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Regulation of endogenous dopamine release in amphibian retina by melatonin: The role of GABA

Published online by Cambridge University Press:  02 June 2009

Jeffrey H. Boatright ,
Nara M. Rubim  and
P. Michael Iuvone
Jeffrey H. Boatright
Affiliation:
Department of Pharmacology and The Neuroscience Training Program, Emory University School of Medicine, Atlanta
Nara M. Rubim
Affiliation:
Department of Pharmacology and The Neuroscience Training Program, Emory University School of Medicine, Atlanta
P. Michael Iuvone
Affiliation:
Department of Pharmacology and The Neuroscience Training Program, Emory University School of Medicine, Atlanta
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Abstract

In the retina of the African clawed frog (Xenopus laevis), endogenous dopamine release increases in light and decreases in darkness. Exogenous melatonin and several chemical analogs of melatonin suppressed light-evoked dopamine release from frog retina in a concentration-dependent manner. The rank order of potency for inhibition of light-evoked dopamine release was melatonin » 5-methoxytryptamine ≥ N-acetylserotonin > 5-methoxytryptophol ⋙ serotonin. Melatonin did not suppress dopamine release below levels seen in darkness. The putative melatonin receptor antagonist luzindole inhibited the effect of melatonin. Luzindole enhanced dopamine release in darkness but had little effect in light. These data suggest a role for endogenous melatonin in dark-induced suppression of retinal dopamine.

Picrotoxin and bicuculline, GABA-A receptor antagonists, blocked melatonin-induced suppression of dopamine release. In the presence of melatonin, bicuculline was significantly less potent in stimulating dopamine release. These results suggest that melatonin enhances GABAergic inhibition of light-evoked dopamine release. This mechanism may underlie the light/dark difference in dopamine release in vertebrate retina.

Keywords

DopamineMelatoninGamma-aminobutyric acidRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 5 , September 1994 , pp. 1013 - 1018
Copyright
Copyright © Cambridge University Press 1994

