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Endogenous opiates in the chick retina and their role in form-deprivation myopia

Published online by Cambridge University Press:  02 June 2009

Ruth L. Pickett Seltner ,
Baerbel Rohrer ,
Vincent Grant  and
William K. Stell
Ruth L. Pickett Seltner
Affiliation:
Lions' Sight Centre/Department of Anatomy/Neuroscience Research Group, Faculty of Medicine, University of Calgary
Baerbel Rohrer
Affiliation:
Lions' Sight Centre/Department of Anatomy/Neuroscience Research Group, Faculty of Medicine, University of Calgary
Vincent Grant
Affiliation:
Lions' Sight Centre/Department of Anatomy/Neuroscience Research Group, Faculty of Medicine, University of Calgary
William K. Stell
Affiliation:
Lions' Sight Centre/Department of Anatomy/Neuroscience Research Group, Faculty of Medicine, University of Calgary
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Abstract

In this study, the possible role of the retinal enkephalin system in form-deprivation myopia (FDM) in the chick eye was investigated. Daily intravitreal injection of the nonspecific opiate antagonist naloxone blocked development of FDM in a dose-dependent manner, while injection of the opiate agonist morphine had no effect at any dose tested. The ED50 for naloxone (calculated maximum concentration in the vitreous) was found to be in the low picomolar range. The results using receptor-subtype-specific drugs were contradictory. Drugs specific for μ and δ receptors had no effect on FDM. The κ-specific antagonist nor-binaltorphimine (nor-BNI) reduced FDM by about 50% at maximum daily retinal doses ranging between 4 X 10-10 and 4 X 10 -7 M, while the κ-specific agonist U50488 blocked FDM in a dose-dependent manner with an ED50 between 5 X 10-8 and 5 X 10-7 M. Met-enkephalin immunoreactivity (ME-IR) was localized immunocytochemically to a subset of amacrine cells (ENSLI cells) and their neurites in the inner plexiform layer (IPL). As reported previously, ENSLI cells from untreated chick retinas showed a cyclical pattern of immunoreactivity, with increased immunoreactivity in the light compared to the dark. Form-deprivation did not appear to change this pattern. Amounts of preproenkephalin mRNA from normal or form-deprived eyes were approximately the same under all conditions. Daily injection of naloxone, however, did increase ME-IR in the dark. These results suggest that naloxone may affect release of enkephalin from the ENSLI cells. The results as presented are inconclusive with regards to the role of the enkephalin system in FDM. While the κ receptor may participate, there is no conclusive evidence here for a direct effect of opiate receptors. The effect of naloxone on form-deprived eyes may be due to its effect on release of peptides from the ENSLI cells.

Keywords

ChickForm-deprivation myopiaEnkephalinAmacrine cellsκ receptor
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 5 , September 1997 , pp. 801 - 809
Copyright
Copyright © Cambridge University Press 1997

