Real-time in vivo monitoring of circadian E-box enhancer activity: A robust and sensitive zebrafish reporter line for developmental, chemical and neural biology of the circadian clock

Developmental Biology

Volumn 380, Issue 2, 2013, Pages 259-273

  Weger, Meltem ^a   Weger, Benjamin D ^a   Diotel, Nicolas ^a   Rastegar, Sepand ^a   Hirota, Tsuyoshi ^b   Kay, Steve A ^b,c   Strähle, Uwe ^a   Dickmeis, Thomas ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Adult brain; Circadian clock; E box; Luciferase reporter; Neurogenesis; Zebrafish

Indexed keywords

LITHIUM CHLORIDE; LUCIFERASE; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CHEMISTRY; CIRCADIAN RHYTHM; CONTROLLED STUDY; CYTOLOGY; DEVELOPMENTAL STAGE; DRUG IDENTIFICATION; DRUG SCREENING; E BOX GENE; EMBRYO; ENHANCER REGION; ENZYME ACTIVITY; FEEDBACK SYSTEM; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE MAPPING; GENE TARGETING; GENETIC LINE; IN VIVO STUDY; LIGHT DARK CYCLE; MATURATION; MOLECULAR MECHANICS; NERVE CELL; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; REPORTER GENE; ZEBRA FISH;

DANIO RERIO; VERTEBRATA;

EID: 84879882231     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.04.035     Document Type: Article

References (87)

