Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T11:18:49.711Z Has data issue: false hasContentIssue false
  • English
  • Français

Dopamine and its agonists reduce a light-sensitive poor of cyclic AMP in mouse photoreceptors

Published online by Cambridge University Press:  02 June 2009

Adolph I. Cohen  and
Christine Blazynski
Adolph I. Cohen
Affiliation:
Departments of Ophthalmology and Visual Sciences, and Anatomy-Neurobiology, Washington University School of Medicine, St. Louis
Christine Blazynski
Affiliation:
Department of Ophthalmology and Visual Sciences, Anatomy-Neurobiology and Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis
Get access Rights & Permissions [Opens in a new window]

Abstract

The exposure to bright light of dark-adapted (DKA) mouse retinas incubated in the dark (DI) in IBMX-containing medium causes a marked loss of cyclic AMP. This light response also occurs if the medium contains 10 mM aspartate or cobaltous ion, agents believed to confine the effects of light to photoreceptors. Thus, the action of light in the presence of either of these agents defines a light-sensitive pool of cyclic AMP in photoreceptors. This pool could also be reduced or eliminated in DKA-DI retinas by nanomolar to micromolar levels of dopamine (if the medium contained SCH23390, a potent antagonist of Dl receptors), thus indicating an agonistic action of dopamine at D2 receptors. The D2 agonists LY171555 (EC50 10 nM) or (+)-3-PPP also reduced the cyclic AMP level in the dark. Of the D2 antagonists tested, the butyrophenone spiperone (in the presence of the 5HT-2 blocker ketanserin) countered the action of the D2 agonists but substituted benzamides were ineffective. Consistently, the D2 agonists had no effect on cyclic AMP levels of mutant retinas lacking photoreceptors (rd'rd), but reduced cyclic AMP in DKA-Dl glutamate-modified retinas which exhibit a major loss of inner retinal neurons without apparent loss of photoreceptors. The Dl antagonist SCH23390 only reduced cyclic AMP levels of DKA-DI retinas when cyclic AMP levels had been elevated by adding dopamine to the incubation medium.

Keywords

DopamineCyclic AMPPhotoreceptorsRetinaMouse
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 1 , January 1990 , pp. 43 - 52
Copyright
Copyright © Cambridge University Press 1990

