Hostname: page-component-77c89778f8-m42fx Total loading time: 0 Render date: 2024-07-21T09:18:36.990Z Has data issue: false hasContentIssue false
  • English
  • Français

Melatonin inhibits ACh release from rabbit retina

Published online by Cambridge University Press:  02 June 2009

Cheryl K. Mitchell  and
Dianna A. Redburn
Cheryl K. Mitchell
Affiliation:
Department of Neurobiology and Anatomy, The University of Texas Medical School, Houston
Dianna A. Redburn
Affiliation:
Department of Neurobiology and Anatomy, The University of Texas Medical School, Houston
Get access Rights & Permissions [Opens in a new window]

Abstract

Previous studies have suggested that melatonin, released from photoreceptors, may modulate retinal dark-adaptive responses by inhibition of dopamine release from retinal interneurons. We have broadened these studies to examine the effect of melatonin on release of another retinal neurotransmitter, acetylcholine (ACh). The ACh system in rabbit retina has been localized to starburst amacrine cells, which release ACh in response to a variety of experimental stimuli, including direct potassium depolarization, flashing light, and glutamatergic as well as GABAergic inputs. The effect of melatonin on release of endogenously synthesized [3H]-ACh was measured in perfusates from retinas or retinal synaptosomes preloaded with [3H]-choline chloride. Melatonin significantly inhibited ACh release stimulated by potassium in intact retina but not in synaptosomes. Stimulation of intact retina by flashing light or by the glutamate receptor agonist, kainic acid, was also inhibited by melatonin. In contrast, there was no significant effect of melatonin on picrotoxin-induced release. These findings suggest that melatonin does have an inhibitory effect on ACh release, either by direct interaction with the cholinergic amacrine cell, or indirectly via GABAergic but not glutamatergic neurons.