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References

Ali, S.F., Hong, J.S. & Bondy, S.C. (1983). Response of neuropeptides and neurotransmitter binding sites in the retina and brain of the developing chick to reduced visual input. International Journal of Developmental Neurology 1, 99–103.Google ScholarPubMed
Amir, S. & Amit, Z. (1979). Enhanced analgesic effects of stress following chronic administration of naltrexone in rats. European Journal of Pharmacology 59, 137.CrossRefGoogle ScholarPubMed
Bjorklund, H., Olson, L. & Seiger, A. (1983). Enkephalin-like immunofluorescence in nerves of the rat iris following systemic capsaicin injection. Medical Biology 61, 280–282.Google ScholarPubMed
Boelen, M.K., Dowton, M. & Chubb, I.W. (1989). Enkephalin release and enkephalin precursors in chicken retina. In NATO ASI Series VH31, Neurobiology of the inner retina, ed. Weiler, R. & Osborne, N.N., pp 469–474. New York: Plenum.CrossRefGoogle Scholar
Brecha, N., Karten, H.J. & Laverack, C. (1979). Enkephalin containing amacrine cells in the avian retina. PNAS (USA) 76, 10–4.CrossRefGoogle ScholarPubMed
Brent, P.J. (1996). Kappa opioid receptor agonists inhibit sigma-1 (σ1) receptor binding in guinea-pig brain, liver and spleen: Autoradiographic evidence. Brain Research 725, 155–165.CrossRefGoogle Scholar
Chen, L., Gu, Y. & Huang, L.Y. (1995). The opioid peptide dynorphin directly blocks NMDA receptor channels in the rat. Journal of Physiology 482, 575–581.CrossRefGoogle ScholarPubMed
Chomczynski, P. & Sacchi, N. (1987). Single step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Analytical Biochemistry 162, 156–159.CrossRefGoogle ScholarPubMed
Comb, M., Seeburg, P.H., Adelman, J., Eiden, L. & Herbert, E. (1982). Primary structure of the human Met- and Leu-enkephalin precursor and its mRNA. Nature 295, 663–666.CrossRefGoogle ScholarPubMed
Dowton, M., Boelen, M.K. & Chubb, I.W. (1990). Light inhibits the release of both [Met5] enkephalin and [Met5] enkephalin-containing peptides in chicken retina but not their synthesis. Neuroscience 38, 187–193.CrossRefGoogle ScholarPubMed
Dowton, M., Boelen, M.K. & Morgan, I.G. (1994). Somatostatin-14 and somatostatin 28 are light-driven and vary during development in the chicken retina. Developmental Brain Research 78, 65–69.CrossRefGoogle ScholarPubMed
Fowler, C.J. & Fraser, G.L. (1994). μ-, δ-, κ-opioid receptors and their subtypes. A critical review with emphasis on radioligand binding experiments. Neurochemistry International 5, 401–426.CrossRefGoogle Scholar
Garner, L.K., Mendelson, B., Albers, K.M., Kindy, M., Overbeck, T.L. & Davis, B.M. (1994). Ontogeny and effect of activity on proen-kephalin mRNA expression during development of the chick spinal cord. Journal of Comparative Neurology 347, 36–46.CrossRefGoogle ScholarPubMed
Gray, D.B., Pilar, G.R. & Ford, M.J. (1989). Opiate and peptide inhibition of transmitter release in parasympathetic nerve terminals. Journal of Neuroscience 9, 1683–1692.CrossRefGoogle ScholarPubMed
Gubler, U., Kilpatrick, D.L., Seeburg, P.H., Gage, L.P. & Uden-friend, S. (1991). Detection and partial characterization of proenkephalin mRNA. PNAS (USA) 78, 5484–5487.CrossRefGoogle Scholar
Hodos, W. & Kuenzel, W.J. (1984). Retinal image degradation produces ocular enlargement in chicks. Investigative Ophthalmology and Visual Science 25, 652–659.Google ScholarPubMed
Koyuncuoglu, H. & Aricioclu, F. (1991). Previous chronic blockade of NMDA receptors intensifies morphine dependence in rats. Pharmacology, Biochemistry, and Behaviour 39, 575–579.CrossRefGoogle ScholarPubMed
