Circadian rhythm of tryptophan hydroxylase activity in chicken retina
- 74 Downloads
Retinal tryptophan hydroxylase activity in chickens (1–4 weeks old and embryos) was estimated by determination of levels of 5-hydroxytryptophan (5HTP) in retinas at defined intervals after inhibition of aromatic L-amino acid decarboxylase withm-hydroxybenzylhydrazine (NSD1015).
The relationship of tryptophan hydroxylase activity to photoperiod was explored. In chickens maintained on a 12-hr light:12-hr dark cycle, a diurnal cycle in tryptophan hydroxylase activity was observed. Activity during middark phase was 4.4 times that seen in midlight phase. Cyclic changes in tryptophan hydroxylase activity persisted in constant darkness with a period of approximately 1 day, indicating regulation of the enzyme by a circadian oscillator. The phase of the tryptophan hydroxylase rhythm was found to be determined by the phase of the light/dark cycle. The relationship of the tryptophan hydroxylase rhythm to the light/dark cycle mirrors previously described rhythms of melatonin synthesis and serotoninN-acetyltransferase (NAT) activity in the retina.
Light exposure for 1 hr during dark phase suppressed NAT activity by 82%, while tryptophan hydroxylase activity was suppressed by only 30%.
Based on the differential responses of retinal NAT activity and tryptophan hydroxylase activity to acute light exposure during dark phase, it was predicted that exposure to light during dark phase would divert serotonin in the retina from melatonin biosynthesis to oxidation by MAO. In support of this, levels of 5-hydroxyindole acetic acid (5HIAA) in retina were found to be elevated approximately two-fold in chickens exposed to 30 min of light during dark phase. In pargyline-treated chickens, 2 hr of light exposure during dark phase was found to increase retinal serotonin levels by 64% over pargyline-treated controls.
Cyclic changes in tryptophan hydroxylase activity and NAT activity persisted for 2–3 days in constant light. Tryptophan hydroxylase activity at mid-night gradually decreased on successive days in constant light; on the first day of constant light, tryptophan hydroxylase activity at mid-night was 70% of activity seen during middark phase of the normal light/dark cycle and decreased further on subsequent days. In contrast, on each of 3 days of constant light, NAT activity at mid-night was approximately 15% of normal middark phase activity.
Cycloheximide completely inhibited the nocturnal increase in tryptophan hydroxylase activity when given immediately before light offset. The nocturnal increase in NAT activity was inhibited in a similar fashion.
Like the development of the NAT rhythm, cyclic changes of tryptophan hydroxylase activity in the retinas of chickens began on or immediately before the day of hatching.
The results indicate that retinal tryptophan hydroxylase activity is controlled by a circadian oscillator. The similarity of the circadian rhythm of tryptophan hydroxylase activity in chicken retina to the rhythms of retinal NAT activity and melatonin levels raises the possibility of a common oscillator regulating NAT and tryptophan hydroxylase activities, as well as involvement of tryptophan hydroxylase as a regulatory component in the melatonin synthetic pathway.
Key wordsserotonin melatonin tryptophan hydroxylase 5-hydroxytryptophan retina circadian rhythms serotoninN-acetyltransferase
Unable to display preview. Download preview PDF.
- Besharse, J. C., Iuvone, P. M., and Pierce, M. E. (1988). Regulation of rhythmic photoreceptor metabolism: A role for post-receptoral neurons. InProgress in Retinal Research (N. Osborne and J. Chader, Eds.), Pergamon Press, Oxford, pp. 21–61.Google Scholar
- Binkley, S., Reilly, K. B., and Hryshchyshyn, M. (1980).N-Acetyltransferase in the chick retina I. Circadian rhythms controlled by environmental lighting are similar to those in the pineal gland.J. Comp. Physiol. B 139103–108.Google Scholar
- Cahill, G. M., and Besharse, J. C. (1990). Circadian regulation of melatonin in the retina ofXenopus laevis: Limitation by serotonin availability.J. Neurochem. 54716–719.Google Scholar
- Carlsson, A., Davis, J. N., Kehr, W., Lundqvist, M., and Atack, C. V. (1972). Simultaneous measurement of tyrosine and tryptophan hydroxylase activities in brain in vivo using an inhibitor of the aromatic amino acid decarboxylase.Nauyn-Schmiedeberg Arch. Pharmacol. 275153–168.Google Scholar
