Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017, Article ID 8459385, 14 pages
https://doi.org/10.1155/2017/8459385
Research Article

Dexamethasone Modulates Nonvisual Opsins, Glucocorticoid Receptor, and Clock Genes in Danio rerio ZEM-2S Cells

Department of Physiology, Institute of Biosciences, University of Sao Paulo, Sao Paulo, SP, Brazil

Correspondence should be addressed to Ana Maria de Lauro Castrucci; rb.psu.bi@tsacldma

Received 10 October 2016; Revised 19 March 2017; Accepted 22 March 2017; Published 14 May 2017

Academic Editor: Giuseppe Piccione

Copyright © 2017 Jennifer Caroline Sousa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. Halberg, “Chronobiology.,” Annual Review of Physiology, vol. 31, pp. 675–725, 1969. View at Publisher · View at Google Scholar · View at Scopus
  2. M. H. Vitaterna, D. P. King, A.-M. Chang et al., “Mutagenesis and mapping of a mouse gene, clock, essential for circadian behavior,” Science, vol. 264, no. 5159, pp. 719–725, 1994. View at Publisher · View at Google Scholar · View at Scopus
  3. H. Tei, H. Okamura, Y. Shigeyoshi et al., “Circadian oscillation of a mammalian homologue of the Drosophila period gene,” Nature, vol. 389, no. 6650, pp. 512–516, 1997. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Takumi, C. Matsubara, Y. Shigeyoshi et al., “A new mammalian period gene predominantly expressed in the suprachiasmatic nucleus,” Genes to Cells, vol. 3, no. 3, pp. 167–176, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Takumi, K. Taguchi, S. Miyake et al., “A light-independent oscillatory gene mPer3 in mouse SCN and OVLT,” The EMBO Journal, vol. 17, no. 16, pp. 4753–4759, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Gekakis, D. Staknis, H. B. Nguyen et al., “Role of the CLOCK protein in the mammalian circadian mechanism,” Science, vol. 280, no. 5369, pp. 1564–1569, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. G. T. J. Van Der Horst, M. Muijtjens, K. Kobayashi et al., “Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms,” Nature, vol. 398, no. 6728, pp. 627–630, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Yamazaki, R. Numano, M. Abe et al., “Resetting central and peripheral circadian oscillators in transgenic rats,” Science, vol. 288, no. 5466, pp. 682–685, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. U. Albrecht and G. Eichele, “The mammalian circadian clock,” Current Opinion in Genetics & Development, vol. 13, no. 3, pp. 271–277, 2003. View at Google Scholar
  10. L. H. R. G. Lima, A. C. Scarparo, M. C. Isoldi, M. A. Visconti, and A. M. L. Castrucci, “Melanopsin in chicken melanocytes and retina,” Biological Rhythm Research, vol. 37, no. 5, pp. 393–404, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. F. P. Farhat, C. B. Martins, L. H. Ribeiro Graciani De Lima, M. C. Isoldi, and A. M. D. L. Castrucci, “Melanopsin and clock genes: regulation by light and endothelin in the zebrafish ZEM-2S cell line,” Chronobiology International, vol. 26, no. 6, pp. 1090–1119, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. L. H. R. G. De Lima, K. P. Dos Santos, and A. M. De Lauro Castrucci, “Clock genes, melanopsins, melatonin, and dopamine key enzymes and their modulation by light and glutamate in chicken embryonic retinal cells,” Chronobiology International, vol. 28, no. 2, pp. 89–100, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. M. N. D. C. M. Moraes, L. R. D. Santos, N. Mezzalira, M. O. Poletini, and A. M. D. L. Castrucci, “Regulation of melanopsins and per1 by α -MSH and melatonin in photosensitive xenopus laevis melanophores,” BioMed Research International, vol. 2014, Article ID 654710, pp. 1–10, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. B. C. R. Ramos, M. N. C. M. Moraes, M. O. Poletini, L. H. R. G. Lima, and A. M. L. Castrucci, “From blue light to clock genes in zebrafish ZEM-2S cells,” PLoS ONE, vol. 9, no. 9, Article ID e106252, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. M. N. D. C. M. Moraes, L. H. R. G. D. Lima, B. C. R. Ramos, M. D. O. Poletini, and A. M. D. L. Castrucci, “Endothelin modulates the circadian expression of non-visual opsins,” General and Comparative Endocrinology, vol. 205, pp. 279–286, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. M. N. Moraes, B. C. Ramos, M. O. Poletini, and A. M. L. Castrucci, “Melanopsins: localization and Phototransduction in Xenopus laevis Melanophores,” Photochemistry and Photobiology, vol. 91, no. 5, pp. 1133–1141, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. M. O. Poletini, B. C. Ramos, M. N. Moraes, and A. M. L. Castrucci, “Nonvisual opsins and