LaGamma, E.F., White, J.D., Adler, J.E., Krause, J.E., McKelvey, J.F. & Black, I.B. (1989). Depolarization regulates adrenal preproenkeph-alin mRNA. Proceedings of the National Academy of Sciences of the U.S.A. 82, 8252–8255.CrossRefGoogle Scholar
Lahti, R.A., Vonvoigtlander, P.F. & Barsuhn, C. (1982). Properties of a selective kappa agonist, U-50488H. Life Sciences 31, 2257.CrossRefGoogle Scholar
Legon, S., Glover, D.M., Hughes, J., Lowry, P.J., Rigby, P.W. & Watson, C.J. (1982). The structure and expression of the preproenkephalin gene. Nucleic Acids Research 10, 7905–7918.CrossRefGoogle ScholarPubMed
Ling, G.S.F., Simantov, R., Clark, J.A. & Pasternak, G.W. (1986). Naloxonazine actions in vivo. European Journal of Pharmacology 129, 33.CrossRefGoogle ScholarPubMed
Luo, D., Stell, W.K. & Cupo, A. (1991). Synthesis and post-translational processing of proenkephalin in light- and dark-adapted chick retinas. Neurochemistry International 19, 483–494.CrossRefGoogle Scholar
Mansour, A., Lewis, M.E., Khachaturian, H., Akil, H. & Watson, S.J. (1986). Pharmacological and anatomical evidence of selective μ, δ, and κ opioid receptor binding in the rat brain. Brain Research 399, 69.CrossRefGoogle ScholarPubMed
McBrien, N.A., Moghaddam, H.O. & Reeder, A.P. (1993). Atropine reduces experimental myopia and eye enlargement via a non-accommodative mechanism. Investigative Ophthalmology and Visual Science 34, 205–215.Google Scholar
Megaw, D., Cluff, P., Morgan, I.G. & Boelen, M.K. (1994). Deprivation of form vision and temporal contrast restores the levels of [leu] enkephalin in the chick retina. Proceedings of the Australian Neuroscience Society 5, 200.Google Scholar
Millar, T.J., Salipan, N., Oliver, J.O., Morgan, I.G. & Chubb, I.W. (1984). The concentration of enkephalin like material in the chick retina is light dependent. Neuroscience 13, 221–226.CrossRefGoogle ScholarPubMed
Molnar, M., Casini, G., Davis, B.M., Brecha, N.C. & Bagnoli, P. (1995). Preproenkephalin messenger RNA-containing amacrine cells in the chicken retina identified with in situ hybridization. Visual Neuroscience 12, 185–189.CrossRefGoogle ScholarPubMed
Morgan, I.G., Wellard, J.W. & Boelen, M.K. (1994). A role for the enkephalin-immunoreactive amacrine cells of the chicken retina in adaptation to light and dark. Neuroscience Letters 174, 64–66.CrossRefGoogle ScholarPubMed
Pickett-Seltner, R.L., Sivak, J.G. & Pasternak, J.J. (1988). Experimentally induced myopia in chicks: Morphometric and biochemical analysis during the first 14 days after hatching. Vision Research 28, 323–328.CrossRefGoogle ScholarPubMed
Portochese, P.S., Lipowski, A.W. & Takemori, A.E. (1987). Bimorphins as highly selective, potent kappa opioid antagonists. Journal of Medical Chemistry 30, 238.CrossRefGoogle Scholar
Rohrer, B., Spira, A. & Stell, W.K. (1993). Apomorphine blocks form deprivation in chickens by a dopamine D2 receptor mechanism acting in retina or pigmented epithelium. Visual Neuroscience 10, 447–453.CrossRefGoogle ScholarPubMed
Rohrer, B. & Stell, W.K. (1994). Basic fibroblast growth factor (bFGF) and transforming growth factor beta (TGF-β) act as stop and go signals to modulate postnatal ocular growth in the chick. Experimental Eye Research 58, 553–562.CrossRefGoogle ScholarPubMed
Rohrer, B. (1995). Dopamine and bFGF regulate ocular growth. Doctoral Thesis, University of Calgary, Calgary, Alberta.Google Scholar
Rosen, H., Douglass, J. & Herbert, E.J. (1984). Isolation and characterization of the rat proenkephalin gene. Journal of Biological Chemistry 259, 14309–14313.CrossRefGoogle ScholarPubMed
Seltner, R.L.P., Grant, V.G. & Stell, W.K. (1994). [Met5]-enkephalin and form deprivation myopia. Investigative Ophthalmology and Visual Science Suppl. 35, 2069.Google Scholar