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References

Anton, A.H. & Sayre, D.F. (1962). A study of the factors affecting the aluminum oxide-trihydroxyindole procedure for the analysis of catecholamines. Journal of Pharmacology and Experimental Therapeutics 138, 360–375.Google ScholarPubMed
Besharse, J.C. & Iuvone, P.M. (1983). Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature 305, 133–135.CrossRefGoogle ScholarPubMed
Blazynski, C. & Dubocovich, M.L. (1991). Localization of 2-[125I]iodomelatonin binding sites in mammalian retina. Journal of Neurochemistry 56, 1873–1880.CrossRefGoogle ScholarPubMed
Boatright, J.H. & Iuvone, P.M. (1989 a). GABA and the regulation of serotonin N-acetyltransferase activity in amphibian retina —I. Effects of GABA agonists and antagonists. Neurochemistry International 15, 541–547.CrossRefGoogle ScholarPubMed
Boatright, J.H. & Iuvone, P.M. (1989 b). Melatonin suppresses the light-evoked release of endogenous dopamine from retinas of frogs (Xenopus laevis). Society for Neuroscience Abstracts 15, 1395.Google Scholar
Boatright, J.H. & Iuvone, P.M. (1991). Multiple inhibitory modulators of dopamine release in frog retina. Investigative Ophthalmology and Visual Science (Abstract) 32, 2902.Google Scholar
Boatright, J.H., Hoel, M.J. & Iuvone, P.M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light and K+-evoked depolarization. Brain Research 482, 164–168.CrossRefGoogle ScholarPubMed
Boatright, J.H., Rubim, N. & Iuvone, P.M. (1994). Regulation of endogenous dopamine release in amphibian retina by gamma-aminobutyric acid and glycine. Visual Neuroscience 11, 1003–1012.CrossRefGoogle ScholarPubMed
Cahill, G.M. & Besharse, J.C. (1990). Circadian regulation of mela-tonin in the retina of Xenopus laevis: Limitation by serotonin availability. Journal of Neurochemistry 54, 716–719.CrossRefGoogle ScholarPubMed
Coloma, P.M. & Niles, L.P. (1988). Melatonin enhancement of [3H]-gamma-aminobutyric acid and [3H]-muscimol binding in rat brain. Biochemical Pharmacology 37, 1271–1274.CrossRefGoogle ScholarPubMed
DeLean, A., Munson, P.J. & Rodbard, D. (1978). Simultaneous analysis of families of sigmoidal curves: Application to bioassay, radio-ligand assay, and physiological dose-response curves. American Journal of Physiology 235, E97–E102.Google Scholar
Dubocovich, M.L. (1983). Melatonin is a potent modulator of dopamine release in the retina. Nature 306, 782–784.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. (1984). N-Acetyltryptamine antagonizes the melatonin-induced inhibition of [3H]dopamine release from retina. European Journal of Pharmacology 105, 193–194.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. (1985). Characterization of a retinal melatonin receptor. Journal of Pharmacology and Experimental Therapeutics 234, 395–401.Google ScholarPubMed
Dubocovich, M.L. (1988). Pharmacology and function of melatonin receptors. FASEB Journal 2, 2765–2773.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. & Takahashi, J.S. (1987). Use of 2-[125I]-iodomelatonin to characterize melatonin binding sites in chicken retina. Proceedings of the National Academy of Sciences of the U.S.A. 84, 3916–3920.CrossRefGoogle ScholarPubMed
Hamm, H.E. & Menaker, M. (1980). Retinal rhythms in chicks-circadian variation in melatonin and serotonin N-acetyltransferase. Proceedings of the National Academy of Sciences of the U.S.A. 77, 4998–5002.CrossRefGoogle ScholarPubMed
Heward, C.B. & Hadley, M.E. (1975). Structure-activity relationships of melatonin and related indoleamines. Life Sciences 17, 1167–1178.CrossRefGoogle ScholarPubMed
Hunt, P., Kannengiesser, M. & Raynaud, J. (1984). Nomifensine: A new potent inhibitor of dopamine uptake into synaptosomes from rat corpus striatum. Journal of Pharmacy and Pharmacology 26, 370–371.CrossRefGoogle Scholar
Iuvone, P.M. & Besharse, J.C. (1983). Regulation of indoleamine N-acetyltransferase activity in the retina: Effects of light and dark, protein synthesis inhibitors and cyclic nucleotides. Brain Research 273, 111–119.CrossRefGoogle Scholar
Iuvone, P.M. & Besharse, J.C. (1986). Dopamine receptor-mediated inhibition of serotonin N-acetyltransferase activity in retina. Brain Research 369, 168–176.CrossRefGoogle ScholarPubMed
Iuvone, P.M. & Gan, J. (1994). Melatonin receptor-mediated inhibition of cyclic AMP accumulation in chick retinal cell cultures. Journal of Neurochemistry 63, 118–124.CrossRefGoogle ScholarPubMed
