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Early appearance and transient expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: An immunocytochemical study

Published online by Cambridge University Press:  02 June 2009

D.V. Pow
Affiliation:
Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, University of Queensland, Brisbane, QLD 4072, Australia
O.K. Crook
Affiliation:
Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, University of Queensland, Brisbane, QLD 4072, Australia
R.O.L. Wong
Affiliation:
Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, University of Queensland, Brisbane, QLD 4072, Australia

Abstract

We have studied, by immunocytochemistry, the ontogeny of GABA, glycine, glutamate, glutamine, and taurine-containing cells in the rabbit retina. Amacrine cells show GABA immunoreactivity by embryonic day 25 (E25) and throughout postnatal life. By contrast, ganglion cells and horizontal cells are only transiently GABA-immunoreactive (-IR); few appear GABA-IR by the third postnatal week. At maturity, glycine is present in amacrine cells and in some bipolar cells. During development, putative ganglion cells transiently contained glycine between E25 and postnatal day 3 (P3), whereas immunolabelling in presumed amacrine cells and bipolar cells persists after birth. Ganglion cells, bipolar cells, photoreceptors, and some amacrine cells are glutamate-IR in the adult retina. Glutamate immunoreactivity first appears in the somata and processes of cytoblastic cells by E20 and is prominent by E25. Surprisingly, ganglion cells are not strongly glutamate-IR until just before eye-opening, at postnatal day 10 (P10), coincident with the appearance of glutamine in their somata and in Müller glial cells. Bipolar cells are glutamate-IR before they or Müller cells contain high levels of glutamine (at P10). Glutamate immunoreactivity in photoreceptors is progressively restricted to the inner segments by eye-opening. At no stage are presumed horizontal cells glutamate-IR or glutamine-IR, but some amacrine cells show glutamate- and glutamine-IR by P10. Taurine is localized to photoreceptors and Müller glial in the adult retina. Some cytoblasts are taurine-IR at E20; with ensuing development, taurine labelling becomes restricted primarily to Müller cells and photoreceptors; some putative bipolar cells may also be labelled. However, for a few days around birth, cells resembling horizontal cells, also show taurine immunoreactivity. The early appearance and often transient expression of these amino acids in retinal cells suggests that these neuroactive molecules may be involved in the structural and functional development of the retina.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Bellhorn, R.W. & Fischer, C.A. (1970). Feline central retinal degeneration. Journal of the American Veterinary Medical Association 157, 842849.Google ScholarPubMed
Bodnarenko, S.R. & Chalupa, L.M. (1993). Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364, 144146.CrossRefGoogle Scholar
Caruso, D.M., Owczarzak, M.T., Goebel, D.J., Hazlett, J.C. & Pourcho, R.G. (1989). GABA-immunoreactivity in ganglion cells of the rat retina. Brain Research 476, 129154.CrossRefGoogle ScholarPubMed
Cohen, E. & Sterling, P. (1986). Accumulation of [3H] glycine by cone bipolar cells in the cat retina. Journal of Comparative Neurology 250, 17.CrossRefGoogle ScholarPubMed
Constantine-Paton, M., Cline, H.Y. & Debski, E. (1990). Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annual Reviews of Neuroscience 13, 129154.CrossRefGoogle ScholarPubMed
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate, and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287302.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Miller, R.F. (1981 a). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. I. Receptors, horizontal, and bipolar cells. Journal of Comparative Neurology 198, 307326.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Miller, R.F. (1981 b). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. II. Amacrine cells. Journal of Comparative Neurology 198, 327334.CrossRefGoogle ScholarPubMed