1. Adolf B., Chapouton P., Lam C.S., Topp S., Tannhauser B., Strahle U., Gotz M., Bally-Cuif L. Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev. Biol. 2006, 295:278-293.
2. Albrecht U. Timing to perfection: the biology of central and peripheral circadian clocks. Neuron 2012, 74:246-260.
3. Amaral I.P., Johnston I.A. Circadian expression of clock and putative clock-controlled genes in skeletal muscle of the zebrafish. Am. J. Physiol. Endocrinol. Metab. 2012, 302:R193-206.
4. Andrews R.V. Circadian rhythms in adrenal organ cultures. Gegenbaurs Morphol. Jahrb. 1971, 117:89-98.
5. Appelbaum L., Anzulovich A., Baler R., Gothilf Y. Homeobox-clock protein interaction in zebrafish. A shared mechanism for pineal-specific and circadian gene expression. J. Biol. Chem. 2005, 280:11544-11551.
6. Balsalobre A., Damiola F., Schibler U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 1998, 93:929-937.
7. Bass J., Takahashi J.S. Circadian integration of metabolism and energetics. Science 2010, 330:1349-1354.
8. Becker C.G., Meyer R.L., Becker T. Gradients of ephrin-A2 and ephrin-A5b mRNA during retinotopic regeneration of the optic projection in adult zebrafish. J. Comp. Neurol. 2000, 427:469-483.
9. Ben-Moshe Z., Vatine G., Alon S., Tovin A., Mracek P., Foulkes N.S., Gothilf Y. Multiple PAR and E4BP4 bZIP transcription factors in zebrafish: diverse spatial and temporal expression patterns. Chronobiol. Int. 2010, 27:1509-1531.
10. Borgs L., Beukelaers P., Vandenbosch R., Nguyen L., Moonen G., Maquet P., Albrecht U., Belachew S., Malgrange B. Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci. 2009, 10:30.
11. Brown S.A., Kowalska E., Dallmann R. (Re)inventing the circadian feedback loop. Dev. Cell 2012, 22:477-487.
12. Burns C.G., Milan D.J., Grande E.J., Rottbauer W., MacRae C.A., Fishman M.C. High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nat. Chem. Biol. 2005, 1:263-264.
13. Burrill J.D., Easter SS Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio). J. Comp. Neurol. 1994, 346:583-600.
14. Cahill G.M. Clock mechanisms in zebrafish. Cell Tissue Res. 2002, 309:27-34.
15. Cavallari N., Frigato E., Vallone D., Frohlich N., Lopez-Olmeda J.F., Foa A., Berti R., Sanchez-Vazquez F.J., Bertolucci C., Foulkes N.S. A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception. PLoS Biol. 2011, 9:e1001142.
16. Cermakian N., Whitmore D., Foulkes N.S., Sassone-Corsi P. Asynchronous oscillations of two zebrafish CLOCK partners reveal differential clock control and function. Proc. Nat. Acad. Sci. U.S.A. 2000, 97:4339-4344.
17. Chapouton P., Webb K.J., Stigloher C., Alunni A., Adolf B., Hesl B., Topp S., Kremmer E., Bally-Cuif L. Expression of hairy/enhancer of split genes in neural progenitors and neurogenesis domains of the adult zebrafish brain. J. Comp. Neurol. 2011, 519:1748-1769.
18. Chen Z., Yoo S.H., Park Y.S., Kim K.H., Wei S., Buhr E., Ye Z.Y., Pan H.L., Takahashi J.S. Identification of diverse modulators of central and peripheral circadian clocks by high-throughput chemical screening. Proc. Nat. Acad. Sci. U.S.A. 2012, 109:101-106.
19. d'Alencon C.A., Pena O.A., Wittmann C., Gallardo V.E., Jones R.A., Loosli F., Liebel U., Grabher C., Allende M.L. A high-throughput chemically induced inflammation assay in zebrafish. BMC Biol. 2010, 8:151.
20. Dekens M.P., Whitmore D. Autonomous onset of the circadian clock in the zebrafish embryo. EMBO J. 2008, 27:2757-2765.
21. Dibner C., Schibler U., Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 2010, 72:517-549.
22. Dickmeis T., Foulkes N.S. Glucocorticoids and circadian clock control of cell proliferation: at the interface between three dynamic systems. Mol. Cell. Endocrinol. 2011, 331:11-22.
