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Regulation of endogenous dopamine release in amphibian retina by gamma-aminobutyric acid and glycine

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

Endogenous dopamine release in the retina of the African clawed frog (Xenopus laevis) increases in light and decreases in darkness. The roles of the inhibitory amino acid transmitters gamma-aminobutyric acid (GABA) and glycine in regulating this light/dark difference in dopamine release were explored in the present study. Exogenous GABA, the GABA-A receptor agonist muscimol, the GABA-B receptor agonist baclofen, and the GABA-C receptor agonist cis-aminocrotonic acid (CACA) suppressed light-evoked dopamine overflow from eyecups. The effects of GABA-A and -B receptor agonists were selectively reversed by their respective receptor-specific antagonists, whereas the effect of CACA was reversed by the competitive GABA-A receptor antagonist bicuculline. The benzodiazepine diazepam enhanced the effect of muscimol on light-evoked dopamine release. Both GABA-A and -B receptor antagonists stimulated dopamine release in light or darkness. Bicuculline was more potent in light than in darkness. These data suggest that retinal dopaminergic neurons are inhibited by GABA-A and -B receptor activation in both light and darkness but that GABA-mediated inhibitory tone may be greater in darkness than in light.

Exogenous glycine inhibited light-stimulated dopamine release in a concentration-dependent and strychnine-sensitive manner. However, strychnine alone did not increase dopamine release in light or darkness, nor did it augment bicuculline-stimulated release in darkness. Additionally, both strychnine and 7-chlorokynurenate, an antagonist of the strychnine-insensitive glycine-binding site of the N-methyl-D-aspartate subtype of glutamate receptor, suppressed light-evoked dopamine release. Thus, the role of endogenous glycine in the regulation of dopamine release remains unclear.

Keywords

DopamineRetinaGamma-aminobutyric acidGlycine
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 5 , September 1994 , pp. 1003 - 1012
Copyright
Copyright © Cambridge University Press 1994

