Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T05:05:16.240Z Has data issue: false hasContentIssue false

Differential effects of excitatory amino acids on photoreceptors of the chick retina: An electron-microscopical study using the zinc-iodide-osmium technique

Published online by Cambridge University Press:  02 June 2009

Jintana Sattayasai
Affiliation:
Department of Anatomy, Monash University, Victoria, Australia
Joe Zappia
Affiliation:
Department of Anatomy, Monash University, Victoria, Australia
David Ehrlich
Affiliation:
Department of Anatomy, Monash University, Victoria, Australia

Abstract

Although excitotoxins derived from acidic amino acids are known to damage neurons in the inner nuclear and ganglion cell layers of the retina, little is known about their effects on photoreceptors. This study examines the acute and long-term effects of excitotoxins on photoreceptors of the chick retina. The zinc-iodide-osmium (ZIO) technique, which darkly labels a substantial subpopulation of synaptic vesicles in normal photoreceptor terminals, was used to supplement routine electron microscopy. Two-day-old chicks received a single intraocular injection of either 10, 50, or 200 nmoles kainic acid (KA), 200 nmoles N-methyl-D-aspartic acid (NMDA), or 200 nmoles quisqualic acid (QUIS), and were allowed to survive for either 6 h, 7 d, or 21 d. At 6 h, following exposure to 10, 50, and 200 nmoles KA, there was swelling and disruption of photoreceptor lamellae of the outer segments. At 7- and 21-d survival, 50 and 200 nmoles KA resulted in rounded, condensed synaptic terminals, which contained a high density of synaptic vesicles. However, there was complete loss of ZIO-positive vesicles within these photoreceptors. Outer segments were still disrupted, although small patches of lamellae were evident, suggestive of regeneration. Following exposure to QUIS, there was extensive swelling of outer segment lamellae at 6 h survival. Synaptic ribbons in terminals were also swollen. At longer survival periods, QUIS exposure resulted in a reduction of ZIO-positive vesicles, as well as swollen lamellae in outer segments. NMDA exposure, at either short or long-term survival, did not alter photoreceptor morphology, including the pattern of ZIO stain. The prolonged effects of KA, and to a lesser extent QUIS, on photoreceptors suggests that these drugs have a long-term effect on photoreceptor function. The ZIO technique provides a novel and potentially useful approach for identification of damaged photoreceptors.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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