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

Besharse, J. C., Dunis, D. A. & Burnside, B. (1982). Effects of cyclic adenosine 3′-,5′-monophosphate on photoreceptor disc shedding and retinomotor movement: inhibition of rod shedding and cone elongation. Journal of General Physiology 79, 75–790.Google ScholarPubMed
Brann, M. R. & Jelsema, C. L. (1985). Dopamine receptors on photoreceptor membranes couple to a GTP-binding protein which is sensitive to both pertussis and cholera toxin. Biochemical and Biophysical Research Communications 133, 222–227.CrossRefGoogle ScholarPubMed
Brann, M. R. & Young, W. S. III. (1986). Dopamine receptors are located on rods in bovine retina. Neuroscience Letters 69, 221–226.CrossRefGoogle ScholarPubMed
Bruinik, A., Dawis, S., Niemeyer, G. & Lichtensteiger, W. (1986). Catecholaminergic binding sites in cat retina, pigment epithelium, and choroid. Experimental Eye Research 43, 147–151.CrossRefGoogle Scholar
Carter-Dawson, L. D., LaVail, M. M. & Sidman, R. L. (1978). Differential effect of the rd mutation on rods and cones in the mouse retina. Investigative Ophthalmology and Visual Science 17, 489–498.Google ScholarPubMed
Carter-Dawson, L. D. & LaVail, M. M. (1979). Rods and cones in the mouse retina, I: Structural analysis using light and electron microscopy. Journal of Comparative Neurology 188, 245–262.CrossRefGoogle ScholarPubMed
Charuchinda, C., Supavilai, P., Karobath, M. & Palacios, J. M. (1987). Dopamine D2 receptors in rat brain: autoradiographic visualization using a high-affinity selective agonist ligand. Journal of neuroscience 7, 1352–1360.CrossRefGoogle ScholarPubMed
Cohen, A. I. (1989). Mouse photoreceptors contain D2 receptors that inhibit adenylate cyclase. Investigative Ophthalmology and Visual Science (Suppl.) 30, 319.Google Scholar
Cohen, A. I. (1967). An electron-microscopic study of the modification by monosodium glutamate of the retinas of normal and “rodless ” mice. American Journal of Anatomy 120, 319–356.CrossRefGoogle Scholar
Cohen, A. I., McDaniel, M. & Orr, H. (1973). Absolute levels of some free amino acids in normal and biologically fractionated retinas. Investigative Ophthalmology 12, 686–693.Google ScholarPubMed
Cohen, A. I. (1982). Increased levels of 3 ′5 ′-cyclic adenosine monophosphate induced by cobaltous ion, or 3-isobutylmethyl-xanthine in the incubated mouse retina: evidence concerning location and response to ions and light. Journal of Neurochemistry 38, 781–796.CrossRefGoogle ScholarPubMed
Cohen, A. I & Blazynski, C. (1987). Tryptamine and some related molecules can block the accumulation of a light-sensitive pool of cyclic AMP in the dark-adapted, dark-incubated mouse retina. Journal of Neurochemistry 48, 729–737.CrossRefGoogle ScholarPubMed
Dacheux, R. & Miller, R. F. (1976). Photoreceptor-bipolar cell transmission in the perfused eyecup of the mudpuppy. Science 191, 963–964.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1985). Dopamine inhibits forskolin- and 3-isobutyl- l -methylxanthine-induced retinomotor movements in isolated teleost retinas. Journal of Neurochemistry 44, 1753–1763.CrossRefGoogle Scholar
Dearry, A. & Burnside, B. (1986 a). 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.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986 b). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas; II: Modulation by γ-aminobutyric acid and serotonin. Journal of Neurochemistry 46, 1022–1031.CrossRefGoogle ScholarPubMed
Dearry, A., Miller, S. & Burnside, B. (1987). Dopamine induces light-adaptive retinomotor movements in bullfrog cones and RPE via D2 and Dl receptors. Society for Neuroscience Abstracts 13, 1298.Google Scholar
Dearry, A. & Burnside, B. (1988). Stimulation of distinct D2 dopaminergic and α2-adrenergic receptors induces light-adaptive pigment dispersion in teleost retinal pigment epithelium. Journal of Neurochemistry 51, 1516–1523.CrossRefGoogle Scholar
DeVries, G.W., Cohen, A.I., Hall, I.A. & Ferrendelli, J.A. (1978). Cyclic nucleotide levels in normal and biologically fractionated mouse retinas: effects of light and dark adaptation. Journal of Neurochemistry 31, 1345–1351.CrossRefGoogle ScholarPubMed
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 201, 7–26.Google Scholar
Dowling, J.E. & Ripps, H. (1972). Adaptation in skate photoreceptors. Journal of General Physiology 60, 698–719.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Watling, K.J. (1981). Dopaminergic mechanisms in the teleost retina, II: Factors affecting the accumulation of cyclic AMP in pieces of intact carp retina. Journal of Neurochemistry 36, 569–579.CrossRefGoogle ScholarPubMed
Drager, U.C. & Hubel, D.H. (1978). Studies of visual function and its decay in mice with hereditary retinal degeneration. Journal of Comparative Neurology 180, 85–114.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. & Hensler, J.G. (1986). Modulation of [3H\-dopamine released by different frequencies of stimulation from rabbit retina. British Journal of Pharmacology 88, 51–61.CrossRefGoogle ScholarPubMed
