Skip to main content
NCBI home page
British Journal of Pharmacology logoLink to British Journal of Pharmacology
. 1994 Nov;113(3):789–794. doi: 10.1111/j.1476-5381.1994.tb17062.x

Enhancement of retinal acetylcholine release by DAMGO: possibly a direct opioid receptor-mediated excitatory effect.

M J Neal 1, S J Paterson 1, J R Cunningham 1
PMCID: PMC1510421  PMID: 7858868

Abstract

1. An eye-cup preparation in anaesthetized rabbits was used to examine opioid modulation of acetylcholine (ACh) release from cholinergic neurones in the retina. 2. The mu-opioid receptor agonist, [D-Ala2, MePhe4, Gly-ol5]-enkephalin (DAMGO), when applied locally to the retina at concentrations between 1-30 microM significantly increased the light-evoked release of ACh. The effect of DAMGO was completely blocked by the selective mu-receptor antagonist CTOP but the kappa-receptor antagonist nor-binaltorphimine (norBNI) did not affect the action of DAMGO on ACh release indicating that the opioid produced its effect by activation of mu-receptors (the rabbit retina has negligible delta-receptors). 3. Blockade with bicuculline and strychnine of GABAergic and glycinergic inputs to the cholinergic neurones did not affect the action of DAMGO on ACh release. Also DAMGO did not reduce the potassium-evoked release of either GABA or glycine from rat isolated retinas. 4. Exposure of the rabbit retina to a combination of an A1-adenosine receptor antagonist, 8-cyclopentyl-1,3 dipropylxanthine (DPCPX), and adenosine deaminase did not affect the enhancing action of DAMGO on the light-evoked release of ACh. 5. When the retina in the rabbit eye-cup was exposed to kainate, the release of ACh was increased by approximately three times the resting release. In the presence of DAMGO the kainate-evoked release of ACh was enhanced by 44%. 6. These experiments show that activation of mu-opioid receptors by DAMGO increases the release of ACh elicited by physiological stimulation (flickering light).(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF
789