Lamnen, J.T. & Saavedra, J.M. (1990). Characterization of melatonin receptors in the rat suprachiasmatic nuclei: Modulation of affinity with cations and guanine nucleotides. Endocrinology 126, 2110–2115.Google Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 193, 265–275.CrossRefGoogle ScholarPubMed
Massey, S.C. & Neal, M.J. (1979). The light evoked release of acetyl-choline from the rabbit retina in vivo and its inhibition by gamma-aminobutyric acid. Journal of Neurochemistry 32, 1327–1329.CrossRefGoogle Scholar
Massey, S.C. & Redburn, D.A. (1982). A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. Journal of Neuroscience 2, 1633–1643.CrossRefGoogle ScholarPubMed
Mitchell, C.K. & Redburn, D.A. (1991). Melatonin inhibits ACh release from rabbit retina. Visual Neuroscience 7, 479–486.CrossRefGoogle ScholarPubMed
Niles, L.P. (1987). [3H]-Melatonin binding in membranes and cytosol fractions from rat and calf brain. Journal of Pineal Research 4, 89–93.CrossRefGoogle Scholar
Niles, L.P. & Peace, C.H. (1990). Allosteric modulation of t-[35S]butyl-bicyclophosphorothionate binding in rat brain by melatonin. Brain Research Bulletin 24, 635–638.CrossRefGoogle Scholar
Niles, L.P., Pickering, D.S. & Sayer, B.C. (1987). HPLC-purified 2-[125I]-iodomelatonin labels multiple binding sites in hamster brain. Biochemical and Biophysical Research Communications 147, 949–956.CrossRefGoogle ScholarPubMed
Nowak, J.Z. (1988). Melatonin inhibits [3H]-dopamine release from the rabbit retina evoked by light, potassium and electrical stimulation. Medical Science Research 16, 1073–1075.Google Scholar
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movements: Interaction of melatonin and dopamine in the control of cone length. Journal of General Physiology 86, 671–689.CrossRefGoogle ScholarPubMed
Pierce, M.E. & Besharse, J.C. (1988). Circadian regulation of retinomotor movements: II. The role of GABA in the regulation of cone position. Journal of Comparative Neurology 270, 279–287.CrossRefGoogle Scholar
Rosenstein, R.E. & Cardinali, D.P. (1986). Melatonin increases in vivo GABA accumulation in rat hypothalamus, cerebellum, cerebral cortex and pineal gland. Brain Research 398, 403–406.CrossRefGoogle ScholarPubMed
Rosenstein, R.E. & Cardinali, D.P. (1990). Central gabaergic mechanisms as targets for melatonin activity in brain. Neurochemistry International 17, 373–379.CrossRefGoogle ScholarPubMed
Rosenstein, R.E., Chuluyan, H.E., Pereyra, E.N. & Cardinali, D.P. (1989 a). Release and effect of gamma-aminobutyric acid (GABA) on rat pineal melatonin production in vitro. Cellular and Molecular Neurobiology 9, 207–219.CrossRefGoogle ScholarPubMed
Rosenstein, R.E., Estevez, A.G. & Cardinali, D.P. (1989 b). Time-dependent effect of glutamic acid decarboxylase and 36Cl− influx in rat hypothalamus. Journal of Neuroendocrinology 1, 443–447.CrossRefGoogle Scholar
Schütte, M. & Witkovsky, P. (1991). Dopaminergic interplexiform cells and centrifugal fibers in the Xenopus retina. Journal of Neurocytology 20, 195–207.CrossRefGoogle ScholarPubMed
Stankov, B., Biella, G., Panara, C., Lucini, V., Capsoni, S., Fau-Teck, J., Cozzi, B. & Fraschini, F. (1992). Melatonin signal transduction and mechanism of action in the central nervous system: Using the rabbit cortex as a model. Endocrinology 130, 2152–2159.Google ScholarPubMed
Sugden, D. (1992). Effect of putative melatonin receptor antagonists on melatonin-induced pigment aggregation in isolated Xenopus laevis melanophores. European Journal of Pharmacology 213, 405–408.CrossRefGoogle ScholarPubMed
Thomas, K.B. & Iuvone, P.M. (1991). Circadian rhythm of tryptophan hydroxylase activity in chicken retina. Cellular and Molecular Neurobiology 11, 511–527.CrossRefGoogle ScholarPubMed
Thomas, K.B., Zawilska, J. & Iuvone, P.M. (1990). Arylalkylamine (serotonin) N-acetyltransferase assay using high-performance liquid chromatography with fluorescence or electrochemical detection of N-acetyltryptamine. Analytical Biochemistry 184, 228–234.CrossRefGoogle ScholarPubMed
Winer, B.J. (1962). Statistical Principles in Experimental Design. New York: McGraw-Hill.CrossRefGoogle Scholar
Zisapel, N. & Laudon, M. (1987). A novel melatonin antagonist affects melatonin-mediated processes in vitro and in vivo. European Journal of Pharmacology 136, 259–260.CrossRefGoogle ScholarPubMed