23. Dickmeis T., Lahiri K., Nica G., Vallone D., Santoriello C., Neumann C.J., Hammerschmidt M., Foulkes N.S. Glucocorticoids play a key role in circadian cell cycle rhythms. PLoS Biol. 2007, 5:e78.
24. Dunlap J., Loros J., DeCoursey P. Chronobiology 2004, Sinauer Associates, Sunderland.
25. Falcon J., Migaud H., Munoz-Cueto J.A., Carrillo M. Current knowledge on the melatonin system in teleost fish. Gen. Comp. Endocrinol. 2010, 165:469-482.
26. Feng D., Lazar M.A. Clocks, metabolism, and the epigenome. Mol. Cell. 2012, 47:158-167.
27. Gachon F., Olela F.F., Schaad O., Descombes P., Schibler U. The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab. 2006, 4:25-36.
28. Grandel H., Kaslin J., Ganz J., Wenzel I., Brand M. Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev. Biol. 2006, 295:263-277.
29. Guilding C., Hughes A.T., Piggins H.D. Circadian oscillators in the epithalamus. Neuroscience 2010, 169:1630-1639.
30. Guilding C., Piggins H.D. Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain?. Eur. J. Neurosci. 2007, 25:3195-3216.
31. Hirota T., Lee J.W., Lewis W.G., Zhang E.E., Breton G., Liu X., Garcia M., Peters E.C., Etchegaray J.P., Traver D., Schultz P.G., Kay S.A. High-throughput chemical screen identifies a novel potent modulator of cellular circadian rhythms and reveals CKIalpha as a clock regulatory kinase. PLoS Biol. 2010, 8:e1000559.
32. Hirota T., Lee J.W., John P.C., Sawa M., Iwaisako K., Noguchi T., Pongsawakul P.Y., Sonntag T., Welsh D.K., Brenner D.A., Doyle F.J., Schultz P.G., Kay S.A. Identification of small molecule activators of Cryptochrome. Science 2012.
33. Hirota T., Lewis W.G., Liu A.C., Lee J.W., Schultz P.G., Kay S.A. A chemical biology approach reveals period shortening of the mammalian circadian clock by specific inhibition of GSK-3beta. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:20746-20751.
34. Inoue D., Wittbrodt J. One for all--a highly efficient and versatile method for fluorescent immunostaining in fish embryos. PLoS One 2011, 6:e19713.
35. Ishikawa T., Hirayama J., Kobayashi Y., Todo T. Zebrafish CRY represses transcription mediated by CLOCK-BMAL heterodimer without inhibiting its binding to DNA. Genes Cells 2002, 7:1073-1086.
36. Isojima Y., Nakajima M., Ukai H., Fujishima H., Yamada R.G., Masumoto K.H., Kiuchi R., Ishida M., Ukai-Tadenuma M., Minami Y., Kito R., Nakao K., Kishimoto W., Yoo S.H., Shimomura K., Takao T., Takano A., Kojima T., Nagai K., Sakaki Y., Takahashi J.S., Ueda H.R. CKIepsilon/delta-dependent phosphorylation is a temperature-insensitive, period-determining process in the mammalian circadian clock. Proc. Nat. Acad. Sci. U.S.A. 2009, 106:15744-15749.
37. Kakizawa T., Nishio S., Triqueneaux G., Bertrand S., Rambaud J., Laudet V. Two differentially active alternative promoters control the expression of the zebrafish orphan nuclear receptor gene Rev-erbalpha. J. Mol. Endocrinol. 2007, 38:555-568.
38. Kaneko M., Cahill G.M. Light-dependent development of circadian gene expression in transgenic zebrafish. PLoS Biol. 2005, 3:e34.
39. Kaneko M., Hernandez-Borsetti N., Cahill G.M. Diversity of zebrafish peripheral oscillators revealed by luciferase reporting. Proc. Nat. Acad. Sci. U.S.A. 2006, 103:14614-14619.
40. Kikuchi K., Poss K.D. Cardiac regenerative capacity and mechanisms. Annu. Rev. Cell Dev. Biol. 2012, 28:719-741.
41. Kizil C., Kaslin J., Kroehne V., Brand M. Adult neurogenesis and brain regeneration in zebrafish. Dev. Neurobiol. 2006, 72:429-461.
42. Kobayashi Y., Ishikawa T., Hirayama J., Daiyasu H., Kanai S., Toh H., Fukuda I., Tsujimura T., Terada N., Kamei Y., Yuba S., Iwai S., Todo T. Molecular analysis of zebrafish photolyase/cryptochrome family: two types of cryptochromes present in zebrafish. Genes Cells 2000, 5:725-738.
43. Kowalska E., Moriggi E., Bauer C., Dibner C., Brown S.A. The circadian clock starts ticking at a developmentally early stage. J. Biol. Rhythms 2010, 25:442-449.