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschuler R. A., Mosinger J. L., Hoffman D. W., Parakkal M. H. Immunocytochemical localization of enkephalin-like immunoreactivity in the retina of the guinea pig. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2398–2400. doi: 10.1073/pnas.79.7.2398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arenas E., Alberch J., Pérez-Navarro E., Solsona C., Marsal J. Neostriatal dopaminergic terminals prevent the GABAergic involvement in the mu- and delta-opioid inhibition of KCl-evoked endogenous acetylcholine release. Brain Res. 1991 Aug 16;556(2):349–352. doi: 10.1016/0006-8993(91)90329-t. [DOI] [PubMed] [Google Scholar]
  3. Blazynski C. Displaced cholinergic, GABAergic amacrine cells in the rabbit retina also contain adenosine. Vis Neurosci. 1989 Nov;3(5):425–431. doi: 10.1017/s0952523800005927. [DOI] [PubMed] [Google Scholar]
  4. Blazynski C., Perez M. T. Adenosine in vertebrate retina: localization, receptor characterization, and function. Cell Mol Neurobiol. 1991 Oct;11(5):463–484. doi: 10.1007/BF00734810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blazynski C., Woods C., Mathews G. C. Evidence for the action of endogenous adenosine in the rabbit retina: modulation of the light-evoked release of acetylcholine. J Neurochem. 1992 Feb;58(2):761–767. doi: 10.1111/j.1471-4159.1992.tb09783.x. [DOI] [PubMed] [Google Scholar]
  6. Braas K. M., Zarbin M. A., Snyder S. H. Endogenous adenosine and adenosine receptors localized to ganglion cells of the retina. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3906–3910. doi: 10.1073/pnas.84.11.3906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brecha N., Johnson D., Peichl L., Wässle H. Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6187–6191. doi: 10.1073/pnas.85.16.6187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crain S. M., Shen K. F. Opioids can evoke direct receptor-mediated excitatory effects on sensory neurons. Trends Pharmacol Sci. 1990 Feb;11(2):77–81. doi: 10.1016/0165-6147(90)90322-y. [DOI] [PubMed] [Google Scholar]
  9. Cunningham J. R., Dawson C., Neal M. J. Evidence for a cholinergic inhibitory feed-back mechanism in the rabbit retina. J Physiol. 1983 Jul;340:455–468. doi: 10.1113/jphysiol.1983.sp014773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cunningham J. R., Neal M. J. Effect of excitatory amino acids and analogues on [3H]acetylcholine release from amacrine cells of the rabbit retina. J Physiol. 1985 Sep;366:47–62. doi: 10.1113/jphysiol.1985.sp015784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cunningham J. R., Neal M. J. Effect of gamma-aminobutyric acid agonists, glycine, taurine and neuropeptides on acetylcholine release from the rabbit retina. J Physiol. 1983 Mar;336:563–577. doi: 10.1113/jphysiol.1983.sp014598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Djamgoz M. B., Stell W. K., Chin C. A., Lam D. M. An opiate system in the goldfish retina. Nature. 1981 Aug 13;292(5824):620–623. doi: 10.1038/292620a0. [DOI] [PubMed] [Google Scholar]
  13. Ehinger B., Lindberg B. Light-evoked release of glycine from the retina. Nature. 1974 Oct 25;251(5477):727–728. doi: 10.1038/251727a0. [DOI] [PubMed] [Google Scholar]
  14. Famiglietti E. V., Jr On and off pathways through amacrine cells in mammalian retina: the synaptic connections of "starburst" amacrine cells. Vision Res. 1983;23(11):1265–1279. doi: 10.1016/0042-6989(83)90102-5. [DOI] [PubMed] [Google Scholar]
  15. Famiglietti E. V. Synaptic organization of starburst amacrine cells in rabbit retina: analysis of serial thin sections by electron microscopy and graphic reconstruction. J Comp Neurol. 1991 Jul 1;309(1):40–70. doi: 10.1002/cne.903090105. [DOI] [PubMed] [Google Scholar]
  16. Ferro E. S., Hamassaki D. E., Camargo A. C., Britto L. R. Endo-oligopeptidase A, a putative enkephalin-generating enzyme, in the vertebrate retina. J Neurochem. 1991 Nov;57(5):1643–1649. doi: 10.1111/j.1471-4159.1991.tb06363.x. [DOI] [PubMed] [Google Scholar]
  17. Jardon B., Bonaventure N., Scherrer E. Possible involvement of cholinergic and glycinergic amacrine cells in the inhibition exerted by the ON retinal channel on the OFF retinal channel. Eur J Pharmacol. 1992 Jan 14;210(2):201–207. doi: 10.1016/0014-2999(92)90672-q. [DOI] [PubMed] [Google Scholar]
  18. Lapchak P. A., Araujo D. M., Collier B. Regulation of endogenous acetylcholine release from mammalian brain slices by opiate receptors: hippocampus, striatum and cerebral cortex of guinea-pig and rat. Neuroscience. 1989;31(2):313–325. doi: 10.1016/0306-4522(89)90376-x. [DOI] [PubMed] [Google Scholar]
  19. Leslie F. M. Methods used for the study of opioid receptors. Pharmacol Rev. 1987 Sep;39(3):197–249. [PubMed] [Google Scholar]
  20. Linn D. M., Blazynski C., Redburn D. A., Massey S. C. Acetylcholine release from the rabbit retina mediated by kainate receptors. J Neurosci. 1991 Jan;11(1):111–122. doi: 10.1523/JNEUROSCI.11-01-00111.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Linn D. M., Massey S. C. GABA inhibits ACh release from the rabbit retina: a direct effect or feedback to bipolar cells? Vis Neurosci. 1992 Feb;8(2):97–106. doi: 10.1017/s0952523800009263. [DOI] [PubMed] [Google Scholar]
  22. Masland R. H., Mills J. W. Autoradiographic identification of acetylcholine in the rabbit retina. J Cell Biol. 1979 Oct;83(1):159–178. doi: 10.1083/jcb.83.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Massey S. C., Neal M. J. The light evoked release of acetylcholine from the rabbit retina iN vivo and its inhibition by gamma-aminobutyric acid. J Neurochem. 1979 Apr;32(4):1327–1329. doi: 10.1111/j.1471-4159.1979.tb11062.x. [DOI] [PubMed] [Google Scholar]
  24. Massey S. C., Redburn D. A. A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina. J Neurosci. 1982 Nov;2(11):1633–1643. doi: 10.1523/JNEUROSCI.02-11-01633.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mulder A. H., Burger D. M., Wardeh G., Hogenboom F., Frankhuyzen A. L. Pharmacological profile of various kappa-agonists at kappa-, mu- and delta-opioid receptors mediating presynaptic inhibition of neurotransmitter release in the rat brain. Br J Pharmacol. 1991 Feb;102(2):518–522. doi: 10.1111/j.1476-5381.1991.tb12203.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Neal M. J., Shah M. A. Baclofen and phaclofen modulate GABA release from slices of rat cerebral cortex and spinal cord but not from retina. Br J Pharmacol. 1989 Sep;98(1):105–112. doi: 10.1111/j.1476-5381.1989.tb16869.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Oron L., Sarne Y., Michaelson D. M. Effect of opioid peptides on electrically evoked acetylcholine release from Torpedo electromotor neurons. Neurosci Lett. 1991 Apr 29;125(2):231–234. doi: 10.1016/0304-3940(91)90036-s. [DOI] [PubMed] [Google Scholar]
  28. PATON W. D. The action of morphine and related substances on contraction and on acetylcholine output of coaxially stimulated guinea-pig ileum. Br J Pharmacol Chemother. 1957 Mar;12(1):119–127. doi: 10.1111/j.1476-5381.1957.tb01373.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Perez M. T., Ehinger B. E., Lindström K., Fredholm B. B. Release of endogenous and radioactive purines from the rabbit retina. Brain Res. 1986 Nov 19;398(1):106–112. doi: 10.1016/0006-8993(86)91255-2. [DOI] [PubMed] [Google Scholar]
  30. Ruzicka B. B., Jhamandas K. The K(+)-evoked release of [3H]acetylcholine from slices of rat globus pallidus: modulation by delta-opioid receptors. Can J Physiol Pharmacol. 1991 Mar;69(3):414–418. doi: 10.1139/y91-063. [DOI] [PubMed] [Google Scholar]
  31. Senba E., Daddona P. E., Nagy J. I. Immunohistochemical localization of adenosine deaminase in the retina of the rat. Brain Res Bull. 1986 Aug;17(2):209–217. doi: 10.1016/0361-9230(86)90117-6. [DOI] [PubMed] [Google Scholar]
  32. Watt C. B., Su Y. Y., Lam D. M. Interactions between enkephalin and GABA in avian retina. Nature. 1984 Oct 25;311(5988):761–763. doi: 10.1038/311761a0. [DOI] [PubMed] [Google Scholar]
  33. Wichmann T., Starke K. Modulation by muscarine and opioid receptors of acetylcholine release in slices from striato-striatal grafts in the rat. Brain Res. 1990 Mar 5;510(2):296–302. doi: 10.1016/0006-8993(90)91380-y. [DOI] [PubMed] [Google Scholar]

Articles from British Journal of Pharmacology are provided here courtesy of The British Pharmacological Society

RESOURCES