Akert, K. & Sandri, C. (1975). Significance of the Maillet method for cytochemical studies of synapses. In Golgi Centennial Symposium Proceedings, ed. Santini, M., pp. 387399. New York: Raven Press.Google Scholar
Akert, K., Kawana, E. & Sandri, C. (1971). ZIO-positive and ZIO-negative vesicles in nerve terminals. In Histochemistry of Nervous Transmission. Progress in Brain Research, Vol. 35, ed. Eranko, O., pp. 305317. Amsterdam: Elsevier.Google Scholar
Coleman, P.A., Massey, S.C. & Miller, R.F. (1986). Kynurenic acid distinguishes kainate and quisqualate receptors in the vertebrate retina. Brain Research 381, 172175.CrossRefGoogle ScholarPubMed
Coyle, J.T., Biziere, K. & Schwarcz, R. (1978). Neurotoxicity of excitatory amino acids in the neural retina. In Kainic Acid as a Tool in Neurobiology, ed. McGeer, E.G., Olney, J.W. & McGeer, P.L., pp. 177188. New York: Raven Press.Google Scholar
Coyle, J.T. & Schwarcz, R. (1983). The use of excitatory amino acids as selective neurotoxins. In Handbook of Chemical Neuroanatomy, Vol. 1: Methods in Chemical Neuroanatomy, ed. Bjorklund, A.R. & Hokfelt, T., pp. 508527. New York: Elsevier Science Publishers.Google Scholar
Ehrlich, D. & Morgan, I.G. (1980). Kainic acid destroys displaced amacrine cells in post-hatch chicken retina. Neuroscience Letters 17, 4348.CrossRefGoogle ScholarPubMed
Gibson, B.L. & Reif-Lehrer, L. (1984). In vitro effects of kainate on embryonic and posthatching chick retina. Departmental Brain Research 15, 93103.Google Scholar
Gibson, B.L. & Reif-Lehrer, L. (1985). Mg2+ reduces N-methyl-D-aspartate neurotoxicity in embryonic chick neural retina in vitro. Neuroscience Letters 57, 1318.CrossRefGoogle ScholarPubMed
Greenberger, L.M. & Besharse, J.C. (1985). Stimulation of photoreceptor disk shedding and pigment epithelial phagocytosis by glutamate, aspartate, and other amino acids. Journal of Comparative Neurology 239, 361372.CrossRefGoogle Scholar
Hampton, C.K., Garcia, C. & Redburn, D.A. (1981). Localization of kainic acid-sensitive cells in mammalian retina. Journal of Neu-roscience Research 6, 99111.CrossRefGoogle ScholarPubMed
Hayat, M.A. (1981). Principles and Techniques of Electron Microscopy: Biological Applications. Vol. 1. (2nd Ed.), pp. 357362. Baltimore: University Park Press.Google Scholar
Ingham, C.A. & Morgan, I.G. (1983). Dose-dependent effects of intravitreal kainic acid on specific cell types in chicken retina. Neuroscience 9, 165181.CrossRefGoogle ScholarPubMed
Kawana, E., Akert, K. & Sandri, C. (1969). Zinc-iodide-osmium tetroxide impregnation of nerve terminals in the spinal cord. Brain Research 16, 325331.CrossRefGoogle ScholarPubMed
Kleinschmidt, J., Zucker, C.L. & Yazulla, S. (1986). Neurotoxic action of kainic acid in the isolated toad and goldfish retina: I. Description of effects. Journal of Comparative Neurology 254, 184195.CrossRefGoogle ScholarPubMed
Krogsgaard-Larsen, P. & Honore, T. (1983). Glutamate receptors and new glutamate agonists. Trends in Pharmacological Science 4, 3133.CrossRefGoogle Scholar
McLennan, H. (1981). On the nature of receptors for various excitatory amino acids in the mammalian central nervous system. In Glutamate as a Neurotransmitter. Advances in Biochemical Psychopharmacology, Vol. 27, ed. DiChiara, G. & Gessa, G.L., pp. 252264. New York: Raven Press.Google Scholar
Miller, R.F. & Slaughter, M.M. (1986). Excitatory amino-acid receptors of the retina: diversity of subtypes and conductance mechanisms. Trends in Neuroscience 9, 211218.CrossRefGoogle Scholar
Morgan, I.G. (1983). Kainic acid as a tool in retinal research. Progress in Retinal Research 2, 249266.CrossRefGoogle Scholar
Morgan, I.G. & Ingham, C.A. (1981). Kainic acid affects both plexi-form layers of chicken retina. Neuroscience Letters 21, 275280.CrossRefGoogle Scholar
Morris, V.B. & Shorey, C.D. (1967). An electron microscope study of types of receptors in the chick retina. Journal of Comparative Neurology 129, 313340.CrossRefGoogle ScholarPubMed
O'dell, T. & Christensen, B.N. (1986). N-methyl-D-aspartate receptors coexist with kainate and quisqualate receptors on single isolated catfish horizontal cells. Brain Research 381, 359362.CrossRefGoogle ScholarPubMed
Olney, J.W. (1978). Neurotoxicity of excitatory amino acids. In Kainic Acid as a Tool in Neurobiology, ed. McGeer, E.G., Olney, J.W. & McGeer, P.L., pp. 95117. New York: Raven Press.Google Scholar
Olney, J.W., ho, O.L. & Rhee, V. (1971). Cytotoxic effects of acidic and sulphur containing amino acids on the infant mouse central nervous system. Experimental Brain Research 14, 6176.CrossRefGoogle ScholarPubMed
Pellegrino De Iraldi, A. (1975). Localizing-SH groups in monoaminergic synaptic vesicles with the mixture of zinc-iodide-osmium tetroxide (ZIO). Brain Research 94, 363367.CrossRefGoogle Scholar
Pellegrino De Iraldi, A. (1977). Significance of the Maillet method (ZIO) for cytochemical studies of subcellular structures. Experientia 33, 110.CrossRefGoogle Scholar
Pellegrino De Iraldi, A. & Guedet, R. (1969). Osmium tetroxidezinc iodide reactive sites in photoreceptor cells of the retina of the rat. Zeitschrift für Zellforschung 101, 203211.CrossRefGoogle ScholarPubMed
Sattayasai, J. & Ehrlich, D. (1987 a). Folic acid protects chick retinal neurons against the neurotoxic action of excitatory amino acids. Experimental Eye Research 44, 523535.CrossRefGoogle ScholarPubMed
Sattayasai, J. & Ehrlich, D. (1987 b). Morphology of quisqualate-induced neurotoxicity in the chicken retina. Investigative Ophthalmology and Visual Science 28, 106117.Google ScholarPubMed
Sattayasai, J., Rogers, L.J. & Ehrlich, D. (1985). Sequential treatment with low doses of kainic acid alters sensitivity of retinal cell types. Neuroscience Letters 54, 277281.CrossRefGoogle ScholarPubMed
Schwarcz, R. & Coyle, J.T. (1977). Kainic acid: neurotoxic effects after intraocular injection. Investigative Ophthalmology 16, 141148.Google ScholarPubMed
Tung, N.N., Morgan, I.G. & Ehrlich, D. (1987). Intravitreal kainic acid severely reduces the size of the developing optic tectum in newly hatched chickens. Brain Research 435, 153159.CrossRefGoogle ScholarPubMed
Watkins, J.C. & Evans, R.H. (1981). Excitatory amino-acid transmitters. Annual Reviews in Pharmacology and Toxicology 21, 165204.CrossRefGoogle ScholarPubMed