Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 715708, 11 pages
http://dx.doi.org/10.1155/2014/715708
Research Article

Adrenergic Activation of Melatonin Secretion in Ovine Pineal Explants in Short-Term Superfusion Culture Occurs via Protein Synthesis Independent and Dependent Phenomena

Department of Histology and Embryology, Faculty of Veterinary Medicine, University of Warmia and Mazury, Oczapowskiego Street 13, 10-719 Olsztyn, Poland

Received 4 April 2014; Revised 23 June 2014; Accepted 24 June 2014; Published 15 July 2014

Academic Editor: Gabriel F. Anhe

Copyright © 2014 Bogdan Lewczuk 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. J. J. Gooley, J. Lu, T. C. Chou, T. E. Scammell, and C. B. Saper, “Melanopsin in cells of origin of the retinohypothalamic tract,” Nature Neuroscience, vol. 4, no. 12, p. 1165, 2001. View at Google Scholar
  2. M. Münch and A. Kawasaki, “Intrinsically photosensitive retinal ganglion cells: classification, function and clinical implications,” Current Opinion in Neurology, vol. 26, no. 1, pp. 45–51, 2013. View at Google Scholar
  3. H. Okamura, S. Yamaguchi, and K. Yagita, “Molecular machinery of the circadian clock in mammals,” Cell and Tissue Research, vol. 309, no. 1, pp. 47–56, 2002. View at Google Scholar
  4. V. Simonneaux and C. Ribelayga, “Generation of the melatonin endocrine message in mammals: a review of the complex regulations of melatonin synthesis by norepinephrine, peptides and other pineal transmitters,” Pharmacological Reviews, vol. 55, no. 2, pp. 325–395, 2003. View at Google Scholar
  5. R. J. Reiter, “The melatonin rhythm: both a clock and a calendar,” Experientia, vol. 49, no. 8, pp. 654–664, 1993. View at Publisher · View at Google Scholar
  6. W. J. Drijfhout, A. G. van der Linde, S. E. Kooi, C. J. Grol, and B. H. Westerink, “Norepinephrine release in the rat pineal gland: the input from the biological clock measured by in vivo microdialysis,” Journal of Neurochemistry, vol. 66, no. 2, pp. 748–755, 1996. View at Google Scholar
  7. P. J. Larsen, L. W. Enquist, and J. P. Card, “Characterization of the multisynaptic neuronal control of the rat pineal gland using viral transneuronal tracing,” European Journal of Neuroscience, vol. 10, no. 1, pp. 128–145, 1998. View at Google Scholar
  8. E. Maronde, M. Pfeffer, C. von Gall et al., “Signal transduction in the rodent pineal organ. From the membrane to the nucleus,” Advances in Experimental Medicine and Biology, vol. 460, pp. 109–131, 1999. View at Google Scholar
  9. T. Liu and J. Borjigin, “N-acetyltransferase is not the ratel imiting enzyme of melatonin synthesis at night,” Journal of Pineal Research, vol. 39, no. 1, pp. 91–96, 2005. View at Google Scholar
  10. E. Maronde and J. H. Stehle, “The mammalian pineal gland: known facts, unknown facets,” Trends in Endocrinology and Metabolism, vol. 18, no. 4, pp. 142–149, 2007. View at Google Scholar
  11. A. K. Ho and C. L. Chik, “Modulation of Aanat gene transcription in the rat pineal gland,” Journal of Neurochemistry, vol. 112, no. 2, pp. 321–331, 2010. View at Google Scholar
  12. J. Borjigin, L. S. Zhang, and A. A. Calinescu, “Circadian regulation of pineal gland rhythmicity,” Molecular and Cellular Endocrinology, vol. 349, no. 1, pp. 13–19, 2012. View at Google Scholar
  13. M. J. Bailey, S. L. Coon, D. A. Carter, A. Humphries, J. S. Kim, and Q. Shi, “Night/day changes in pineal expression of >600 genes: central role of adrenergic/cAMP signaling,” The Journal of Biological Chemistry, vol. 284, no. 12, pp. 7606–7622, 2009. View at Google Scholar
  14. A. K. Ho and C. L. Chik, “Post-receptor mechanism in dual receptors regulation of second messengers in rat pineal gland,” Progress in Clinical and Biological Research, vol. 342, pp. 139–145, 1990. View at Google Scholar
  15. E. Maronde, C. Schomerus, J. H. Stehle, and H. W. Korf, “Control of CREB phosphorylation and its role for induction of melatonin synthesis in rat pinealocytes,” Biology of the Cell, vol. 89, no. 8, pp. 505–511, 1997. View at Google Scholar
  16. H. W. Korf, C. Schomerus, E. Maronde, and J. H. Stehle, “Signal transduction molecules in the rat pineal organ: Ca2+, pCREB, and ICER,” Naturwissenschaften, vol. 83, no. 12, pp. 535–543, 1996. View at Google Scholar
