Skip to main content
Log in

Circadian expression of Bmal1 and serotonin-N-acetyltransferase mRNAs in chicken retina cells and pinealocytes in vivo and in vitro

  • Original Article
  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

Unlike mammals, rhythmic changes in serotonin N-acetyltransferase (arylalkylamine N-acetyltransferase [AANAT]) transcripts in chicken pineal cells are controlled by an oscillator located in the pinealocytes themselves, which is comprised of clock genes. A similar clock-dependent pathway has been postulated to regulate the retinal melatonin rhythm. In chicken retinal photoreceptor cells and pinealocytes, the chicken AANAT gene (cAANAT) is coexpressed with clock genes, including cBmal1 and cClock, which might regulate cAANAT transcription. Here, we have studied the temporal profile of cBmal1, cClock, and cAANAT mRNA expression in retinal cells in vivo with chickens housed in a 14/10-h light/dark (LD) cycle for 2 wk and in vitro cultured in a superfusion system for 4 LD cycles. mRNA levels of these genes were analyzed by RT-PCR and compared with their corresponding pineal transcripts. cBmal1 mRNA showed a peak during the light phase between Zeitgeber time (ZT) 8 and 10, preceding the amplitude of the nocturnal increase in cAANAT expression at ZT 16–17. Retinal cBmal1 and cAANAT mRNAs exhibited less robust cycling than their corresponding pineal transcripts in the same animal. cClock mRNA levels failed to exhibit a well-detectable rhythm. The phase of the rhythms of retinal cBmal1 and cAANAT mRNAs suggests a link between retinal cBmal1 and cAANAT expressions similar to the regulation of pineal cAANAT transcription. Based on the highly conserved nature of the clockwork, it is reasonable to consider that chicken retina and pineal gland might serve as a useful tool for the development of drugs that could infuence clock function in man.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abraham U., Albrecht U., Gwinner E., and Brandstatter R. (2002) Spatial and temporal variation of passer Per2 gene expression in two distinct cell groups of the suprachiasmatic hypothalamus in the house sparrow (Passer domesticus). Eur. J. Neurosci. 16, 429–436.

    Article  PubMed  Google Scholar 

  • Arendt J. (2001) The pineal gland: basic physiology and clinical implications, in Endocrinology, 4th ed., DeGroot, L.J., and Jameson, J. L., eds., W. B. Saunders, Philadelphia, PA, pp. 377–387.

    Google Scholar 

  • Bailey M., Chong, N. W., Xiong, J., and Cassone V. M. (2002) Chickens' Cry2: molecular analysis of an avian cryptochromein retinal and pineal photoreceptors. FEBS Lett. 513, 169–174.

    Article  PubMed  CAS  Google Scholar 

  • Bartness T. J. and Goldman B. D. (1989) Mammalian pineal melatonin: a clock for all seasons. Experientia 45, 939–945.

    Article  PubMed  CAS  Google Scholar 

  • Bernard M., Guerlotte J., Greve P., Grechez-Cassiau A., Iuvone P. M., Zatz M., et al. (1999) Melatonin synthesis pathway: circadian regulation of the genes encoding the key enzymes in the chicken pineal gland and retina. Reprod. Nutr. Dev. 39, 325–334.

    Article  PubMed  CAS  Google Scholar 

  • Bernard M., Iuvone P. M., Cassone V. M., Roseboom P. H., Coon S. L., and Klein D. C. (1997a_. Avian melatonin synthesis: photic and circadian regulation of serotonin N-acetytransferase mRNA in the chicken pineal gland and retina. J. Neurochem. 68, 213–224.

    Article  PubMed  CAS  Google Scholar 

  • Bernard M., Klein D. C., and Zatz M. (1997b) Chick pineal clock regulates serotonin N-acetyltransferase mRNA rhythmin culture. Proc. Natl. Acad. Sci. U. S. A. 94, 304–309.

    Article  PubMed  CAS  Google Scholar 

  • Binkley S. (1993) Structures and molecules involved in generation and regulation of biological rhythms in vertebrates and invertebrates. Experientia 49, 648–653.

    Article  PubMed  CAS  Google Scholar 

  • Binkley S. A., Riebman J. B., and Reilly K. B (1978) The pineal gland: a biological clock in vitro. Science 202, 1198–1201.

    Article  PubMed  CAS  Google Scholar 

  • Cassone V. M. (1990) Effects of melatonin on vertebrate circadian systems. Trends Neurosci 13, 457–463.

    Article  PubMed  CAS  Google Scholar 

  • Cassone V. M. and Menaker M. (1984) Is the avian circadian system a neuroendocrine loop? J. Exp. Zool. 232, 539–549.

    Article  PubMed  CAS  Google Scholar 

  • Chang D. C. and Reppert S. M. (2001) The circdian clocks of mice and men. Neuron 29, 555–558.

