Light and melatonin schedule neuronal differentiation in the habenular nuclei

Developmental Biology

Volumn 358, Issue 1, 2011, Pages 251-261

  de Borsetti, Nancy Hernandez ^a,b   Dean, Benjamin J ^a   Bain, Emily J ^a   Clanton, Joshua A ^a   Taylor, Robert W ^a   Gamse, Joshua T ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSIDAD NACIONAL DE JUJUY   (Argentina)

Author keywords

Circadian rhythm; Epithalamus; Neurogenesis; Neuropil; Photoperiod; Pineal organ; Zebrafish

Indexed keywords

MELATONIN; MELATONIN RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DARKNESS; EMBRYO; EMBRYO DEVELOPMENT; HABENULA; HORMONAL REGULATION; LIGHT; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROPIL; NONHUMAN; PINEAL BODY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; ZEBRA FISH;

DANIO RERIO;

EID: 80052623295     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.07.038     Document Type: Article

References (69)

1. Agetsuma M., Aizawa H., Aoki T., Nakayama R., Takahoko M., Goto M., Sassa T., Amo R., Shiraki T., Kawakami K., Hosoya T., Higashijima S., Okamoto H. The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat. Neurosci. 2010, 13:1354-1356.
2. Amano M., Iigo M., Kitamura S., Amiya N., Yamamori K. Changes in melatonin binding sites under artificial light-dark, constant light and constant dark conditions in the masu salmon brain. Comp. Biochem. Physiol. Part A. Mol. Integr. Physiol. 2006, 144:509-513.
3. Bellon A., Ortiz-Lopez L., Ramirez-Rodriguez G., Anton-Tay F., Benitez-King G. Melatonin induces neuritogenesis at early stages in N1E-115 cells through actin rearrangements via activation of protein kinase C and Rho-associated kinase. J. Pineal Res. 2007, 42:214-221.
4. Bertolucci C., Foa A. Extraocular photoreception and circadian entrainment in nonmammalian vertebrates. Chronobiol. Int. 2004, 21:501-519.
5. Bolliet V., Falcón J., Ali M.A. Regulation of melatonin secretion by light in the isolated pineal organ of the white sucker (Catostomus commersoni). J. Neuroendocrinol. 1995, 7:535-542.
6. Bourgeron T. The possible interplay of synaptic and clock genes in autism spectrum disorders. Cold Spring Harb. Symp. Quant. Biol. 2007, 72:645-654.
7. Budaev S., Andrew R.J. Patterns of early embryonic light exposure determine behavioural asymmetries in zebrafish: a habenular hypothesis. Behav. Brain Res. 2009, 200:91-94.
8. Cahill G.M. Circadian regulation of melatonin production in cultured zebrafish pineal and retina. Brain Res. 1996, 708:177-181.
9. Cheung C.Y., Webb S.E., Meng A., Miller A.L. Transient expression of apoaequorin in zebrafish embryos: extending the ability to image calcium transients during later stages of development. Int. J. Dev. Biol. 2006, 50:561-569.
10. Chong S.W., Emelyanov A., Gong Z., Korzh V. Expression pattern of two zebrafish genes, cxcr4a and cxcr4b. Mech. Dev. 2001, 109:347-354.
11. Concha M.L., Burdine R.D., Russell C., Schier A.F., Wilson S.W. A nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron 2000, 28:399-409.
12. Danilova N., Krupnik V.E., Sugden D., Zhdanova I.V. Melatonin stimulates cell proliferation in zebrafish embryo and accelerates its development. FASEB J. 2004, 18:751-753.
13. Daulat A.M., Maurice P., Froment C., Guillaume J.L., Broussard C., Monsarrat B., Delagrange P., Jockers R. Purification and identification of G protein-coupled receptor protein complexes under native conditions. Mol. Cell. Proteomics 2007, 6:835-844.
14. D'Autilia S., Broccoli V., Barsacchi G., Andreazzoli M. Xenopus Bsx links daily cell cycle rhythms and pineal photoreceptor fate. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:6352-6357.
15. Dekens M.P., Whitmore D. Autonomous onset of the circadian clock in the zebrafish embryo. EMBO J. 2008, 27:2757-2765.
16. Dekens M.P., Santoriello C., Vallone D., Grassi G., Whitmore D., Foulkes N.S. Light regulates the cell cycle in zebrafish. Curr. Biol. 2003, 13:2051-2057.
17. Dubocovich M.L. Luzindole (N-0774): a novel melatonin receptor antagonist. J. Pharmacol. Exp. Ther. 1988, 246:902-910.
18. Dufourcq P., Rastegar S., Strahle U., Blader P. Parapineal specific expression of gfi1 in the zebrafish epithalamus. Gene Expr. Patterns 2004, 4:53-57.