the regulation of peripheral clocks by light and hormones,” Photochemistry and Photobiology, vol. 91, no. 5, pp. 1046–1055, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. G. M. Cahill, “Clock mechanisms in zebrafish,” Cell and Tissue Research, vol. 309, no. 1, pp. 27–34, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Vatine, D. Vallone, Y. Gothilf, and N. S. Foulkes, “It's time to swim! Zebrafish and the circadian clock,” FEBS Letters, vol. 585, no. 10, pp. 1485–1494, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Whitmore, N. S. Foulkes, and P. Sassone-Corsi, “Light acts directly on organs and cells in culture to set the vertebrate circadian clock,” Nature, vol. 404, no. 6773, pp. 87–91, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. I. Provencio, G. Jiang, W. J. De Grip, W. Pär Hayes, and M. D. Rollag, “Melanopsin: an opsin in melanophores, brain, and eye,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 1, pp. 340–345, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. I. Provencio, I. R. Rodriguez, G. Jiang, W. P. Hayes, E. F. Moreira, and M. D. Rollag, “A novel human opsin in the inner retina,” Journal of Neuroscience, vol. 20, no. 2, pp. 600–605, 2000. View at Google Scholar
  23. I. Provencio, M. D. Rollag, and A. M. L. Castrucci, “Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from nigh,” Nature, vol. 415, no. 6871, article 493, 2002. View at Google Scholar
  24. J. Bellingham, D. Whitmore, A. R. Philp, D. J. Wells, and R. G. Foster, “Zebrafish melanopsin: isolation, tissue localisation and phylogenetic position,” Molecular Brain Research, vol. 107, no. 2, pp. 128–136, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Bellingham, S. S. Chaurasia, Z. Melyan et al., “Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates,” PLoS Biology, vol. 4, no. 8, article no. e254, pp. 1334–1343, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. M. J. Bailey and V. M. Cassone, “Melanopsin expression in the chick retina and pineal gland,” Molecular Brain Research, vol. 134, no. 2, pp. 345–348, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Frigato, D. Vallone, C. Bertolucci, and N. S. Foulkes, “Isolation and characterization of melanopsin and pinopsin expression within photoreceptive sites of reptiles,” Naturwissenschaften, vol. 93, no. 8, pp. 379–385, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Cavallari, E. Frigato, D. Vallone et al., “A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception,” PLoS Biology, vol. 9, no. 9, Article ID e1001142, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. W. I. L. Davies, L. Zheng, S. Hughes et al., “Functional diversity of melanopsins and their global expression in the teleost retina,” Cellular and Molecular Life Sciences, vol. 68, no. 24, pp. 4115–4132, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Alsop and M. Vijayan, “The zebrafish stress axis: molecular fallout from the teleost-specific genome duplication event,” General and Comparative Endocrinology, vol. 161, no. 1, pp. 62–66, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. D. M. Berson, F. A. Dunn, and M. Takao, “Phototransduction by retinal ganglion cells that set the circadian clock,” Science, vol. 295, no. 5557, pp. 1070–1073, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Hattar, H.-W. Liao, M. Takao, D. M. Berson, and K.-W. Yau, “Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity,” Science, vol. 295, no. 5557, pp. 1065–1070, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Whitmore, N. S. Foulkes, U. Strähle, and P. Sassone-Corsi, “Zebrafish Clock rhythmic expression reveals independent peripheral circadian oscillators,” Nature Neuroscience, vol. 1, no. 8, pp. 701–707, 1998. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Cermakian, M. P. Pando, C. L. Thompson et al., “Light induction of a vertebrate clock gene involves signaling through blue-light receptors and MAP kinases,” Current Biology, vol. 12, no. 10, pp. 844–848, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. A.-J. F. Carr and D. Whitmore, “Imaging of single light-responsive clock cells reveals fluctuating free-running periods,” Nature Cell Biology, vol. 7, no. 3, pp. 319–321, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Ye, C. P. Selby, Y. Y. Chiou, I. Ozkan-Dagliyan, S. Gaddameedhi, and A. Sancar, “Dual modes of CLOCK:BMAL1 inhibition mediated by Cryptochrome and Period proteins in the mammalian circadian clock,” Genes & Development, vol. 28, no. 18, pp. 1989–1998, 2014. View at Google Scholar
