storz, S., Tovin, A., Mracek, P., Alon, S., Foulkes, N. S. and Gothilf, Y. (2013) Casein kinase 1delta activity: a key element in the zebrafish circadian timing system. PLoS One, 8, e54189.
35. Tovin, A., Alon, S., Ben-Moshe, Z., Mracek, P., Vatine, G., Foulkes, N. S., Jacob-Hirsch, J., Rechavi, G., Toyama, R., Coon, S. L. et al. (2012) Systematic identification of rhythmic genes reveals camk1gb as a new element in the circadian clockwork. PLoS Genet., 8, e1003116.
36. Voorhoeve, P. M., le Sage, C., Schrier, M., Gillis, A. J., Stoop, H., Nagel, R., Liu, Y. P., van Duijse, J., Drost, J., Griekspoor, A. et al. (2006) A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell, 124, 1169-1181.
37. Gothilf, Y., Coon, S. L., Toyama, R., Chitnis, A., Namboodiri, M. A. and Klein, D. C. (1999) Zebrafish serotonin N-acetyltransferase-2: marker for development of pineal photoreceptors and circadian clock function. Endocrinology, 140, 4895-4903.
38. Duffy, J. F. and Wright, K. P. Jr. (2005) Entrainment of the human circadian system by light. J. Biol. Rhythms, 20, 326-338.
39. Hirayama, J., Cardone, L., Doi, M. and Sassone-Corsi, P. (2005) Common pathways in circadian and cell cycle clocks: lightdependent activation of Fos/AP-1 in zebrafish controls CRY-1a and WEE-1. Proc. Natl Acad. Sci. USA, 102, 10194-10199.
40. Hirayama, J., Cho, S. and 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, 15747-15752.
41. Honma, S., Kawamoto, T., Takagi, Y., Fujimoto, K., Sato, F., Noshiro, M., Kato, Y. and Honma, K. (2002) Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature, 419, 841-844.
42. Teboul, M., Guillaumond, F., Grechez-Cassiau, A. and Delaunay, F. (2008) The nuclear hormone receptor family round the clock. Mol. Endocrinol., 22, 2573-2582.
43. Doi, M., Nakajima, Y., Okano, T. and Fukada, Y. (2001) Lightinduced phase-delay of the chicken pineal circadian clock is associated with the induction of cE4bp4, a potential transcriptional repressor of cPer2 gene. Proc. Natl Acad. Sci. USA, 98, 8089-8094.
44. Ohno, T., Onishi, Y. and Ishida, N. (2007) A novel E4BP4 element drives circadian expression of mPeriod2. Nucleic Acids Res., 35, 648-655.
45. Yamaguchi, S., Mitsui, S., Yan, L., Yagita, K., Miyake, S. and Okamura, H. (2000) Role of DBP in the circadian oscillatory mechanism. Mol. Cell. Biol., 20, 4773-4781.
46. Semenza, G. L. (1998) Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr. Opin. Genet. Dev., 8, 588-594.
47. Chilov, D., Hofer, T., Bauer, C., Wenger, R. H. and Gassmann, M. (2001) Hypoxia affects expression of circadian genes PER1 and CLOCK in mouse brain. FASEB J., 15, 2613-2622.
48. Ghorbel, M. T., Coulson, J. M. and Murphy, D. (2003) Cross-talk between hypoxic and circadian pathways: cooperative roles for hypoxia-inducible factor 1alpha and CLOCK in transcriptional activation of the vasopressin gene. Mol. Cell. Neurosci., 22, 396-404.
49. Egg, M., Koblitz, L., Hirayama, J., Schwerte, T., Folterbauer, C., Kurz, A., Fiechtner, B., Most, M., Salvenmoser, W., Sassone-Corsi, P. et al. (2013) Linking oxygen to time: the bidirectional interaction between the hypoxic signaling pathway and the circadian clock. Chronobiol. Int., 30, 510-529.
50. Minchenko, O., Opentanova, I., Minchenko, D., Ogura, T. and Esumi, H. (2004) Hypoxia induces transcription of 6-phosphofructo-2-kinase/fructose-2,6- biphosphatase-4 gene via hypoxia-inducible factor-1alpha activation. FEBS Lett., 576, 14-20.
51. Guillaumond, F., Dardente, H., Giguere, V. and Cermakian, N. (2005) Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J. Biol. Rhythms, 20, 391-403.