44. Lahiri K., Vallone D., Gondi S.B., Santoriello C., Dickmeis T., Foulkes N.S. Temperature regulates transcription in the zebrafish circadian clock. PLoS Biol. 2005, 3:e351.
45. Lam C.S., Marz M., Strahle U. gfap and nestin reporter lines reveal characteristics of neural progenitors in the adult zebrafish brain. Dev. Dyn. 2009, 238:475-486.
46. Lessman C.A. The developing zebrafish (Danio rerio): a vertebrate model for high-throughput screening of chemical libraries. Birth Defects Res. C: Embryo Today 2011, 93:268-280.
47. Levi F., Okyar A., Dulong S., Innominato P.F., Clairambault J. Circadian timing in cancer treatments. Annu. Rev. Pharmacol. Toxicol. 2010, 50:377-421.
48. Li J., Lu W.Q., Beesley S., Loudon A.S., Meng Q.J. Lithium impacts on the amplitude and period of the molecular circadian clockwork. PLoS One 2012, 7:e33292.
49. Marz M., Chapouton P., Diotel N., Vaillant C., Hesl B., Takamiya M., Lam C.S., Kah O., Bally-Cuif L., Strahle U. Heterogeneity in progenitor cell subtypes in the ventricular zone of the zebrafish adult telencephalon. Glia 2010, 58:870-888.
50. Mehra A., Baker C.L., Loros J.J., Dunlap J.C. Post-translational modifications in circadian rhythms. Trends Biochem. Sci. 2009, 34:483-490.
51. Menaker M., Moreira L.F., Tosini G. Evolution of circadian organization in vertebrates. Braz. J. Med. Biol. Res. 1997, 30:305-313.
52. Mistlberger R.E. Neurobiology of food anticipatory circadian rhythms. Physiol. Behav. 2011, 104:535-545.
53. Mohawk J.A., Green C.B., Takahashi J.S. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 2012, 35:445-462.
54. Nüsslein-Volhard C. Zebrafish, A Practical Approach 2002, Oxford University Press, Oxford.
55. Pando M.P., Pinchak A.B., Cermakian N., Sassone-Corsi P. A cell-based system that recapitulates the dynamic light-dependent regulation of the vertebrate clock. Proc. Nat. Acad. Sci. U.S.A. 2001, 98:10178-10183.
56. Peal D.S., Peterson R.T., Milan D. Small molecule screening in zebrafish. J. Cardiovasc. Transl. Res. 2010, 3:454-460.
57. Pellegrini E., Mouriec K., Anglade I., Menuet A., Le Page Y., Gueguen M.M., Marmignon M.H., Brion F., Pakdel F., Kah O. Identification of aromatase-positive radial glial cells as progenitor cells in the ventricular layer of the forebrain in zebrafish. J. Comp. Neurol. 2007, 501:150-167.
58. Pendergast J.S., Oda G.A., Niswender K.D., Yamazaki S. Period determination in the food-entrainable and methamphetamine-sensitive circadian oscillator(s). Proc. Nat. Acad. Sci.U.S.A. 2012, 109:14218-14223.
59. Prasai M.J., Pernicova I., Grant P.J., Scott E.M. An endocrinologist's guide to the clock. J. Clin. Endocrinol. Metab. 2011, 96:913-922.
60. Pronk A., Ji B.T., Shu X.O., Xue S., Yang G., Li H.L., Rothman N., Gao Y.T., Zheng W., Chow W.H. Night-shift work and breast cancer risk in a cohort of Chinese women. Am. J. Epidemiol. 2010, 171:953-959.
61. Reischl S., Kramer A. Kinases and phosphatases in the mammalian circadian clock. FEBS Lett. 2011, 585:1393-1399.
62. Rihel J., Prober D.A., Arvanites A., Lam K., Zimmerman S., Jang S., Haggarty S.J., Kokel D., Rubin L.L., Peterson R.T., Schier A.F. Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 2010, 327:348-351.
63. Rinkwitz, S., Mourrain, P., Becker, T.S., 2010. Zebrafish: an integrative System for neurogenomics and neurosciences. Prog. Neurobiol. 93, 231-243.
64. Saini C., Suter D.M., Liani A., Gos P., Schibler U. The mammalian circadian timing system: synchronization of peripheral clocks. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:39-47.
65. Scheer F.A., Hilton M.F., Mantzoros C.S., Shea S.A. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc. Nat. Acad. Sci. U.S.A. 2009, 106:4453-4458.