  17. P. H. Roseboom, S. L. Coon, R. Baler, S. K. McCune, J. L. Weller, and D. C. Klein, “Melatonin synthesis: analysis of the more than 150-fold nocturnal increase in serotonin N-acetyltransferase messenger ribonucleic acid in the rat pineal gland,” Endocrinology, vol. 137, no. 7, pp. 3033–3045, 1996. View at Google Scholar
  18. E. Maronde, M. Pfeffer, J. Olcese et al., “Transcription factors in neuroendocrine regulation: rhythmic changes in pCREB and ICER levels frame melatonin synthesis,” Journal of Neuroscience, vol. 19, no. 9, pp. 3326–3336, 1999. View at Google Scholar
  19. J. A. Gastel, P. H. Roseboom, P. A. Rinaldi, J. L. Weller, and D. C. Klein, “Melatonin production: proteasomal proteolysis in serotonin N-acetyltransferase regulation,” Science, vol. 279, no. 5355, pp. 1358–1360, 1998. View at Google Scholar
  20. C. Schomerus, H. W. Korf, E. Laedtke, J. L. Weller, and D. C. Klein, “Selective adrenergic/cyclic AMP-dependent switch-off of proteasomal proteolysis alone switches on neural signal transduction: an example from the pineal gland,” Journal of Neurochemistry, vol. 75, no. 5, pp. 2123–2132, 2000. View at Google Scholar
  21. C. Schomerus, E. Laedtke, and H. W. Korf, “Activation of arylalkylamines N-acetyltransferase by phorbol esters in bovine pinealocytes suggests a novel regulatory pathway in melatonin synthesis,” Journal of Neuroendocrinology, vol. 16, no. 9, pp. 741–749, 2004. View at Google Scholar
  22. J. H. Stehle, C. Vongall, C. Schomerus, and H. W. Korf, “Of rodents and ungulates and melatonin: creating a uniform code for darkness by different signaling mechanisms,” Journal of Biological Rhythms, vol. 16, no. 4, pp. 312–325, 2001. View at Publisher · View at Google Scholar
  23. S. L. Coon, P. H. Roseboom, R. Baler et al., “Pineal serotonin N-acetyltransferase : expression cloning and molecular analysis,” Science, vol. 270, no. 5242, pp. 1681–1683, 1995. View at Google Scholar
  24. J. V. Fleming, P. Barrett, S. L. Coon, P. J. Morgan, and D. C. Klein, “Ovine arylalkylamine N-acetyltransferase in the pineal and pituitary glands: differences in function and regulation,” Endocrinology, vol. 140, no. 2, pp. 972–978, 1999. View at Google Scholar
  25. S. L. Coon, E. del Olmo, W. S. Young, and D. C. Klein, “Melatonin synthesis enzymes in Macaca mulatta: focus on arylalkylamine N-acetyltransferase (EC 2.3.1.87),” The Journal of Clinical Endocrinology and Metabolism, vol. 87, no. 10, pp. 4699–4706, 2002. View at Publisher · View at Google Scholar
  26. E. Maronde, A. Saade, K. Ackermann et al., “Dynamics in enzymatic protein complexes offer a novel principle for the regulation of melatonin synthesis in the human pineal gland,” Journal of Pineal Research, vol. 51, no. 1, pp. 145–155, 2011. View at Publisher · View at Google Scholar
  27. J. H. Stehle, A. Saade, O. Rawashdeh, K. Ackermann, A. Jilg, and T. Sebeste, “A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases,” Journal of Pineal Research, vol. 51, no. 1, pp. 17–43, 2011. View at Google Scholar
  28. S. J. Lee, T. Liu, A. Chattoraj et al., “Posttranscriptional regulation of pineal melatonin synthesis in Octodon degus,” Journal of Pineal Research, vol. 47, no. 1, pp. 75–81, 2009. View at Google Scholar
  29. S. Ganguly, J. Gastel, J. L. Weller et al., “Role of a pineal cAMP-operated arylalkylamine N-acetyltransferase/14-3-3-binding switch in melatonin synthesis,” Proceedings of the National Academy of Sciences, vol. 98, no. 14, pp. 8083–8088, 2001. View at Google Scholar
  30. S. L. Coon, J. L. Weller, H. W. Korf, M. A. Namboodiri, M. Rollag, and D. C. Klein, “cAMP regulation of arylalkylamine N- acetyltransferase (AANAT, EC 2.3.1.87)—a new cell line (1E7) provides evidence of intracellular AANAT activation,” The Journal of Biological Chemistry, vol. 276, no. 26, pp. 24097–24107, 2001. View at Google Scholar
  31. T. Obsil, R. Ghirlando, D. C. Klein, S. Ganguly, and F. Dyda, “Crystal structure of the 14-3-35 zeta: serotonin N-acetyltransferase complex: a role for scaffolding in enzyme regulation,” Cell, vol. 105, no. 2, pp. 257–267, 2001. View at Google Scholar
  32. B. Lewczuk, Mechanisms of adrenergic regulation of melatonin secretion in the pig pineal gland. In vitro study [Dissertations and monographs], UWM Press Olsztyn, 2002.