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References

Adolph, A., Dowling, J.E. & Ehinger, B. (1980). Monoaminergic neurons of the mudpuppy retina. Cell and Tissue Research 210, 269–282.CrossRefGoogle ScholarPubMed
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. (1992). Critique: Is dopamine a light-adaptive or dark-adaptive modulator in retina? Neurochemistry International 20, 193–199.CrossRefGoogle ScholarPubMed
Besharse, J.C., Iuvone, P.M. & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: A role for post-receptoral neurons. In Progress in Retinal Research, ed. Osborne, N. & Chader, G.J., pp. 21–61. Oxford, England: Pergamon Press.Google Scholar
Boatright, J.H., Hoel, M.J. & Iuvone, P.M. (1987). Evidence that light stimulates endogenous dopamine release and metabolism in retinas of frogs (Xenopus laevis). Society of Neurosciences Abstract 28, 1298.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. & Iuvone, P.M. (1990). Regulation of dopamine release from frog retina by GABA agonists and antagonists. Investigative Ophthalmology and Visual Science (Abstract) 31, 334.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. & 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). GABA and the regulation of serotonin N-acetyltransferase activity in amphibian retina –II. The role of dopamine. Neurochemistry International 15, 549–554.CrossRefGoogle ScholarPubMed
Buelow, N.F., Kelly, M.F. & Barlow, R.B. (1992). Dopamine: A cir-cadian modulator of rod-cone dominance in quail? Investigative Ophthalmology and Visual Science (Abstract) 33, 3572.Google Scholar
Cahill, G.M. & Besharse, J.C. (1991). Resetting the circadian clock in cultured Xenopus eyecups: Regulation of retinal melatonin rhythms by light and D2 dopamine receptors. Journal of Neurosciences 11, 2959–2971.CrossRefGoogle ScholarPubMed
Cutting, G.R., Lu, L., O'Hara, B.F., Kasch, L.M., Montrose-Rafizadeh, C., Donovan, D.M., Shimada, S., Antonarakis, S.E., Guggino, W.B., Uhl, G.R. & Kazazian, H.H. Jr., (1991). Cloning of the gamma-aminobutyric acid (GABA). rho1 cDNA: A GABA receptor subunit highly expressed in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2673–2677.CrossRefGoogle Scholar
Dearry, A. & Burnside, B. (1986). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas. I. Induction of cone contraction is mediated by D2 receptors. Journal of Neurochemistry 46, 1006–1021.Google Scholar
Dearry, A. & Burnside, B. (1989). Light-induced dopamine release from teleost retinas acts as a light-adaptive signal to the retinal pigment epithelium. Journal of Neurochemistry 53, 870–878.CrossRefGoogle Scholar
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
Delgado, M.J., Alonso-Gomez, A.L., Gancedo, B., De Pedro, N., Valenciano, A.I. & Alonso-Bedate, M. (1993). Serotonin N-acetyltransferase (NAT) activity and melatonin levels in the frog retina are not correlated during the seasonal cycle. General and Comparative Endocrinology 92, 143–150.CrossRefGoogle Scholar
Djamgoz, M.B.A. & Wagner, H.-J. (1992). Localization and function of dopamine in the adult vertebrate retina. Neurochemistry International 20, 139–192.Google Scholar
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system. I. Synapses of the dopaminergic neurons of the goldfish retina. Proceedings of the Royal Society B (London) 201, 7–26.Google Scholar
Drew, C.A., Johnston, G.A.R. & Weatherby, R.P. (1984). Bicuculline-insensitive GABA receptors: Studies on the binding of (−)-baclofen to rat cerebellar membranes. Neuroscience Letters 52, 317–321.Google Scholar
Feigenspan, A., Wassle, H. & Bormann, J. (1993). Pharmacology of GABA receptor Cl− channels in rat retinal bipolar cells. Nature 361, 159–162.CrossRefGoogle ScholarPubMed
Friedman, D.L. & Redburn, D.A. (1990). Evidence for functionally distinct subclasses of gamma-aminobutyric acid receptors in rabbit retina. Journal of Neurochemistry 55, 1189–1199.Google Scholar
Frucht, Y., Vidauri, J. & Melamed, E. (1982). Light activation of dopaminergic neurons in rat retina is mediated through photoreceptors. Brain Research 249, 153–156.Google Scholar
Gibson, C.J. (1990). A simple perfusion system for measuring endogenous retinal dopamine release. Journal of Neuroscience Methods 32, 75–79.Google Scholar
Godley, B.F. & Wurtman, R.J. (1988). Release of endogenous dopamine from the superfused rabbit retina in vitro: Effect of light stimulation. Brain Research 452, 393–395.CrossRefGoogle ScholarPubMed
Graham, L.T. Jr., Baxter, C.F. & Lolley, R.N. (1970). In vivo influence of light or darkness on the GABA system in the retina of the frog (Rana pipiens). Brain Research 20, 379–388.Google Scholar
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
