Summary
-
1.
Enkephalin-like immunoreactive amacrine cells were visualized using the highly sensitive avidin-biotin method. The somas of these cells were situated in the inner nuclear and ganglion cell layers. Enkephalin-stained processes were observed in layers 1, 3, and 5 of the inner plexiform layer.
-
2.
The biosynthesis of sulfur-containing compounds in the goldfish retina was studied by means of a pulse-chase incubation with35S-methionine. A35S-labeled compound, which comigrated with authentic Met5-enkephalin on high-performance liquid chromatography (HPLC), was synthesized and was bound competitively by antibodies to enkephalin and by opiate receptors. This compound was tentatively identified as “Met5-enkephalin.”
-
3.
The newly synthesized35S-Met5-enkephalin was released upon depolarization of the retina with a high K+ concentration. This K+-stimulated release was greatly suppressed by 5 mM Co2+, suggesting that the release was Ca2+ dependent.
-
4.
Using a double-label technique, enkephalin immunoreactivity andγ-aminobutyric acid (GABA) uptake were colocalized to some amacrine cells, whereas others labeled only for enkephalin or GABA.
-
5.
The possible significance of enkephalin-GABA interactions is also discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschuler, R. A., Mosinger, J. W., Hoffman, D. W., and Parakkal, M. H. (1982). Immunocytochemical localization of enkephalin-like immunoreactivity in the retina of the guinea pig.Proc. Natl. Acad. Sci. USA 792398–2400.
Brecha, N., Karten, H. J., and Laverack, C. (1979). Enkephalin-containing amacrine cells in the avian retina: Immunohistochemical localization.Proc. Natl. Acad. Sci. USA 763010–3014.
Cotman, C. W. (1974). Isolation of synaptosomes and synaptic plasma membrane fractions. InMethods in Enzymology, Vol. 31, Biomembranes (Fleusher, S., and Pacher, L., eds.), Academic Press, New York, pp. 445–452.
Djamgoz, M. B. A., Stell, W. K., Chin, C. A., and Lam, D. M. K. (1981). An opiate system in the goldfish retina.Nature 292620–623.
Eldred, W., and Karten, H. J. (1984). Characterization and quantification of peptidergic amacrine cells in the turtle retina: enkephalin, neurotensin and glucagon.J. Comp. Nerol. 221371–378.
Eldred, W., and Karten, H. J. (1985). Ultrastructure and synaptic contacts of enkephalinergic amacrine cells in the retina of turtle.J. Comp. Neurol. 22236–48.
Fukuda, M. (1982). Localization of neuropeptides in the avian retina: An immunohistochemical analysis.Cell. Mol. Biol. 28275–283.
Howells, R. K., Groth, J., Miller, J. M., and Simon, E. J. (1980). Opiate binding sites in the retina: Properties and distribution.J. Pharmacol. Exp. Ther. 215 60–64.
Hsu, S.-M., Raine, L., and Fanger, H. (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures.J. Histochem. Cytochem. 29577–580.
Ishimoto, I., Shiosaka, S., Kuwayama, Y., Fuduka, M., Inagaki, S., Takagi, H., Sakanaka, M., Sasaoka, A., Senba, E., Sakiyama, T., and Tohyama, M. (1983). Leucine-enkephalin-like immunoreactivity in the chicken retina with a special reference to its fine structure.Invest. Ophthalmol. Vis. Sci. 24879–885.
Kuljis, R. O., and Karten, H. J. (1985). Substance P and leucine-enkephalin in ganglion cell axons in the anuran retina.Soc. Neurosci. Abstr. 10 458.
Lam, D. M. K., Li, H.-B., Su, Y. Y. T., and Watt, C. B. (1985). The signature hypothesis: Co-localizations of neuroactive substances as anatomical probes for circuitry analysis.Vision Res. 251353–1364.
Lasater, E. M., and Lam, D. M. K. (1984). The identification and some functions of GABAergic neurons in the proximal retina of the catfish.Vision Res. 24875–881.
Lindberg, I., Yang, H. Y. T., and Costa, E. (1982). Enzymatic production of Met5 - and Leu5-enkephalin in adrenal chromaffin granules.Adv. Biochem. Psychopharmacol. 33182–191.
Loh, H. H., and Ross, D. H. (1979).Neurochemical Mechanisms of Opiates and Endorphins, Raven Press, New York.
Louis, J. C., Rougeot, C., Bepoldin, O., Vulliez, B., Mandel, P., and Dray, F. (1983). Presence of somatostatin, enkephalins and substance P-like peptides in cultured neurons from embryonic chick cerebral hemispheres.J. Neurochem. 41930–930.