Ehinger, B. (1976). Biogenic monoamines as transmitters in the retina. In Transmitters in the Visual Process, ed. Bonting, S. L., pp. 145–163. London, England: Pergamon Press.CrossRefGoogle Scholar
Ehinger, B. & Nordenfelt, L. (1977). Destruction of retinal dopamine-containing neurons in rabbit and goldfish. Experimental Eye Research 24, 179–188.CrossRefGoogle ScholarPubMed
Evans, J.A., Hood, D.C. & Holtzman, E. (1978). Differential effects of cobalt ions on rod and cone activity in the isolated frog retina. Vision Research 18, 145–151.CrossRefGoogle ScholarPubMed
Fain, G.L., Quandt, F.N. & Gershenfeld, H.M. (1977). Calcium-dependent regenerative responses in rods. Nature 269, 707–709.CrossRefGoogle ScholarPubMed
Fain, G.L., Quandt, F.N., Bastian, B.L. & Gershenfeld, H.M. (1978). Contribution of a caesium-sensitive conductance increase to the rod photoresponse. Nature 272, 467–469.CrossRefGoogle Scholar
Ferrendelli, J.A. & Cohen, A.I. (1976). The effects of light and dark adaptation on the levels of cyclic nucleotides in retinas of mice heterozygous for a gene for photoreceptor dystrophy. Biochemical and Biophysical Research Communications 73, 421–427.CrossRefGoogle ScholarPubMed
Ferrendelli, J.A., DeVries, G.W., Cohen, A.I. & Lowry, O.H. (1980). Localization and roles of cyclic nucleotide systems in retina. Neurochemistry International 1, 311–326.CrossRefGoogle Scholar
Fisher, L.J. (1979). Interplexiform cell of the mouse retina. A Golgi demonstration. Investigative Ophthalmology and Visual Science 18,521–523.Google ScholarPubMed
Frucht, Y. & Melamed, E. (1984). The dopaminergic amacrine system and its response to light stimulation in rats with inherited retinal dystrophy. Experimental Eye Research 38, 391–398.CrossRefGoogle ScholarPubMed
Godley, B.F. & Wurtman, R.J. (1988). Release of endogenous dopamine from the superfused rabbit retina in vitro: effect of light stimulation. Brain Research 252, 393–395.CrossRefGoogle Scholar
Hamasaki, D. I., Trattler, W. B. & Hajek, A. S. (1986). Light on depresses and light off enhances the release of dopamine from the cat's retina. Neuroscience Letters 68, 112–116.CrossRefGoogle ScholarPubMed
Harper, J.F. & Brooker, G. (1975). Femtomole sensitive radioimmunoassay for cAMP and cGMP after 2′0 acetylation by acetic anhydride in aqueous solution. Journal of Cyclic Nucleotide Research 1, 207–218.Google Scholar
Hedden, W. L. & Dowling, J. E. (1978). The interplexiform cell, II: Effects of dopamine on goldfish retinal neurons. Proceedings of the Royal Society B 201, 27–55.Google Scholar
Hess, E.J. & Creese, I. (1987). Biochemical characterization of dopamine receptors. In Dopamine Receptors; Receptor Biochemistry and Methodology, Vol. 8, ed. Creese, I. & Fraser, C. M., pp. 1–27. New York: Alan R. Liss.Google Scholar
Imazu, Y., Kobayashi, K. & Shohmori, T. (1989). Comparative study of sulpiride and haloperidol on dopamine turnover in the rat brain. Neurochemical Research 14, 459–464.CrossRefGoogle ScholarPubMed
Iuvone, P.M., Galli, C.L., Garrison-Gund, C.K. & Neff, N.H. (1978). Light stimulates tyrosine hydroxylase and dopamine synthesis in retinal amacrine cells. Science 202, 901–902.CrossRefGoogle Scholar
Iuvone, P.M. (1985). Evidence for a dopamine receptor in retina that decreases cyclic AMP accumulation and serotonin N-acetyltransferase activity. Investigative Ophthalmology and Visual Science (Suppl.) 26, 279.Google Scholar
Iuvone, P.M., Avendano, G. & Adler, R. (1989). Serotonin N-acetyltransferase in photoreceptor-enriched retinal cell cultures, 1: Effects of cyclic AMP and dopamine. Investigative Ophthalmology and Visual Science (Suppl.) 30, 123.Google Scholar
Jelsema, C.L., Ishihara, Y. & Brann, M.R. (1985). Dopamine D-2 receptors and light couple to cyclic GMP-phosphodiesterase, phospholipase A2, and phospholipase C in rod outer segment membranes. Society for Neuroscience Abstracts 11, 312.Google Scholar
Jensen, R.J. & Daw, N.W. (1984). Effects of dopamine antagonists on receptive fields of brisk cells and directionally selective cells in the rabbit retina. Journal of Neuroscience 4, 2972–2985.CrossRefGoogle ScholarPubMed
Kamp, C. W. (1985). The dopamine system of the retina. In Retinal Transmitters and Modulators: Models for the Brain, Vol. II, ed. Morgan, W.W., pp. 1–31. Boca Raton, Florida: CRC Press.Google Scholar
Kaneko, A. & Tachibana, M. (1986). Blocking effects of cobalt and related ions on the γ-aminobutyric acid-induced current in turtle retinal cones. Journal of Physiology 373, 463–479.CrossRefGoogle ScholarPubMed