    Article  PubMed  CAS  Google Scholar 

  • Chong N. W., Bernard M., and Klein D. C. (2000) Characterization of the chicken serotonin N-acetyltransferase gene. J. Biol. Chem. 275, 32,991–32,998.

    Article  CAS  Google Scholar 

  • Chong N. W., Chaurasia S. S., Haque R., Klein D. C., and Iuvone P.M. (2003) Temporal-spatial characterization of chicken clock genes: circadian expression in retina, pineal gland, and peripheral tissues. J. Neurochem. 85, 851–860.

    Article  PubMed  CAS  Google Scholar 

  • Deguchi T. (1979) A circadian oscillator in cultured cells of chicken pineal gland. Nature 282, 94–96.

    Article  PubMed  CAS  Google Scholar 

  • Doi M., Nakajima Y., Okano T., and Fukada Y. (2001) Light-induced phase-delay of the chicken pineal circadian clock is associated with the induction of cE4bp4, a potential transriptional repressor of cPer2 gene. Proc. Natl. Acad. Sci. U. S. A. 98, 8089–8094.

    Article  PubMed  CAS  Google Scholar 

  • Dunlap J. C. (1999) Molecular basis for circadian clock. Cell 96, 271–290.

    Article  PubMed  CAS  Google Scholar 

  • Fidler A. E. and Gwinner E. (2003) Comparative analysis of avian BMAL1 and CLOCK protein sequences: a search for features associated with owl nocturnal behaviour. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 136, 861–874.

    Article  PubMed  CAS  Google Scholar 

  • Fu Z., Inaba M., Noguchi T., and Kato H. (2002) Molecular cloning and circadian regulation of cryptochrome genes in Japanese quail (Coturnix coturnix japonica). J. Biol. Rhythms 17, 14–27.

    Article  PubMed  CAS  Google Scholar 

  • Fukada Y. and Okano T. (2002) Circadian clock system in the pineal gland. Mol. Neurobiol. 25, 19–30.

    Article  PubMed  CAS  Google Scholar 

  • Haque R., Chaurasia S. S., Wessel J. H., and Iuvone P. M. (2002) Dual regulation of cryptochrome 1 mRNA expression in chicken retina by light and circadian oscillator. Neuroreport 13, 2247–2251.

    Article  PubMed  CAS  Google Scholar 

  • Iuvone P. M., Brown A. D., Haque R., Weller J., Zawilska J. B., Chaurasia S. S., et al. (2002) Retinal melatonin production: role of proteasomal proteolysis in circadian and photic control of arylalkylamine N-acetyltransferase. Invest. Ophthal. Vis. Sci. 43, 564–572.

    PubMed  Google Scholar 

  • Ivanova T. N. and Iuvone P. M. (2003) Melatonin synthesis in retina: circadian regulation of arylalkylamine N-acetytransferase activity in cultured photoreceptor cells of embryonic chicken retina. Brain Res. 973, 56–63.

    Article  PubMed  CAS  Google Scholar 

  • Jin, X., Shearman L. P., Weaver D. R., Zylka M. J., de Vries G. J., and Reppert S. M. (1999) A molecular mechanism regulating rhythmic output from the suprachiasmatic circadian clock. Cell 96, 57–68.

    Article  PubMed  CAS  Google Scholar 

  • Karsch F. J., Woodfill C. J., Malpaux B., Robinson J. E., and Wayne N. L. (1991) Melatonin and mammalian photoperiodism: synchronization of annual reproductive cycles, in Suprachiasmatic Nucleus: The Mind's Clock, Klein, D. C., Moore, R. Y., and Reppert, S. M., eds., Oxford University Press, New York, pp. 217–232.

    Google Scholar 

  • King D. P. and Takahashi J. S. (2000) Molecular genetics of circadian rhythms in mammals. Annu. Rev. Neurosci. 23, 713–742.

    Article  PubMed  CAS  Google Scholar 

  • Klein D. C. (1985) Photoneural regulation of the mammalian pineal gland, in Photoperiodism, Melatonin and the Pineal, Evered, D., and Clark, S., eds.), Pittmann, London, pp. 38–56.

    Google Scholar 

  • Klein D. C., Coon S. L., Roseboom P. H., Weller J. L., Bernard M., Gastel J. A., et al., The melatonin rhythm-generating enzyme: molecular regulation of serotonin N-acetyltransferase in the pineal gland. Recent Prog. Horm. Res. 52, 307–358.

  • Klein D. C., Moore R. Y., and Reppert S. M. (1991) Suprachiasmatic Nucleus: The Mind's Clock, Oxford University Press, New York.

    Google Scholar 

  • Kume K., Zylka M. J., Sriram S., Shearman L. P., Weaver D. R., Jin X., et al. (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98, 193–205.

    Article  PubMed  CAS  Google Scholar 

  • Larkin P., Baehr W., and Semple-Rowland S. L. (1999) Circadian regulation of iodopsin and clock is altered in theretinal degeneration of the chicken retina. Brain Res. Mol. Brain Res. 70, 253–263.

