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. 1986 Dec;6(4):331–347. doi: 10.1007/BF00711404

Enkephalin in the goldfish retina

Y Y Thomas Su 1,✉, Keith R Fry 1, Dominic Man-Kit Lam 1, Carl B Watt 1
PMCID: PMC11567201  PMID: 3030554

Abstract

  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.

Key words: enkephalins, γ-aminobutyric acid (GABA), goldfish retina, immunocytochemistry, autoradiography, biosynthesis, release, double-label technique, colocalization, corelease, presynaptic autoreceptor

References

  1. 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. USA792398–2400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brecha, N., Karten, H. J., and Laverack, C. (1979). Enkephalin-containing amacrine cells in the avian retina: Immunohistochemical localization.Proc. Natl. Acad. Sci. USA763010–3014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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. [DOI] [PubMed] [Google Scholar]
  4. Djamgoz, M. B. A., Stell, W. K., Chin, C. A., and Lam, D. M. K. (1981). An opiate system in the goldfish retina.Nature292620–623. [DOI] [PubMed] [Google Scholar]
  5. 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. [DOI] [PubMed] [Google Scholar]
  6. 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. [DOI] [PubMed] [Google Scholar]
  7. Fukuda, M. (1982). Localization of neuropeptides in the avian retina: An immunohistochemical analysis.Cell. Mol. Biol.28275–283. [PubMed] [Google Scholar]
  8. 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. [PubMed] [Google Scholar]
  9. 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. [DOI] [PubMed] [Google Scholar]
  10. 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. [PubMed] [Google Scholar]
  11. 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. [Google Scholar]
  12. 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. [DOI] [PubMed] [Google Scholar]
  13. 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. [DOI] [PubMed] [Google Scholar]
  14. 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. [PubMed] [Google Scholar]
  15. Loh, H. H., and Ross, D. H. (1979).Neurochemical Mechanisms of Opiates and Endorphins, Raven Press, New York. [Google Scholar]
  16. 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. [DOI] [PubMed] [Google Scholar]
  17. Lundberg, J. M., and Hokfelt, T. (1983). Coexistence of peptide and classical neurotransmitters.Trends Neurosci.6325–333. [Google Scholar]
  18. 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. [DOI] [PubMed] [Google Scholar]
  19. 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. [DOI] [PubMed] [Google Scholar]
  20. 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.Neuropharmacology23847. [Google Scholar]
  21. Osborne, N., and Hertz, A. (1981). Opiate binding protein in bovine retina.Neurochem. Int.3143–148.20487818 [Google Scholar]
  22. 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. [DOI] [PubMed] [Google Scholar]
  23. 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. [Google Scholar]
  24. Su, Y. Y. T. (1982). Biosynthesis and release of Met5-enkephalin in teleost retina.Soc. Neurosci. Abstr.8587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Su, Y. Y. T. (1984). Opiate binding sites in the avian retina.Soc. Neurosci. Abstr.10585. [Google Scholar]
  26. Su, Y. Y. T. (1985). Effect of morphine on enkephalin release.Soc. Neurosci. Abstr.111200. [Google Scholar]
  27. 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. [Google Scholar]
  28. 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. [Google Scholar]
  29. 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. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tornqvist, K., Loren, I., Hakanson, R., and Sundler, F. (1981). Peptide-containing neurons in the chicken retina.Expl. Eye Res.3355–64. [DOI] [PubMed] [Google Scholar]
  31. 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. [Google Scholar]
  32. Watt, C. B., Su, Y. Y. T., and Lam, D. M. K. (1984). Interactions between enkephalin and GABA in an avian retina.Nature311761–763. [DOI] [PubMed] [Google Scholar]
  33. 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. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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. [Google Scholar]
  35. Weiler, R. (1985). Mesencephalic pathway to the retina exhibits enkephalin-like immunoreactivity.Neurosci. Lett.55 11–16. [DOI] [PubMed] [Google Scholar]
  36. 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. USA774364–4368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yang, H. Y. T., Hong, J. S., Fratta, W. and Costa, E. (1978) Rat brain enkephalins distribution and biosynthesis.Adv. Biochem. Psychopharmacol.26149–159. [PubMed] [Google Scholar]

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