Keywords

MelatoninACh releaseKainic acidLight stimulationCholinergic amacrine cells
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 5 , November 1991 , pp. 479 - 486
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anton-Tay, F. (1974). Melatonin effects on brain function. Advances in Biochemical Psychopharmacology 11, 315–324.Google ScholarPubMed
Anton-Tay, F., Chou, C., Anton, S. & Wurtman, R.J. (1968). Brain serotonin concentration: elevation following intraperitoneal administration of melatonin. Science 162, 277–278.CrossRefGoogle ScholarPubMed
Besharse, J.C. & Dunis, D.A. (1983). Methoxyindoles and photoreceptor metabolism activation of rod shedding. Science 219, 1341–1343.CrossRefGoogle ScholarPubMed
Besharse, J.C., Iuvone, P.M. & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: a role for post-receptor neurons. In Progress in Retinal Research, Vol 7. ed. Osborne, N. & Chader, G., pp. 21–61. New York: Pergamon Press.Google Scholar
Boatright, J.H., Iuvone, P.M. & Pierce, M.E. (1988). Melatonin sup-presses the light-evoked release of endogenous dopamine from retinas of frogs (Xenopus laevis). Society of Neuroscience Abstracts 15, 1395.Google Scholar
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: immunocytochemical localization and relationship to GABAergic and cholinesterase-containing neurons. Brain Research 401, 385–391.CrossRefGoogle ScholarPubMed
Brecha, N., Johnson, D., Peichl, L. & Wassle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and γ-aminobutyrate immunoreactivity. Proceedings of National Academy of Science of the U.S.A. 85, 6187–6191.CrossRefGoogle ScholarPubMed
Bubenik, G.A., Purtill, R.A., Brown, G.M. & Grota, L.J. (1978). Melatonin in the retina and the harderian gland ontogeny, diurnal variations, and melatonin treatment. Experimental Eye Research 27, 323–333.CrossRefGoogle ScholarPubMed
Cardinali, D.P. (1975). Changes in hypothalamic neurotransmitter uptake following pinealectomy, superior cervical ganglionectomy, or melatonin administration to rats. Neuroendocrinology 19, 91–95.CrossRefGoogle ScholarPubMed
Cardinali, D.P., Nagle, C.A., Freire, F. & Rosner, J.M. (1975). Effects of melatonin on neurotransmitter uptake and release by synaptosome-rich homogenates of the rat hypothalamus. Neuroendocrinology 18, 72–75.CrossRefGoogle ScholarPubMed
Cardinali, D.P., Vacas, M.I. & Boyer, E.E. (1979). Specific binding of melatonin in bovine brain. Endocrinology 105, 437–441.CrossRefGoogle ScholarPubMed
Chun, M.H., Wassle, H. & Brecha, N. (1988). Colocalization of [3H]-muscimol uptake and choline acetyltransferase immunoreactivity in amacrine cells of the cat retina. Neuroscience Letters 94, 259–263.CrossRefGoogle ScholarPubMed
Cohen, M., Roselle, D., Chabner, B., Schmidt, T.J. & Lippman, M. (1978). Evidence for a cytoplasmic melatonin receptor. Nature 274, 894.CrossRefGoogle ScholarPubMed
Cunningham, J.R. & Neal, M.J. (1983). Effect of excitatory amino acids and analogues on [3H]-acetylcholine release from amacrine cells of the rabbit retina. Journal of Physiology 366, 47–62.CrossRefGoogle Scholar
Dubocovich, M.L. (1983). Melatonin is a potent modulator dopamine release in the retina. Nature 306, 782–784.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. (1985). Characterization of a retinal melatonin receptor. Journal of Pharmacology and Experimental Therapeutics 234, 395–409.Google ScholarPubMed
Dubocovich, M.L. (1988). Pharmacology and function of melatonin receptors. Journal of the Federation of American Societies for Experimental Biology 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 National Academy of Science of the U.S.A. 84, 3916–3920.CrossRefGoogle ScholarPubMed
Dubocovich, M.L., Shankar, G. & Mickel, M. (1989). 2-[125I]-iodomelatonin labels sites with identical pharmacological characteristics in chicken brain and chicken retina. European Journal of Pharmacology 162, 289–299.CrossRefGoogle ScholarPubMed
Duncan, M.J., Takahashi, J.S. & Dubocovich, M.L. (1988). 2-[125I]-iodomelatonin binding sites in hamster brain membranes: pharmacological characteristics and regional distribution. Endocrinology 122, 1825–1833.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr., (1983a). Starburst amacrine cells and cholinergic neurons: mirror symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138–144.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr, (1983b). ON and OFF pathways through amacrine cells in mammalian retina: the synaptic connections of “Star-burst” amacrine cells. Vision Research 23, 1265–1279.CrossRefGoogle Scholar
Friedman, D.A. & Redburn, D.A. (1990). Evidence for functionally distinct subclasses of γ-aminobutyric acid receptors in rabbit retina. Journal of Neurochemistry 55, 1189–1199.CrossRefGoogle ScholarPubMed
Hamm, H.E. & Menaker, M. (1980). Retinal rhythms in chicks—circadian variation in melatonin and serotonin N-acetyltransferase activity. Proceedings of the National Academy of Sciences of the U.S.A. 77, 4998–5002.CrossRefGoogle ScholarPubMed
Hensler, J.G. & Dubocovich, M.L. (1986). D1-dopamine receptor activation mediates [3H]-acetylcholine release from rabbit retina. Brain Research 398, 407–412.CrossRefGoogle ScholarPubMed
Hollander, C.S., Prasad, R., Richardson, S., Herooka, Y. & Suzuki, S. (1977). Melatonin modulates hormonal release from organ cultures of rat hypothalamus. Journal of Neural Transmission (Suppl.) 13, 369.Google Scholar
Iuvone, P.M., Galli, G.L., Garrison-Gund, C.K. & Neff, N.H. (1978). Light stimulates tyrosine activity and dopamine synthesis in retinal amacrine cells. Science 202, 901–902.CrossRefGoogle Scholar
Iuvone, P.M., Boatright, J.H. & Bloom, M.M. (1987). Dopamine mediates the light-evoked suppression of serotonin N-acetyltransferase activity in retina. Brain Research 418, 314–324.CrossRefGoogle ScholarPubMed