  37. Y. Kobayashi, T. Ishikawa, J. Hirayama et al., “Molecular analysis of zebrafish photolyase/cryptochrome family: two types of cryptochromes present in zebrafish,” Genes to Cells, vol. 5, no. 9, pp. 725–738, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Wang, “Comparative analysis of period genes in teleost fish genomes,” Journal of Molecular Evolution, vol. 67, no. 1, pp. 29–40, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. M. P. Pando, A. B. Pinchak, N. Cermakian, and P. Sassone-Corsi, “A cell-based system that recapitulates the dynamic light-dependent regulation of the vertebrate clock,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 18, pp. 10178–10183, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Ziv and Y. Gothilf, “Circadian time-keeping during early stages of development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 11, pp. 4146–4151, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Gavriouchkina, S. Fischer, T. Ivacevic, J. Stolte, V. Benes, and M. P. S. Dekens, “Thyrotroph embryonic factor regulates light-induced transcription of repair genes in zebrafish embryonic cells,” PLoS ONE, vol. 5, no. 9, Article ID e12542, pp. 1–10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Dickmeis, B. D. Weger, and M. Weger, “The circadian clock and glucocorticoids—interactions across many time scales,” Molecular and Cellular Endocrinology, vol. 380, no. 1-2, pp. 2–15, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. K. L. Gamble, R. Berry, S. J. Frank, and M. E. Young, “Circadian clock control of endocrine factors,” Nature Reviews Endocrinology, vol. 10, no. 8, pp. 466–475, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. A. H. Tsang, J. L. Barclay, and H. Oster, “Interactions between endocrine and circadian systems,” Journal of Molecular Endocrinology, vol. 52, no. 1, pp. R1–R16, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Balsalobre, L. Marcacci, and U. Schibler, “Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts,” Current Biology, vol. 10, no. 20, pp. 1291–1294, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Yamamoto, Y. Nakahata, M. Tanaka et al., “Acute physical stress elevates mouse Period1 mRNA expression in mouse peripheral tissues via a glucocorticoid-responsive element,” Journal of Biological Chemistry, vol. 280, no. 51, pp. 42036–42043, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Y.-L. So, T. U. Bernal, M. L. Pillsbury, K. R. Yamamoto, and B. J. Feldman, “Glucocorticoid regulation of the circadian clock modulates glucose homeostasis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 41, pp. 17582–17587, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. I. P. Torra, V. Tsibulsky, F. Delaunay et al., “Circadian and glucocorticoid regulation of Rev-erbα expression in liver,” Endocrinology, vol. 141, no. 10, pp. 3799–3806, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Dickmeis, K. Lahiri, G. Nica et al., “Glucocorticoids play a key role in circadian cell cycle rhythms,” PLoS Biology, vol. 5, no. 4, pp. 854–864, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. A. T. McCurley and G. V. Callard, “Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment,” BMC Molecular Biology, vol. 9, article 102, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. L. V. M. de Assis, M. N. Moraes, S. da Silveira Cruz-Machado, and A. M. L. Castrucci, “The effect of white light on normal and malignant murine melanocytes: a link between opsins, clock genes, and melanogenesis,” Biochimica et Biophysica Acta, vol. 1863, no. 6, pp. 1119–1133, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. A. R. Cashmore, J. A. Jarillo, Y.-J. Wu, and D. Liu, “Cryptochromes: blue light receptors for plants and animals,” Science, vol. 284, no. 5415, pp. 760–765, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. T. P. Mommsen, M. M. Vijayan, and T. W. Moon, “Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation,” Reviews in Fish Biology and Fisheries, vol. 9, no. 3, pp. 211–268, 1999. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Dickmeis and N. S. Foulkes, “Glucocorticoids and circadian clock control of cell proliferation: at the interface between three dynamic systems,” Molecular and Cellular Endocrinology, vol. 331, no. 1, pp. 11–22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. J. W. Funder, “Glucocorticoid receptors,” Journal of Steroid Biochemistry and Molecular Biology, vol. 43, no. 5, pp. 389–394, 1992. View at Publisher · View at Google Scholar · View at Scopus
  56. S. L. Lightman, R. J. Windle, M. D. Julian et al., “Significance of pulsatility in the HPA axis,” in Proceedings of the Novartis Foundation Symposia, vol. 227, pp. 244–257, 2000.