52. Cowell, I. G. (2002) E4BP4/NFIL3, a PAR-related bZIP factor with many roles. Bioessays, 24, 1023-1029.
53. Cahill, G. M., Hurd, M. W. and Batchelor, M. M. (1998) Circadian rhythmicity in the locomotor activity of larval zebrafish. Neuroreport, 9, 3445-3449.
54. Abe, T., Ishikawa, T., Masuda, T., Mizusawa, K., Tsukamoto, T., Mitani, H., Yanagisawa, T., Todo, T. and Iigo, M. (2006) Molecular analysis of Dec1 and Dec2 in the peripheral circadian clock of zebrafish photosensitive cells. Biochem. Biophys. Res. Commun., 351, 1072-1077.
55. Clokie, S. J., Lau, P., Kim, H. H., Coon, S. L. and Klein, D. C. (2012) MicroRNAs in the pineal gland: miR-483 regulates melatonin synthesis by targeting arylalkylamine n-acetyltransferase. J. Biol. Chem., 287, 25312-25324.
56. Krol, J., Busskamp, V., Markiewicz, I., Stadler, M. B., Ribi, S., Richter, J., Duebel, J., Bicker, S., Fehling, H. J., Schubeler, D. et al. (2010) Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell, 141, 618-631.
57. Ulitsky, I., Shkumatava, A., Jan, C. H., Subtelny, A. O., Koppstein, D., Bell, G. W., Sive, H. and Bartel, D. P. (2012) Extensive alternative polyadenylation during zebrafish development. Genome Res., 22, 2054-2066.
58. Klein, D. C. (2007) Arylalkylamine N-acetyltransferase: ''the Timezyme''. J. Biol. Chem., 282, 4233-4237.
59. Mehta, N. and Cheng, H. Y. (2012) Micro-managing the circadian clock: the role of microRNAs in biological timekeeping. J. Mol. Biol., 425, 3609-3624.
60. Rossner, M. J., Oster, H., Wichert, S. P., Reinecke, L., Wehr, M. C., Reinecke, J., Eichele, G., Taneja, R. and Nave, K. A. (2008) Disturbed clockwork resetting in Sharp-1 and Sharp-2 single and double mutant mice. PLoS One, 3, e2762.
61. Xu, S., Witmer, P. D., Lumayag, S., Kovacs, B. and Valle, D. (2007) MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J. Biol. Chem., 282, 25053-25066.
62. Pierce, L. X., Noche, R. R., Ponomareva, O., Chang, C. and Liang, J. O. (2008) Novel functions for Period 3 and Exorhodopsin in rhythmic transcription and melatonin biosynthesis within the zebrafish pineal organ. Brain Res., 1223, 11-24.
63. Toyama, R., Chen, X., Jhawar, N., Aamar, E., Epstein, J., Reany, N., Alon, S., Gothilf, Y., Klein, D. C. and Dawid, I. B. (2009) Transcriptome analysis of the zebrafish pineal gland. Dev Dyn., 238, 1813-1826.
64. Ziv, L., Tovin, A., Strasser, D. and Gothilf, Y. (2007) Spectral sensitivity of melatonin suppression in the zebrafish pineal gland. Exp. Eye Res., 84, 92-99.
65. Moutsaki, P., Whitmore, D., Bellingham, J., Sakamoto, K., David-Gray, Z. K. and Foster, R. G. (2003) Teleost multiple tissue (tmt) opsin: a candidate photopigment regulating the peripheral clocks of zebrafish? Brain Res. Mol. Brain Res., 112, 135-145.
66. Cavallari, N., Frigato, E., Vallone, D., Frohlich, N., Lopez-Olmeda, J. F., Foa, A., Berti, R., Sanchez-Vazquez, F. J., Bertolucci, C. and Foulkes, N. S. (2011) A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception. PLoS Biol., 9, e1001142.
67. Ceriani, M. F., Darlington, T. K., Staknis, D., Mas, P., Petti, A. A., Weitz, C. J. and Kay, S. A. (1999) Light-dependent sequestration of TIMELESS by CRYPTOCHROM E. Science, 285, 553-556.
68. Kobayashi, Y., Ishikawa, T., Hirayama, J., Daiyasu, H., Kanai, S., Toh, H., Fukuda, I., Tsujimura, T., Terada, N., Kamei, Y. et al. (2000) Molecular analysis of zebrafish photolyase/cryptochrome family: two types of cryptochromes present in zebrafish. Genes Cells, 5, 725-738.
69. Hogenesch, J. B., Gu, Y. Z., Jain, S. and Bradfield, C. A. (1998) The basic-helix-loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc. Natl Acad. Sci. USA, 95, 5474-5479.