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
Kao, L.W.L. & Weisz, J. (1977). Release of gonadotrophin-releasing hormone (Gn-RH) from isolated, perfused medial basal hypothalamus by melatonin. Endocrinology 100, 1723–1730.Google Scholar
Laitinen, J.T. & Saavedra, J.M. (1990a). Characterization of melatonin receptors in the rat suprachiasmatic nuclei: modulation of affinity with cations and guanine nucleotides. Endocrinology 126, 2110–2115.CrossRefGoogle ScholarPubMed
Laitinen, J.T. & Saavedra, J.M. (1990b). The chick retinal melatonin receptor revisited: localization and modulation of agonist binding with guanine nucleotides. Brain Research 528, 349–352.CrossRefGoogle ScholarPubMed
Lerner, A.B., Case, J.D. & Heinzelman, R.V. (1959). Structure of melatonin. Journal of American Chemistry Society 81, 6084–6085.CrossRefGoogle Scholar
Linn, D.M., Blazynski, C., Redburn, D.A. & Massey, S.C. (1990). The release of acetylcholine from the rabbit retina: evidence for input via kainate receptors. Journal of Neuroscience 7, 319–329.Google Scholar
Lowenstein, P.R., Rosenstein, R. & Cardinali, D.P. (1985). Melatonin reverses pinealectomy-induced decrease of benzodiazepine binding in rat cerebral cortex. Neurochemistry International 7, 675–681.CrossRefGoogle ScholarPubMed
Marangos, P.J., Patel, J., Hirata, F., Sondhein, D., Paul, S.M., Skolnick, P. & Goodwin, F.K. (1981). Inhibition of diazepam binding by tryptophan derivatives including melatonin and its brain metabolite N-acetyl-5-methoxykynurenamine. Life Sciences 29, 256–267.CrossRefGoogle Scholar
Masland, R.H. & Livingston, C.J. (1976). Effect of stimulation with light on the synthesis and release of acetylcholine by an isolated mammalian retina. Journal of Neurophysiology 39, 1210–1219.CrossRefGoogle ScholarPubMed
Masland, R.H. & Livingston, C.J. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 83, 159–178.CrossRefGoogle ScholarPubMed
Masland, R.H., Mills, J.W. & Cassidy, C. (1984). The functions of acetylcholine in rabbit retina. Proceedings of the Royal Society B (London) 223, 121–129.Google Scholar
Massey, S.C. & Neal, M.J. (1979). The light-evoked release of acetylcholine from the rabbit retina in vivo and its inhibition by γ-aminobutyric acid. Journal of Neurochemistry 32, 1327–1329.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1982). A tonic γ-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. Journal of Neuroscience 2, 1633–1643.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1985). Light-evoked release of acetylcholine in response to a single flash: cholinergic amacrine cells receive ON and OFF input. Brain Research 328, 374–377.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 55–96.CrossRefGoogle ScholarPubMed
Morgan, M.W. & Kemp, C.W. (1980). A GABAergic influence on the light-induced increase in dopamine turnover in the dark-adapted rat retina in vivo. Journal of Neurochemistry 34, 1082–1087.CrossRefGoogle ScholarPubMed
Niles, L.P. (1984). Pharmacologic effects of melatonin on acute stress-induced changes in brain γ-aminobutyric acid levels and receptors. 14th Annual Meeting of Society of Neuroscience Abstract 329, 12.Google Scholar
Niles, L.P., Wong, Y., Mishra, R.K. & Brown, G.A. (1979). Melatonin receptors in brain. European Journal of Pharmacology 55, 219–220.CrossRefGoogle ScholarPubMed
Pang, S.F. & Allen, A.E. (1986). Extra-pineal melatonin in retina: its regulation and physiological function. Pineal Research Reviews 4, 55–95.Google Scholar
Pautler, E.L. & Hall, F.L. (1987). Movement of melatonin across the retinal pigment epithelium. Experimental Eye Research 45, 351–355.CrossRefGoogle ScholarPubMed
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retino-motor movements, I: Interaction of melatonin and dopamine in the control of cone length. Journal of General Physiology 86, 671–689.CrossRefGoogle Scholar
Quay, W.B. (1965). Retinal and pineal hydroxyindole-O-methyltransferase activity in vertebrates. Life Sciences 4, 983–329.CrossRefGoogle Scholar
Quay, W.R. & McLeod, R.W. (1968). Melatonin and photic stimulation of cone contraction in the retina of larval Xenopus lavis. Anatomical Records 160, 491.Google Scholar
Redburn, D.A. & Churchill, L. (1987). An indolamine system in photoreceptor cell terminals of the Long-Evans rat retina. Journal of Neuroscience 7, 319–329.CrossRefGoogle Scholar
Reppert, S.M., Weaver, D.R., Rivkees, S.A. & Stopa, E.G. (1988). Putative melatonin receptors in a human biological clock. Science 42, 78–81.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
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–119.Google Scholar
Tauchi, M. & Masland, R.H. (1985). Local order among the dendrites of an amacrine cell population. Journal of Neuroscience 5, 2494–2501.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1984). “Coronate” amacrine cells in the rabbit retina have the “Starburst” dendritic morphology. Proceedings of the Royal Society B (London) 220, 501–508.Google Scholar
Weaver, D.R., Rivkees, S.A. & Reppert, S.M. (1989). Localization and characterization of melatonin receptors in rodent brain by in vitro autoradiography. Journal of Neuroscience 9, 2581–2590.CrossRefGoogle ScholarPubMed
White, M.P. & Fisher, L.J. (1980). Melatonin effects on circadian rod outer segment shedding. Society of Neuroscience Abstracts 6, 344.Google Scholar
Wiechmann, A.F., Yang, X., Wu, S. & Hollyfield, J.G. (1988). Melatonin enhances horizontal cell sensitivity in salamander retina. Brain Research 453, 377–380.CrossRefGoogle ScholarPubMed
Wurtman, R.J. & Axelrod, J. (1965). The pineal gland. Scientific American 213, 50–60.CrossRefGoogle ScholarPubMed