Ishita, S., Negishi, K., Teranishi, T., Shimada, Y. & Kato, S. (1988). GABAergic inhibition on dopamine cells of the fish retina: A [3H]dopamine release study with isolated cell fractions. Journal of Neurochemistry 50, 1–6.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. (1986). Neurotransmitters and neuromodulators in the retina: Regulation, interactions and cellular effects. In The Retina, A Model for Cell Biology Studies, Part II, ed. Adler, R. & Farber, D., pp. 1–72. Orlando, Florida: Academic Press.Google 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
Johnson, J.W. & Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurones. Nature 325, 325–327.CrossRefGoogle Scholar
Johnston, G.A.R. (1986). In Benzodiazepine/GABA Receptors and Chloride Channels. Receptor Biochemistry and Methodology. New York: Liss, p. 57.Google Scholar
Kamp, C.W. & Morgan, W.W. (1981). GABA antagonists enhance dopamine turnover in the rat retina. European Journal of Pharmacology 69, 273–279.CrossRefGoogle ScholarPubMed
Kamp, C.W. & Morgan, W.W. (1982). Benzodiazepines suppress the light response of retinal dopaminergic neurones in vivo. European Journal of Pharmacology 77, 343–346.Google Scholar
Kazula, A., Nowak, J.Z. & Iuvone, P.M. (1993). Regulation of melatonin and dopamine biosynthesis in chick retina: The role of GABA. Visual Neuroscience 10, 621–629.CrossRefGoogle ScholarPubMed
Kirsch, M. & Wagner, H.-J. (1989). Release pattern of endogenous dopamine in teleost retinae during light adaptation and pharmacological stimulation. Vision Research 29, 147–154.Google Scholar
Kolbinger, W., Kohler, K., Oetting, H. & Weiler, R. (1990). Endogenous dopamine and cyclic events in the fish retina, I: HPLC assay of total content, release, and metabolic turnover during different light/dark cycles. Visual Neuroscience 5, 143–149.CrossRefGoogle ScholarPubMed
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
Mao, C.C., Guidotti, A. & Costa, E. (1975). Evidence for an involvement of GABA in the mediation of the cerebellar cGMP decrease and the anticonvulsant action diazepam. Nauyn Schmiedeberg's Archives of Pharmacology 289, 369–378.Google Scholar
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.Google Scholar
Mariani, A.P., Cosenza, M.D. & Barker, J.L. (1987). GABAergic synapses and benzodiazepine receptors are not identically distributed in the primate retina. Brain Research 415, 153–157.Google Scholar
Marshburn, P.B. & Iuvone, P.M. (1981). The role of GABA in the regulation of the dopamine tyrosine hydroxylase-containing neurons of the rat retina. Brain Research 214, 335–347.CrossRefGoogle ScholarPubMed
Matsumoto, R.R. (1989). GABA receptors: Are cellular differences reflected in function? Brain Research Reviews 14, 203–225.CrossRefGoogle ScholarPubMed
Morgan, W.W. & Kamp, C.W. (1983). Effect of strychnine and of bicuculline on dopamine synthesis in retinas of dark-maintained rats. Brain Research 278, 362–365.Google Scholar
Naarendorp, F. & Sieving, P.A. (1991). The scotopic threshold of the cat ERG is suppressed selectively by GABA and glycine. Vision Research 31, 1–15.CrossRefGoogle ScholarPubMed
O'Connor, P., Dorison, S.J., Watling, K. & Dowling, J.E. (1986). Factors influencing the release of 3H-dopamine from perfused carp retina. Journal of Neurosciences 6, 1857–1865.Google Scholar
O'Connor, P., Zucker, C. & Dowling, J. (1987). Regulation of dopamine release from interplexiform cell processes in the outer plexi-form layer of the carp retina. Journal of Neurochemistry 49, 916–920.Google Scholar
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movements. I. Interaction of melatonin and dopamine in the control of cone length. Journal of General Physiology 86, 671–689.Google Scholar
Pierce, M.E. & Besharse, J.C. (1986). Melatonin and dopamine interactions in the regulation of rhythmic photoreceptor metabolism. In Pineal and Retinal Relationships, ed. O'Brien, P. & Klein, D.C., pp. 219–237. New York: Academic Press.Google Scholar
Pierce, M.E. & Besharse, J.C. (1987). Melatonin and rhythmic photoreceptor metabolism: Melatonin-induced cone elongation is blocked by high light intensity. Brain Research 405, 400–404.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.Google Scholar
Polenzani, L., Woodward, R.M. & Miledi, R. (1991). Expression of mammalian gamma-aminobutyric acid receptors with distinct pharmacology in Xenopus oocytes. Proceedings of the National Academy of Sciences of the U.S.A. 88, 4318–4322.Google Scholar
Qian, H. & Dowling, J.E. (1993). Novel GABA responses from rod-driven retinal horizontal cells. Nature 361, 162–164.CrossRefGoogle ScholarPubMed