- Ehinger, B., and Rose, B. (1988). Diurnal variation in chick retinal 5-hydroxytryptamine.Exp. Eye Res. 46819–821.Google Scholar
- Hamm, H. E., and Menaker, M. (1980). Retinal rhythms in chicks: Circadian variation in melatonin and serotoninN-acetyltransferase activity.Proc. Natl. Acad. Sci. USA 774998–5002.Google Scholar
- Iuvone, P. M. (1990). Development of melatonin synthesis in chicken retina: Regulation of serotoninN-acetyltransferase activity by light, circadian oscillators and cyclic AMP.J. Neurochem. 541562–1568.Google Scholar
- Iuvone, P. M., and Besharse, J. C. (1983). Regulation of indoleamineN-acetyltransferase activity in the retina: Effects of light and dark, protein synthesis inhibitors and cyclic nucleotide analogs.Brain Res. 273111–119.Google Scholar
- King, T. S., Steger, R. W., Steinlechner, S., and Reiter, R. J. (1984). Day-night differences in estimate rates of 5-hydroxytryptamine turnover in the rat pineal gland.Exp. Brain Res. 54432–436.Google Scholar
- Klein, D. C., and Weller, J. L. (1973). Adrenergic adenosine 3′,5′-monophosphate regulation of serotoninN-acetyltransferase activity and the temporal relationship of serotoninN-acetyltransferase activity to synthesis of3H-N-acetylserotonin and3H-melatonin in the cultured rat pineal gland.J. Pharmcol. Exp. Ther. 186516–527.Google Scholar
- Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent.J. Biol. Chem. 193265–275.Google Scholar
- Nowack, J. Z., Zurawska, E., and Zawilska, J. (1988). Light-mediated regulation of serotonin synthesis and serotoninN-acetyltransferase (NAT) activity in the rabbit retina.Neurosci. Res. Comm. 347–54.Google Scholar
- Osborne, N. N. (1980). In vitro experiments on the metabolism, uptake and release of 5-hydroxytryptamine in bovine retina.Brain Res. 184283–297.Google Scholar
- Osborne, N. N. (1982). Evidence for serotonin being a neurotransmitter in the retina. InBiology of Serotonergic Transmission (N. N. Osborne, Ed.), John Wiley and Sons, Chichester, pp. 401–430.Google Scholar
- Osborne, N. N., Nesselhut, T., Nicholas, D. A., and Cuello, A. C. (1981). Serotonin: A transmitter candidate in the vertebrate retina.Neurochem. Int. 3171–176.Google Scholar
- Osborne, N. N., Patel, S., and Beaton, D. W. (1984). Serotonin, a major metabolite of tryptophan in the rabbit retina. InProgress in Tryptophan and Serotonin Research (H. G. Schlossberger, W. Kochen, B. Linzen, and H. Steinhart, Eds.), Walter de Gruyter, Berlin, pp. 275–284.Google Scholar
- Parkinson, D., and Rando, R. R. (1981). Evidence for a neurotransmitter role for 5-hydroxytryptamine in chick retina.J. Neurosci. 11211–1217.Google Scholar
- Pierce, M. E., Barker, D., Harrington, J., and Takahashi, J. S. (1989). Cyclic AMP-dependent melatonin production in Y79 human retinoblastoma cells.J. Neurochem. 53307–310.Google Scholar
- Redburn, D. A. (1984). Serotonin systems in the inner and outer plexiform layers of the vertebrate retina.Fed. Proc. 432699–2703.Google Scholar
- Reppert, S. M., and Sagar, S. M. (1983). Characterization of the day-night variation of retinal melatonin content in the chick.Invest. Ophthalmol. Vis. Sci. 24294–300.Google Scholar
- Shibuya, H., Toru, M., and Watanabe, S. (1978). A circadian rhythm of tryptophan hydroxylase in rat pineals.Brain Res. 138364–368.Google Scholar
- Sitaram, B. R., and Lees, G. J. (1978). Diurnal rhythm and turnover of tryptophan hydroxylase in the pineal gland of the rat.J. Neurochem. 311021:1026.Google Scholar
- Sugden, D., Grady, R. Jr., and Mefford, I. N. (1989). Measurement of tryptophan hydroxylase activity in rat pineal glands and pinealocytes using an HPLC assay with electrochemical detection.J. Pineal Res. 6285–292.Google Scholar
- Thomas, K. B., and Iuvone, P. M. (1989). Tryptophan hydroxylase activity in chicken retina and pineal gland displays circadian rhythmicity.Soc. Neurosci. Abstr. 12:546.9.Google Scholar
- Thomas, K. B., Zawilska, J., and Iuvone, P. M. (1990). Arylalkylamine (serotonin)N-acetyltransferase assay using high performance liquid chromatography with fluorescence or electrochemical detection ofN-acetyltryptamine.Anal. Biochem. 184228–234.Google Scholar
- Wiechmann, A. F. (1986). Melatonin: parallels in pineal gland and retina.Exp. Eye Res. 42507–527.Google Scholar
- Zawilska, J., and Iuvone, P. M. (1989). Catecholamine receptors regulating serotoninN-acetyltransferase activity and melatonin content of chicken retina and pineal gland: D2 dopamine receptors in retina and alpha-2 adrenergic receptors in pineal gland.J. Pharmacol. Exp. Ther. 25086–92.Google Scholar