66. Segall L.A., Amir S. Glucocorticoid regulation of clock gene expression in the mammalian limbic forebrain. J. Mol. Neurosci. 2010, 42:168-175.
67. Sehgal A., Mignot E. Genetics of sleep and sleep disorders. Cell 2011, 146:194-207.
68. Seron-Ferre M., Mendez N., Abarzua-Catalan L., Vilches N., Valenzuela F.J., Reynolds H.E., Llanos A.J., Rojas A., Valenzuela G.J., Torres-Farfan C. Circadian rhythms in the fetus. Mol. Cell. Endocrinol. 2012, 349:68-75.
69. Son G.H., Chung S., Choe H.K., Kim H.D., Baik S.M., Lee H., Lee H.W., Choi S., Sun W., Kim H., Cho S., Lee K.H., Kim K. Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc. Nat. Acad.Sci. U.S.A. 2008, 105:20970-20975.
70. Takahashi J.S., Hong H.K., Ko C.H., McDearmon E.L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 2008, 9:764-775.
71. Tran T.C., Sneed B., Haider J., Blavo D., White A., Aiyejorun T., Baranowski T.C., Rubinstein A.L., Doan T.N., Dingledine R., Sandberg E.M. Automated, quantitative screening assay for antiangiogenic compounds using transgenic zebrafish. Cancer Res. 2007, 67:11386-11392.
72. Vallone D., Gondi S.B., Whitmore D., Foulkes N.S. E-box function in a period gene repressed by light. Proc. Nat. Acad. Sci. U.S.A. 2004, 101:4106-4111.
73. Vallone D., Lahiri K., Dickmeis T., Foulkes N.S. Start the clock! Circadian rhythms and development. Dev. Dyn. 2007, 236:142-155.
74. Vatine G., Vallone D., Appelbaum L., Mracek P., Ben-Moshe Z., Lahiri K., Gothilf Y., Foulkes N.S. Light directs zebrafish period2 expression via conserved D and E boxes. PLoS Biol. 2009, 7:e1000223.
75. Vatine G., Vallone D., Gothilf Y., Foulkes N.S. It's time to swim! Zebrafish and the circadian clock. FEBS Lett. 2012, 585:1485-1494.
76. Weger B.D., Sahinbas M., Otto G.W., Mracek P., Armant O., Dolle D., Lahiri K., Vallone D., Ettwiller L., Geisler R., Foulkes N.S., Dickmeis T. The light responsive transcriptome of the zebrafish: function and regulation. PLoS One 2011, 6:e17080.
77. Weger B.D., Weger M., Nusser M., Brenner-Weiss G., Dickmeis T. A chemical screening system for glucocorticoid stress hormone signaling in an intact vertebrate. Chem. Biol. 2012, 7:1178-1183.
78. Westerfield M. The zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio) 2007, University of Oregon Press, Eugene. fifth ed.
79. Whitmore D., Foulkes N.S., Sassone-Corsi P. Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 2000, 404:87-91.
80. Whitmore D., Foulkes N.S., Strahle U., Sassone-Corsi P. Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators. Nat. Neurosci. 1998, 1:701-707.
81. Wulff K., Gatti S., Wettstein J.G., Foster R.G. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat. Rev. Neurosci. 2010, 11:589-599.
82. Wullimann M.F., Rupp B., Reichert H. Neuroanatomy of the Zebrafish Brain-A Topological Atlas 1996, Birkhäuser, Basel, Boston, Berlin.
83. Yagita K., Horie K., Koinuma S., Nakamura W., Yamanaka I., Urasaki A., Shigeyoshi Y., Kawakami K., Shimada S., Takeda J., Uchiyama Y. Development of the circadian oscillator during differentiation of mouse embryonic stem cells in vitro. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:3846-3851.
84. Yoo S.H., Yamazaki S., Lowrey P.L., Shimomura K., Ko C.H., Buhr E.D., Siepka S.M., Hong H.K., Oh W.J., Yoo O.J., Menaker M., Takahashi J.S. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Nat. Acad. Sci. U.S.A. 2004, 101:5339-5346.
85. Zhang E.E., Kay S.A. Clocks not winding down: unravelling circadian networks. Nat. Rev. Mol. Cell Biol. 2010, 11:764-776.
86. Ziv L., Gothilf Y. Circadian time-keeping during early stages of development. Proc. Nat. Acad. Sci. U.S.A. 2006, 103:4146-4151.
87. Ziv L., Levkovitz S., Toyama R., Falcon J., Gothilf Y. Functional development of the zebrafish pineal gland: light-induced expression of period2 is required for onset of the circadian clock. J. Neuroendocrinol. 2005, 17:314-320.