19. Dulcis D., Spitzer N.C. Illumination controls differentiation of dopamine neurons regulating behaviour. Nature 2008, 456:195-201.
20. Elsea S.H., Girirajan S. Smith-Magenis syndrome. Eur. J. Hum. Genet. 2008, 16:412-421.
21. Gamse J.T., Shen Y.C., Thisse C., Thisse B., Raymond P.A., Halpern M.E., Liang J.O. Otx5 regulates genes that show circadian expression in the zebrafish pineal complex. Nat. Genet. 2002, 30:117-121.
22. Gamse J.T., Thisse C., Thisse B., Halpern M.E. The parapineal mediates left-right asymmetry in the zebrafish diencephalon. Development 2003, 130:1059-1068.
23. Gamse J.T., Kuan Y.S., Macurak M., Brosamle C., Thisse B., Thisse C., Halpern M.E. Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target. Development 2005, 132:4869-4881.
24. Gothilf Y., Coon S.L., Toyama R., Chitnis A., Namboodiri M.A., Klein D.C. Zebrafish serotonin N-acetyltransferase-2: marker for development of pineal photoreceptors and circadian clock function. Endocrinology 1999, 140:4895-4903.
25. Hendricks M., Jesuthasan S. Asymmetric innervation of the habenula in zebrafish. J. Comp. Neurol. 2007, 502:611-619.
26. Hikosaka O. The habenula: from stress evasion to value-based decision-making. Nat. Rev. Neurosci. 2010, 11:503-513.
27. Hirayama J., Cho S., Sassone-Corsi P. Circadian control by the reduction/oxidation pathway: catalase represses light-dependent clock gene expression in the zebrafish. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15747-15752.
28. Hockberger P.E., Skimina T.A., Centonze V.E., Lavin C., Chu S., Dadras S., Reddy J.K., White J.G. Activation of flavin-containing oxidases underlies light-induced production of H2O2 in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:6255-6260.
29. Jockers R., Maurice P., Boutin J.A., Delagrange P. Melatonin receptors, heterodimerization, signal transduction and binding sites: what's new?. Br. J. Pharmacol. 2008, 154:1182-1195.
30. Kaneko M., Hernandez-Borsetti N., Cahill G.M. Diversity of zebrafish peripheral oscillators revealed by luciferase reporting. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:14614-14619.
31. Kazimi N., Cahill G.M. Development of a circadian melatonin rhythm in embryonic zebrafish. Brain Res. Dev. Brain Res. 1999, 117:47-52.
32. Kemali M., Guglielmotti V., Fiorino L. The asymmetry of the habenular nuclei of female and male frogs in spring and in winter. Brain Res. 1990, 517:251-255.
33. Kim C.H., Ueshima E., Muraoka O., Tanaka H., Yeo S.Y., Huh T.L., Miki N. Zebrafish elav/HuC homologue as a very early neuronal marker. Neurosci. Lett. 1996, 216:109-112.
34. Klein D.C. Evidence for the placental transfer of 3 H-acetyl-melatonin. Nat. New Biol. 1972, 237:117-118.
35. Kong X., Li X., Cai Z., Yang N., Liu Y., Shu J., Pan L., Zuo P. Melatonin regulates the viability and differentiation of rat midbrain neural stem cells. Cell. Mol. Neurobiol. 2008, 28:569-579.
36. Korf H.W., Oksche A., Ekstrom P., Gery I., Zigler J.S., Klein D.C. Pinealocyte projections into the mammalian brain revealed with S-antigen antiserum. Science 1986, 231:735-737.
37. Kuan Y.S., Gamse J.T., Schreiber A.M., Halpern M.E. Selective asymmetry in a conserved forebrain to midbrain projection. J. Exp. Zool. B Mol. Dev. Evol. 2007, 308:669-678.
38. Kuan Y.S., Yu H.H., Moens C.B., Halpern M.E. Neuropilin asymmetry mediates a left-right difference in habenular connectivity. Development 2007, 134:857-865.
39. Kulman G., Lissoni P., Rovelli F., Roselli M.G., Brivio F., Sequeri P. Evidence of pineal endocrine hypofunction in autistic children. Neuro Endocrinol. Lett. 2000, 21:31-34.
40. Lee A., Mathuru A.S., Teh C., Kibat C., Korzh V., Penney T.B., Jesuthasan S. The habenula prevents helpless behavior in larval zebrafish. Curr. Biol. 2010, 20:2211-2216.
41. Melke J., Goubran Botros H., Chaste P., Betancur C., Nygren G., Anckarsater H., Rastam M., Stahlberg O., Gillberg I.C., Delorme R., Chabane N., Mouren-Simeoni M.C., Fauchereau F., Durand C.M., Chevalier F., Drouot X., Collet C., Launay J.M., Leboyer M., Gillberg C., Bourgeron T. Abnormal melatonin synthesis in autism spectrum disorders. Mol. Psychiatry 2008, 13:90-98.
42. Moriya T., Horie N., Mitome M., Shinohara K. Melatonin influences the proliferative and differentiative activity of neural stem cells. J. Pineal Res. 2007, 42:411-418.