Rayborn, M.E., Sarthy, P.V., Lam, D.M.K. & Hollyfield, J.G. (1981). The emergence, localization and maturation of neurotrans-mitter systems during development of the retina of Xenopus laevis. II. Glycine. Journal of Comparative Neurology 195, 585–593.Google Scholar
Robbins, J. & Ikeda, H. (1989). Benzodiazepines and the mammalian retina. III. Postnatal development. Brain Research 479, 334–338.CrossRefGoogle ScholarPubMed
Rubim, N. M., Boatright, J.H. & Iuvone, P.M. (1992). NMDA receptors regulate dopamine release in amphibian retina. Investigative Ophthalmology and Visual Science (Abstract) 34, 1063.Google Scholar
Sarthy, P.V., Rayborn, M.E., Hollyfield, J.G. & Lam, D.M.K. (1981). The emergence, localization, and maturation of neurotrans-mitter systems during development of the retina in Xenopus laevis. III. Dopamine. Journal of Comparative Neurology 195, 595–602.CrossRefGoogle Scholar
Schütte, M. & Witkovsky, P. (1991). Dopaminergic interplexiform cells and centrifugal fibers in the Xenopus retina. Journal of Neurocytology 20, 195–207.Google Scholar
Sivilotti, L. & Nistri, A. (1989). Pharmacology of a novel effect of gamma-aminobutyric acid on the frog tectum in vitro. European Journal of Pharmacology 164, 205–212.CrossRefGoogle ScholarPubMed
Smiley, J.F. & Basinger, S.F. (1988). Somatostatin-like immunoreactivity and glycine high-affinity uptake colocalize to an interplexiform cell of the Xenopus laevis retina. Journal of Comparative Neurology 274, 608–618.Google Scholar
Smiley, J.F. & Basinger, S.F. (1990). Glycine stimulates calcium-independent release of 3H-GABA from isolated retinas of Xenopus laevis. Visual Neuroscience 4, 337–348.Google Scholar
Smiley, J.F. & Yazulla, S. (1990). Glycinergic contacts in the outer plexiform layer of the Xenopus laevis retina characterized by antibodies to glycine, GABA, and glycine receptors. Journal of Comparative Neurology 299, 375–388.Google Scholar
Stone, S. & Witkovsky, P. (1984). The actions of gamma-aminobutyric acid, glycine and their antagonists upon horizontal cells of the Xenopus retina. Journal of Physiology 353, 249–264.Google Scholar
Sugden, A.L., Sugden, D. & Klein, D.C. (1986). Essential role of calcium influx in the adrenergic regulation of cAMP and cGMP in rat pinealocytes. Journal of Biological Chemistry 261, 11608–11612.CrossRefGoogle ScholarPubMed
Sugden, A.L., Sugden, D. & Klein, D.C. (1987). a1-Adrenoceptor activation elevates cytosolic calcium in rat pinealocytes by increasing net influx. Journal of Biological Chemistry 262, 741–745.Google Scholar
Uhl, G.R., Cutting, G.R., Shimada, S., O'Hara, B., Donovan, D. & Kitayama, S. (1991). GABA C receptors?: Unusual pharmaco-logic profile and homo-oligomeric expression of retina-enriched receptor GABA rho 1. Society for Neuroscience Abstracts 17, 76.Google Scholar
Weiler, R., Kolbinger, W. & Kohler, K. (1989). Reduced light responsiveness of the cone pathway during prolonged darkness does not result from an increase of dopaminergic activity in the fish retina. Neuroscience Letters 99, 214–218.Google Scholar
Witkovsky, P. & Dearry, A. (1991). Functional role of dopamine in the vertebrate retina. In Progress in Retinal Research, Vol. 11, ed. Osborne, N. & Chader, G.J., pp. 248–292. Oxford, England: Pergamon Press.Google Scholar
Witkovsky, P., Nicholson, C., Rice, M.E., Bohmaker, K. & Meller, E. (1993). Extracellular dopamine concentration in the retina of the clawed frog, Xenopus laevis. Proceedings of the National Academy of Sciences of the U.S.A. 90, 5667–5671.CrossRefGoogle ScholarPubMed
Witkovsky, P., Stone, S. & Besharse, J.C. (1988). The effects of dopa-mine and related ligands on photoreceptor to horizontal cell transfer in the Xenopus retina. Biomedical Research (Suppl. 2) 9, 93–107.Google Scholar
Witkovsky, P. & Shi, X.-P. (1990). Slow light and dark adaptation of horizontal cells in the Xenopus retina: A role for endogenous dopamine. Visual Neuroscience 5, 405–413.Google Scholar
Yazulla, S. & Zucker, C.L. (1988). Synaptic organization of dopa-minergic interplexiform cells in the goldfish retina. Visual Neuroscience 1, 13–29.Google Scholar
Zarbin, M.A., Wamsley, J.K., Palacios, J.M. & Kuhar, M.J. (1986). Autoradiographic localization of high affinity GABA, benzodiaz-epine, dopaminergic, adrenergic and muscarinic receptors in the rat, monkey, and human retina. Brain Research 374, 75–92.Google Scholar
Zawilska, J. & Iuvone, P.M. (1989). Catecholamine receptors regulating serotonin N-acetyltransferase activity and melatonin content of chicken retina and pineal gland: D2-doparaine receptors in retina and alpha-2 adrenergic receptors in pineal gland. Journal of Pharmacology and Experimental Therapeutics 250, 86–92.Google Scholar