Seltner, R.L.P. & Stell, W.K. (1995 a). The effect of vasoactive intestinal peptide on development of form-deprivation myopia in the chick: A pharmacological and immunocytochemical study. Vision Research 35, 1265–1270.CrossRefGoogle Scholar
Seltner, R.L.P. & Stell, W.K. (1995 b). Form-deprivation myopia in the chick retina—a pharmacological investigation of the opiate and NMDA systems. Society for Neurosciences Abstracts 21, 1559.Google Scholar
Shih, Y.-F., Fitzgerald, M.E.C., Norton, T.T., Gamlin, P.D.R., Hodos, W. & Reiner, A. (1993). Reduction in choroidal blood flow occurs in chicks wearing goggles that induce eye growth towards myopia. Current Eye Research 12, 219–227.CrossRefGoogle Scholar
Shukla, V.K. & Lemaire, S. (1994). Non-opioid effects of dynorphins: Possible role of the NMDA receptor. Trends in Pharmacological Science 15, 420–424.CrossRefGoogle ScholarPubMed
Slaughter, M.M., Mattler, J.A. & Gottlieb, D.I. (1985). Opiate binding sites in the chick, rabbit and goldfish retina. Brain Research 339, 39–47.CrossRefGoogle ScholarPubMed
Sofuoglu, M., Portoghese, P.S. & Takemori, A.E. (1991). Differential antagonism of delta opioid agonists by naltrindole and its benzofuran analog (NTB) in mice: Evidence for delta opioid receptor subtypes. Journal of Pharmacology and Experimental Therapeutics 257, 676.Google ScholarPubMed
Stone, R.A., Lin, T., Iuvone, P.M. & Laties, A.M. (1990). Postnatal control of ocular growth: Dopaminergic mechanisms. In Myopia and the Control of Eye Growth, ed. Bock, G. & Widdows, K., pp. 45–62. Chichester, England: John Wiley and Sons Ltd.Google Scholar
Stone, R.A., Lin, T. & Laties, A.M. (1991). Muscarinic antagonists effects on experimental chick myopia [letter]. Experimental Eye Research 52, 755–758.CrossRefGoogle ScholarPubMed
Tinsley, P.W., Fridland, G.H., Killmar, J.T. & Desiderio, D.M. (1988). Purification, characterization, and localization of neuropeptides in the cornea. Peptides 9, 1373–1379.CrossRefGoogle ScholarPubMed
Uhl, G.R., Childers, S. & Pasternak, G. (1994). An opiate-receptor gene family reunion. Trends in Neurosciences 17, 89–93.CrossRefGoogle ScholarPubMed
Wallman, J., Turkel, J. & Trachtman, J. (1978). Extreme myopia produced by modest changes in early visual experience. Science (Washington, D.C.) 201, 1249–1251.CrossRefGoogle ScholarPubMed
Wallman, J., Wildsoet, C., Xu, A., Gottlieb, M.D., Nickla, D.L., Marran, L., Krebs, W. & Christensen, A.M. (1995). Moving of the retina: Choroidal modulation of refractive state. Vision Research 35, 37–50.CrossRefGoogle ScholarPubMed
Watt, C.B., Su, Y.-Y. & Lam, D.M-K. (1985). Enkephalin in the verte-brate retina. Progress in Retinal Research 4, 221–242.CrossRefGoogle Scholar
Watt, C.B. & Florack, V.J. (1994). A triple-label analysis demonstrating that enkephalin-, somatostatin-, and neurotensin-like immunoreactivities are expressed by a single population of amacrine cells in the chick retina. Brain Research 634, 310–316.CrossRefGoogle Scholar
Wollemann, M., Benyhe, S. & Siman, J. (1993). The kappa opioid receptor: Evidence for the different subtypes. Life Sciences 52, 599–611.CrossRefGoogle ScholarPubMed
Wu, S.M. & Lam, D.M. (1988). The coexistence of three neuroactive substances in amacrine cells of the chicken retina. Brain Research 458, 195–198.CrossRefGoogle ScholarPubMed
Yoshikawa, K., Williams, C. & Sabol, S.L. (1984). Rat brain preproenkephalin mRNA. Journal of Biological Chemistry 259, 14301–14308.CrossRefGoogle ScholarPubMed
Zamboni, L. & DeMartino, C. (1967). Buffered picric acid formalde-hyde: A new fixative for electron microscopy. Journal of Cell Biology 35, 148A.Google Scholar