  33. A. Chattoraj, T. Liu, L. S. Zhang, Z. Huang, and J. Borjigin, “Melatonin formation in mammals: in vivo perspectives,” Reviews in Endocrine and Metabolic Disorders, vol. 10, no. 4, pp. 237–243, 2009. View at Google Scholar
  34. S. Ganguly, J. L. Weller, A. Ho, P. Chemineau, B. Malpaux, and D. C. Klein, “Melatonin synthesis: 14-3-3-dependent activation and inhibition of arylalkylamine Nacetyltransferase mediated by phosphoserine-205,” Proceedings of the National Academy of Sciences, vol. 102, no. 4, pp. 1222–1227, 2005. View at Google Scholar
  35. M. A. Namboodiri, D. Sugden, D. C. Klein, L. Tamarkin, and I. N. Mefford, “Serum melatonin and pineal indoleamine metabolism in a species with a small day/night N-acetyltransferase rhythm,” Comparative Biochemistry and Physiology Part B, vol. 80, no. 4, pp. 731–736, 1985. View at Google Scholar
  36. M. A. Namboodiri, D. Sugden, D. C. Klein, R. Grady, and I. N. Mefford, “Rapid nocturnal increase in ovine pineal N-acetyltransferase activity and melatonin synthesis: effects of cycloheximide,” Journal of Neurochemistry, vol. 45, no. 3, pp. 832–835, 1985. View at Publisher · View at Google Scholar
  37. J. Falcón, S. Barraud, C. Thibault, and V. Bégay, “Inhibitors of messenger RNA and protein synthesis affect differently serotonin arylalkylamine N-acetyltransferase activity in clock-controlled and non clock-controlled fish pineal,” Brain Research, vol. 797, no. 1, pp. 109–117, 1998. View at Publisher · View at Google Scholar
  38. Z. Huang, T. Liu, and J. Borjigin, “N-terminal residues regulate proteasomal degradation of AANAT,” Journal of Pineal Research, vol. 48, no. 3, pp. 290–296, 2010. View at Google Scholar
  39. D. L. Terriff, C. L. Chik, D. M. Price, and A. K. Ho, “Proteasomal proteolysis in the adrenergic induction of arylalkylamine-N-acetyltransferase in rat pinealocytes,” Endocrinology, vol. 146, no. 11, pp. 4795–4803, 2005. View at Google Scholar
  40. V. Simonneaux, N. Sinitskaya, A. Salingre, M. L. Garidou, and P. Pévet, “Rat and Syrian hamster: two models for the regulation of Aanat gene expression,” Chronobiology International, vol. 23, no. 1-2, pp. 351–359.
  41. C. von Gall, A. J. Lewy, C. Schomerus et al., “Transcription factor dynamics and neuroendocrine signalling in the mouse pineal gland: a comparative analysis of melatonin-deficient C57Bl mice and melatonin-proficient C3H mice,” European Journal of Neuroscience, vol. 12, no. 3, pp. 964–972, 2000. View at Google Scholar
  42. M. L. Garidou, F. Gauer, B. Vivien-Roels, B. Sicard, P. Pévet, and V. Simonneaux, “Pineal arylalkylamine N-acetyltransferase gene expression is highly stimulated at night in the diurnal rodent, Arvicanthis ansorgei,” European Journal of Neuroscience, vol. 15, no. 10, pp. 1632–1640, 2002. View at Google Scholar
  43. M. Bernard, J. Guerlotté, P. Grève, A. Gréchez-Cassiau, and M. P. Iuvone, “Melatonin synthesis pathway: circadian regulation of the genes encoding the key enzymes in the chicken pineal gland and retina,” Reproduction Nutrition Development, vol. 39, no. 3, pp. 325–334, 1999. View at Google Scholar
  44. B. Lewczuk and B. Przybylska-Gornowicz, “The effect of continuous darkness and illumination on the function and the morphology of the pineal gland in the domestic pig. II. The effect on pinealocyte ultrastructure,” Neuroendocrinology Letters, vol. 21, no. 4, pp. 293–299, 2000. View at Google Scholar
  45. B. Lewczuk and B. Przybylska-Gornowicz, “Effects of sympathicolytic and sympaticomimetic drugs on pineal ultrastructure in the domestic pig,” Journal of Pineal Research, vol. 23, no. 4, pp. 198–208, 1997. View at Publisher · View at Google Scholar
  46. B. Lewczuk and B. Przybylska-Gornowicz, “Effects of sympathicolytic and sympathicomimetic drugs on plasma immunoreactive melatonin in the domestic pig,” Journal of Pineal Research, vol. 23, no. 4, pp. 209–220, 1997. View at Google Scholar
  47. B. Lewczuk and B. Przybylska-Gornowicz, “The effect of continuous darkness and illumination on the function and the morphology of the pineal gland in the domestic pig. I. The effect on plasma melatonin level,” Neuroendocrinology Letters, vol. 21, no. 4, pp. 283–291, 2000. View at Google Scholar