    Article  PubMed  CAS  Google Scholar 

  • Okano T., Yamamoto K., Okano K., Hirota T., Kasahara T., Sasaki M., et al. (2001) Chicken pineal clock genes: implication of BMAL 2 as a bidirectional regulator in circadian clock oscillation. Genes Cells 6, 825–836.

    Article  PubMed  CAS  Google Scholar 

  • Pittendrigh C. S. (1993) Temporal organization: reflections of a Drawinian clock-watcher. Annu. Rev. Physiol. 55, 16–54.

    Article  PubMed  CAS  Google Scholar 

  • Rekasi Z. and Czompoly T. (2002) Accumulation of rat pineal serotonin N-acetyltransferase mRNA induced by pituitary adenylate cyclase activating polypeptide and vasoactive intestinal peptide in vitro. J. Mol. Endocrinol. 28, 19–31.

    Article  PubMed  CAS  Google Scholar 

  • Rekasi Z., Csernus V., Horvath J., Vigh S., and Mess B. (1991) Long-term dynamic in vitro system for investigating rat pineal melatonin secretion. J. Neuroendocrinol. 3, 563–568.

    Article  CAS  Google Scholar 

  • Rekasi Z., Varga J. L., Schally A. V., Halmos G., Groot K., and Czompoly T. (2000) Antagonistic actions of analogs related to growth hormone-releasing hormone (GHRH) on receptors for GHRH and vasoactive intestinal peptide on rat pituitary and pineal cells in vitro. Proc. Natl. Acad. Sci. U. S. A. 97, 1218–1223.

    Article  PubMed  CAS  Google Scholar 

  • Reppert S. M. and Weaver D. R. (2002) Coordination of circadian timing in mammals. Nature 418, 935–941.

    Article  PubMed  CAS  Google Scholar 

  • Roseboom P. H., Coon S. L., Baler R., McCune S. K., Weller J. L., and Klein D. C. (1996) Melatonin synthesis: analysis of the more than 150-fold nocturnal increase in serotonin N-acetyltransferase messenger ribonucleic acid in the rat pineal gland. Endocrinology 137, 3033–3045.

    Article  PubMed  CAS  Google Scholar 

  • Shearman L. P., Sriram S., Weaver D. R., Maywood E. S., Chaves I., Zheng B., et al. (2000) Interacting molecular loops in the mammalian circadian clock. Science 288, 1013–1019.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi J. S., Hamm H., and Menaker M. (1980) Circadian rhythms of melatonin release from individual superfused chicken pineal gland in vitro. Proc. Natl. Acad. Sci. U. S. A. 77, 2319–2322.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi J. S., Murakami N., Nikaido S. S., Pratt B. L., and Robertson L. M. (1989) The avian pineal, a vertebrate model system of the circadian oscillator: cellular regulation of circadian rhythms by light, second messengers, and macromolecular synthesis. Recent Prog. Horm. Res. 45, 279–352.

    PubMed  CAS  Google Scholar 

  • Underwood H. (1990) The pineal and melatonin: regulators of circadian function in lower vertebrates. Experientia 46, 120–128.

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto K., Okano T., and Fukada Y. (2001) Chicken pineal Cry genes: light-dependent up-regulation of cCry1 and cCry2 transcripts. Eurosci. Lett. 313, 13–16.

    Article  CAS  Google Scholar 

  • Yoshimura T., Suzuki Y., Makino E., Suzuki T., Kuroiwa A., Matsuda Y., et al. (2000) Molecular analysis of avian circadian clock genes. Brain Res. Mol. Brain Res. 78, 207–215.

    Article  PubMed  CAS  Google Scholar 

  • Zatz M. (1996) Melatonin rhythms: trekking toward the heart of darknes in the chick pineal. Semin. Cell Dev. Biol. 7, 811–820.

    Article  CAS  Google Scholar 

  • Zawilska J. B. and Iuvone P. M. (1992) Melatonin synthesis in chicken retina: effect of kainic acid-induced lesions on the diurnal rhythm and D2-dopamine receptor-mediated regulation of serotonin N-acetyltransferase activity. Neurosci. Lett. 135, 71–74.

    Article  PubMed  CAS  Google Scholar 

  • Zawilska J. B. and Nowak J. Z. (1992) Reegulatory mechanisms in melatonin biosynthesis in retina. Neurochem. Int. 20, 23–36.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zoltan Rekasi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Toller, G.L., Nagy, E., Horvath, R.A. et al. Circadian expression of Bmal1 and serotonin-N-acetyltransferase mRNAs in chicken retina cells and pinealocytes in vivo and in vitro. J Mol Neurosci 28, 143–150 (2006). https://doi.org/10.1385/JMN:28:2:143

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/JMN:28:2:143

Index Entries

Navigation