Lundberg, J. M., and Hokfelt, T. (1983). Coexistence of peptide and classical neurotransmitters.Trends Neurosci. 6325–333.
Marc, R. E., Stell, W. K., Bok, D., and Lam, D. M. K. (1978). GABAergic pathways in the goldfish retina.J. Comp. Neurol. 182221–246.
Miller, R. F., Frumkes, T. E., Slaughter, M., and Dacheux, R. F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina.J. Neurophysiol. 45764–782.
Morelli, M., and Chiara, G. D. (1984). Coexistence of GABA and enkephalin striatal neurons and possible coupling of GABA-ergic and opiatergic systems in the basal ganglia.Neuropharmacology 23847.
Osborne, N., and Hertz, A. (1981). Opiate binding protein in bovine retina.Neurochem. Int. 3143–148.
Sar, M., Stumpf, W. E., Miller, R. F., Chang, K.-J., and Cuatrecasas, P. (1978). Immunohistochemical localization of enkephalin in rat brain and spinal cord.J. Comp. Neurol. 18217–38.
Stell, W. K., Chohan, K. S., and Brecha, N. (1981). Enkephalin-immunoreactive amacrine cells in the retinas of some teleost fish.Soc. Neurosci. Abstr. 794.
Su, Y. Y. T. (1982). Biosynthesis and release of Met5-enkephalin in teleost retina.Soc. Neurosci. Abstr. 8587.
Su, Y. Y. T. (1984). Opiate binding sites in the avian retina.Soc. Neurosci. Abstr. 10585.
Su, Y. Y. T. (1985). Effect of morphine on enkephalin release.Soc. Neurosci. Abstr. 111200.
Su, Y. Y. T., Watt, C. B., and Lam, D. M. K. (1983). An enkephalin system in the chick retina. II. Biosynthesis, release and physiological studies.Soc. Neurosci. Abstr. 9282.
Su, Y. Y. T., Su, S., and Lam, D. M. K. (1984). An enkephalin system in the chicken retina: Receptor binding and physiological studies.Invest. Ophthalmol. Vis. Sci. (Suppl.)25292.
Su, Y. Y. T., Watt, C. B., and Lam, D. M. K. (1985). Opiate pathways in an avian retina. 1. The content, biosynthesis and release of Met5-enkephalin.J. Neurosci. 5851–856.
Tornqvist, K., Loren, I., Hakanson, R., and Sundler, F. (1981). Peptide-containing neurons in the chicken retina.Expl. Eye Res. 3355–64.
Watt, C. B., Tavella, D., Su, Y. Y. T., Peng, Y.-W., and Lam, D. M. K. (1983). An enkephalin system in the chicken retina. 1. Production and characterization of monoclonal antibodies; Enkephalin content and immunocytochemical localization.Soc. Neurosci. Abstr. 9282.
Watt, C. B., Su, Y. Y. T., and Lam, D. M. K. (1984). Interactions between enkephalin and GABA in an avian retina.Nature 311761–763.
Watt, C. B., Su, Y. Y. T., and Lam, D. M. K. (1985a). Opioid pathways in an avian retina. 2. The synaptic organization of enkephalin-immunoreactive amacrine cells.J. Neurosci. 5857–865.
Watt, C. B., Su, Y. Y. T., and Lam, D. M. K. (1985b). Enkephalins in the vertebrate retina. InProgress in Retinal Research, Vol. 4 (Osborne, N. N., and Chader, G. J., Eds.), Pergamon Press, Oxford and New York, pp. 221–242.
Weiler, R. (1985). Mesencephalic pathway to the retina exhibits enkephalin-like immunoreactivity.Neurosci. Lett. 55 11–16.
Wilson, S. P., Chang, -.J., and Viveros, H. (1980). Synthesis of enkephalins by adrenal medullary chromaffin cells: reserpine increases incorporation of radiolabeled amino acids.Proc. Natl. Acad. Sci. USA 774364–4368.
Yang, H. Y. T., Hong, J. S., Fratta, W. and Costa, E. (1978) Rat brain enkephalins distribution and biosynthesis.Adv. Biochem. Psychopharmacol. 26149–159.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Su, Y.Y.T., Fry, K.R., Lam, D.MK. et al. Enkephalin in the goldfish retina. Cell Mol Neurobiol 6, 331–347 (1986). https://doi.org/10.1007/BF00711404
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00711404