43. Moutsaki P., Whitmore D., Bellingham J., Sakamoto K., David-Gray Z.K., Foster R.G. Teleost multiple tissue (tmt) opsin: a candidate photopigment regulating the peripheral clocks of zebrafish?. Brain Res. Mol. Brain Res. 2003, 112:135-145.
44. Nir I. Biorhythms and the biological clock involvement of melatonin and the pineal gland in life and disease. Biomed. Environ. Sci. 1995, 8:90-105.
45. Oliveira C., Ortega A., Lopez-Olmeda J.F., Vera L.M., Sánchez-Vázquez F.J. Influence of constant light and darkness, light intensity, and light spectrum on plasma melatonin rhythms in senegal sole. Chronobiol. Int. 2007, 24:615-627.
46. Pandi-Perumal S.R., Trakht I., Srinivasan V., Spence D.W., Maestroni G.J., Zisapel N., Cardinali D.P. Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways. Prog. Neurobiol. 2008, 85:335-353.
47. Parrish J.Z., Emoto K., Kim M.D., Jan Y.N. Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu. Rev. Neurosci. 2007, 30:399-423.
48. Reppert S.M., Klein D.C. Transport of maternal[3H]melatonin to suckling rats and the fate of [3H]melatonin in the neonatal rat. Endocrinology 1978, 102:582-588.
49. Rivkees S.A., Reppert S.M. Appearance of melatonin receptors during embryonic life in Siberian hamsters (Phodopus sungorous). Brain Res. 1991, 568:345-349.
50. Roussigne M., Bianco I.H., Wilson S.W., Blader P. Nodal signalling imposes left-right asymmetry upon neurogenesis in the habenular nuclei. Development 2009, 136:1549-1557.
51. Seron-Ferre M., Valenzuela G.J., Torres-Farfan C. Circadian clocks during embryonic and fetal development. Birth Defects Res. C Embryo Today 2007, 81:204-214.
52. Snelson C.D., Santhakumar K., Halpern M.E., Gamse J.T. Tbx2b is required for the development of the parapineal organ. Development 2008, 135:1693-1702.
53. Sutherland R.J. The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci. Biobehav. Rev. 1982, 6:1-13.
54. Tamai T.K., Vardhanabhuti V., Foulkes N.S., Whitmore D. Early embryonic light detection improves survival. Curr. Biol. 2004, 14:R104-R105.
55. Tamai T.K., Carr A.J., Whitmore D. Zebrafish circadian clocks: cells that see light. Biochem. Soc. Trans. 2005, 33:962-966.
56. Tamai T.K., Young L.C., Whitmore D. Light signaling to the zebrafish circadian clock by Cryptochrome 1a. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:14712-14717.
57. Thisse B., Thisse C. Fast Release Clones: A High Throughput Expression Analysis 2004.
58. Tordjman S., Anderson G.M., Pichard N., Charbuy H., Touitou Y. Nocturnal excretion of 6-sulphatoxymelatonin in children and adolescents with autistic disorder. Biol. Psychiatry 2005, 57:134-138.
59. Toyama R., Chen X., Jhawar N., Aamar E., Epstein J., Reany N., Alon S., Gothilf Y., Klein D.C., Dawid I.B. Transcriptome analysis of the zebrafish pineal gland. Dev. Dyn. 2009, 238:1813-1826.
60. Vallone D., Lahiri K., Dickmeis T., Foulkes N.S. Start the clock! Circadian rhythms and development. Dev. Dyn. 2007, 236:142-155.
61. 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.
62. Vuilleumier R., Besseau L., Boeuf G., Piparelli A., Gothilf Y., Gehring W.G., Klein D.C., Falcon J. Starting the zebrafish pineal circadian clock with a single photic transition. Endocrinology 2006, 147:2273-2279.
63. Walker C. Haploid screens and gamma-ray mutagenesis. Methods in Cell Biology 1999, 43-70. Elsevier, London.
64. Weaver D.R., Rivkees S.A., Reppert S.M. Localization and characterization of melatonin receptors in rodent brain by in vitro autoradiography. J. Neurosci. 1989, 9:2581-2590.
65. 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.
66. 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.
67. Witt-Enderby P.A., MacKenzie R.S., McKeon R.M., Carroll E.A., Bordt S.L., Melan M.A. Melatonin induction of filamentous structures in non-neuronal cells that is dependent on expression of the human mt1 melatonin receptor. Cell Motil. Cytoskeleton 2000, 46:28-42.
68. Zilberman-Peled B., Appelbaum L., Vallone D., Foulkes N.S., Anava S., Anzulovich A., Coon S.L., Klein D.C., Falcon J., Ron B., Gothilf Y. Transcriptional regulation of arylalkylamine-N-acetyltransferase-2 gene in the pineal gland of the gilthead seabream. J. Neuroendocrinol. 2007, 19:46-53.
69. 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.