  57. S. L. Lightman, R. J. Windle, X.-M. Ma et al., “Hypothalamic-pituitary-adrenal function,” Archives of Physiology and Biochemistry, vol. 110, no. 1-2, pp. 90–93, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. S. L. Lightman, C. C. Wiles, H. C. Atkinson et al., “The significance of glucocorticoid pulsatility,” European Journal of Pharmacology, vol. 583, no. 2-3, pp. 255–262, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. T. Rhen and J. A. Cidlowski, “Antiinflammatory action of glucocorticoids—new mechanisms for old drugs,” New England Journal of Medicine, vol. 353, no. 16, pp. 1658–1723, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. A. McMaster, M. Jangani, P. Sommer et al., “Ultradian cortisol pulsatility encodes a distinct, biologically important signal,” PLoS ONE, vol. 6, no. 1, Article ID e15766, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Balsalobre, S. A. Brown, L. Marcacci et al., “Resetting of circadian time in peripheral tissues by glucocorticoid signaling,” Science, vol. 289, no. 5488, pp. 2344–2347, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Koyanagi, S. Okazawa, Y. Kuramoto et al., “Chronic treatment with prednisolone represses the circadian oscillation of clock gene expression in mouse peripheral tissues,” Molecular Endocrinology, vol. 20, no. 3, pp. 573–583, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Cuesta, N. Cermakian, and D. B. Boivin, “Glucocorticoids entrain molecular clock components in human peripheral cells,” The FASEB Journal, vol. 29, no. 4, pp. 1360–1370, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. M. P. S. Dekens and D. Whitmore, “Autonomous onset of the circadian clock in the zebrafish embryo,” The EMBO Journal, vol. 27, no. 20, pp. 2757–2765, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Husse, G. Eichele, and H. Oster, “Synchronization of the mammalian circadian timing system: Light can control peripheral clocks independently of the SCN clock: Alternate routes of entrainment optimize the alignment of the body's circadian clock network with external time,” BioEssays, vol. 37, no. 10, pp. 1119–1128, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Pezük, J. A. Mohawk, L. A. Wang, and M. Menaker, “Glucocorticoids as entraining signals for peripheral circadian oscillators,” Endocrinology, vol. 153, no. 10, pp. 4775–4783, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. T. Ota, J.-M. Fustin, H. Yamada, M. Doi, and H. Okamura, “Circadian clock signals in the adrenal cortex,” Molecular and Cellular Endocrinology, vol. 349, no. 1, pp. 30–37, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Kalsbeek and E. Fliers, “Daily regulation of hormone profiles,” in Handbook of Experimental Pharmacolology, vol. 217, pp. 185–226, 2013. View at Google Scholar
  69. J. F. López-Olmeda, B. Blanco-Vives, I. M. Pujante, Y. S. Wunderink, J. M. Mancera, and F. J. Sánchez-Vázquez, “Daily rhythms in the hypothalamus-pituitary-interrenal axis and acute stress responses in a teleost flatfish, solea senegalensis,” Chronobiology International, vol. 30, no. 4, pp. 530–539, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Sánchez-Bretaño, M. Callejo, M. Montero, Á. L. Alonso-Gómez, M. J. Delgado, and E. Isorna, “Performing a hepatic timing signal: glucocorticoids induce gper1a and gper1b expression and repress gclock1a and gbmal1a in the liver of goldfish,” Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, vol. 186, no. 1, pp. 73–82, 2016. View at Publisher · View at Google Scholar · View at Scopus