Kramer, S.G. (1971). Dopamine: a retinal neurotransmitter, I: Retinal uptake, storage, and light-stimulated release of [H3\-dopamine in vivo. Investigative Ophthalmology 10, 438–452.Google 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
Makman, M.H., Brown, J.H. & Mishra, R.K. (1975). Cyclic AMP in retina and caudate nucleus: influence of dopamine and other agents. Advances in Cyclic Nucleotide Research 5, 661–679.Google ScholarPubMed
Mitzel, D.L., Hall, I.A., DeVries, G.W., Cohen, A.I. & Ferrendelli, J.A. (1978).Comparison of cyclic nucleotide and energy metabolism of intact mouse retina in situ and in vitro. Experimental Eye Research 27, 27–37.CrossRefGoogle ScholarPubMed
Negishi, K. & Drujan, B.D. (1979). Effect of catecholamines and related compounds on horizontal cell in the fish retina. Journal of Neuroscience Research 4, 311–334.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, S. (1983). A GABA antagonist, bicuculline, exerts its uncoupling action on external horizontal cells through dopamine cells in carp retina. Neuroscience Letters 37, 261–266.CrossRefGoogle ScholarPubMed
Nguyen-Legros, J., Simon, A. & Moussafi, F. (1989). Dopaminergic terminals from interplexiform cells reach the outer nuclear layer in rat and monkey retinas. Investigative Opthalmology and Visual Science (Suppl.) 30, 120.Google Scholar
O'Connor, P.M., Zucker, C.L. & Dowling, J.E. (1987). Regulation of dopamine release from interplexiform cell processes in the outer plexiform layer of the carp retina. Journal of Neurochemistry 49, 916–920.CrossRefGoogle ScholarPubMed
Parkinson, D. & Rando, R.R. (1983). Effects of light on dopamine metabolism in the chick retina. Journal of Neurochemistry 40, 39–46.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3′:5 ′-monophosphate in horizontal cells of turtle retina. Journal of Neuroscience 4, 2477–2488.CrossRefGoogle ScholarPubMed
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movements, I: Interaction of melatonin and dopamine in control of cone length. Journal of General Physiology 86, 671–689.CrossRefGoogle ScholarPubMed
Qu, Z.-X., Neff, N.H., Fertel, R. & Hadjiconstantinou, M. (1987). Activation of retinal D-2 receptors inhibits adenylate cyclase activity. Federation Proceedings (Abstract) 46, 392.Google Scholar
Ripps, H., Shakib, M. & MacDonald, E.D. (1976). Peroxidase uptake by photoreceptor terminals of the skate retina. Journal of Cell Biology 70, 86–96.CrossRefGoogle ScholarPubMed
Ross, D., Cohen, A.I. & McDougal, D.B. Jr (1975). Choline acetyltransferase and acetylcholine esterase activities in normal and biologically fractionated retinas. Investigative Ophthalmology 14, 756–761.Google ScholarPubMed
Seeman, P., Grigoriadis, D.E. & Niznik, H.B. (1986). Selectivity of agonists and antagonists at D2 dopamine receptors compared to D1 and S2 receptors. Drug Development Research 9, 63–69.CrossRefGoogle Scholar
Seeman, P. & Grigoriadis, D. (1987). Dopamine receptors in brain and periphery. Neurochemistry International 10, 1–25.CrossRefGoogle ScholarPubMed
Schwartz, E.A. (1986). Synaptic transmission in amphibian retinae during conditions unfavorable for calcium entry into presynaptic terminals. Journal of Physiology 376, 411–428.CrossRefGoogle ScholarPubMed
Sillman, A.J., Ito, H. & Tomita, T. (1969). Studies on the mass potential of the isolated frog retina, I: General properties of the response. Vision Research 9, 1435–1442.CrossRefGoogle ScholarPubMed
Steiner, A.L., Parker, C.H. & Kipnis, D. M. (1972). Radioimmunoassay for cyclic nucleotides. Journal of Biological Chemistry 247, 1106–1113.CrossRefGoogle ScholarPubMed
Umino, O. & Watanabe, K. (1987). Decline of blocking effect of cobalt ions on transmission from photoreceptors to horizontal cells during its prolonged application. Neuroscience Letters 82, 291–296.CrossRefGoogle ScholarPubMed
Vasse, M., Protais, P., Costentin, J. & Schwartz, J. -C. (1985). Unexpected potentiation by discriminant benzamide derivatives of stereotyped behaviors elicited by dopamine agonists in mice. Naunyn-Schmiedeberg's Archives of Pharmacology 329, 108–116.CrossRefGoogle ScholarPubMed
Versaux-Botteri, C., Nguyen-Legros, J., Vigny, A. & Raoux, N. (1984). Morphology, density, and distribution of tyrosine hydroxylase-like immunoreactive cells in the retina of mice. Brain Research 301, 192–197.CrossRefGoogle ScholarPubMed
Witkovsky, P., Stone, S. & Besharse, J. (1987). Dopamine mimics light adaptation in horizontal cells of Xenopus retina. Society for Neuroscience Abstracts 13, 24.Google Scholar
Witkovsky, P., Stone, S. & Besharse, J. (1988). Dopamine modifies the balance of rod and cone inputs to horizontal cells of the Xenopus retina. Brain Research 449, 332–336.CrossRefGoogle ScholarPubMed
Zawilska, J. & Iuvone, P.M. (1989). D2-dopamine receptor activation decreases melatonin content and serotonin N-acetyltransferase activity of chicken retina. Investigative Ophthalmology and Visual Science (Suppl.) 30, 123.Google Scholar