Edwards, R.B. (1977). Accumulation of taurine by cultures retinal pigment epithelium of the rat. Investigative Ophthalmology 16, 201208.Google ScholarPubMed
Ehinger, B. (1973). Glial uptake of taurine in the rabbit retina. Brain Research 60, 512516.CrossRefGoogle ScholarPubMed
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. & Dowling, J. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 83218325.CrossRefGoogle ScholarPubMed
Fung, S.-K., Kong, Y.-U. & Lam, D. M.-K. (1982). Prenatal development of GABAergic, glycinergic, and dopaminergic neurons in the rabbit retina. Journal of Neuroscience 2, 16231632.CrossRefGoogle ScholarPubMed
Goodman, C.S. & Shatz, C.J. (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72/Neuron 10(Suppl.) 7798.Google Scholar
Gordon-Weeks, P.R., Lockerbie, R.O. & Pearce, B.R. (1984). Uptake and release of [3H]GABA by growth cones isolated from the neonatal rat brain. Neuroscience Letters 52, 205210.CrossRefGoogle ScholarPubMed
Greiner, J.V. & Weidman, T.A. (1982). Embryogenesis of the rabbit retina. Experimental Eye Research 34, 749765.CrossRefGoogle ScholarPubMed
Grünert, U. & Wässle, H. (1990). GABA-like immunoreactivity in the Macaque monkey retina: A light and electron microscopic study. Journal of Comparative Neurology 297, 509524.Google Scholar
Harman, A.M. & Beazley, L.D. (1989). Generation of retinal cells in the wallably Setonix brachyurus (quokka). Neuroscience 28, 219232.Google Scholar
Hayes, K.C., Carey, R.E. & Schmidt, S.Y. (1975). Retinal degeneration associated with taurine deficiency in the cat. Science 188, 949951.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Koontz, M.A., Pourcho, R.G., Sarthy, P.V. & Goebel, D.J. (1988). Localization of glycine-containing neurons in Macaca monkey retina. Journal of Comparative Neurology 273, 473478.CrossRefGoogle ScholarPubMed
Huxtable, R.J. (1992). Physiological actions of taurine. Physioiogical Reviews 72, 101163.CrossRefGoogle ScholarPubMed
Jäger, J. & Wässle, H. (1987). Localization of glycine uptake and receptors in the cat retina. Neuroscience Letters 75, 147151.CrossRefGoogle ScholarPubMed
Kong, Y.-C., Fung, S.-C. & Lam, D.M.-K. (1980). Postnatal development of glycinergic neurons in the rabbit retina. Journal of Comparative Neurology 193, 11271135.CrossRefGoogle ScholarPubMed
Koontz, M.A., Hendrickson, A.E. & Ryan, M.K. (1989). GABA-immunoreactive synaptic plexus in the nerve fiber layer of primate retina. Visual Neuroscience 2, 1925.CrossRefGoogle ScholarPubMed
Lake, N. (1992). Taurine, GABA and GFAP immunoreactivity in the developing and adult rat optic nerve. Brain Research 596, 124132.Google Scholar
Lake, N. & Verdone-Smith, C. (1989). Immunocytochemical localisation of taurine in the mammalian retina. Current Eye Research 18, 163173.CrossRefGoogle Scholar
Lam, D.M. -K., Fung, S.-C. & Kong, Y.-U. (1980). Postnatal development of GABA-ergic neurons in the rabbit retina. Journal of Comparative Neurology 193, 89102.Google ScholarPubMed
Lauder, J.M. (1993). Neurotransmitters as growth regulatory signals: Role of receptors and second messengers. Trends in Neuroscience 16, 233240.CrossRefGoogle ScholarPubMed
La Vail, M.M., Rapaport, D.H. & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86114.Google Scholar
Lima, L., Drujan, B. & Matus, P. (1990). Spatial distribution of taurine in the teleost retina and its role in retinal tissue regeneration. In Taurine: Functional Neurochemistry, Physiology, and Cardiology, ed. Pasantes-Morales, H., pp. 103112. Chichester: Wiley-Liss Inc.Google Scholar
Lipton, S.A. & Kater, S.B. (1989). Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends in Neuroscience 7, 265270.CrossRefGoogle Scholar
Lombardini, J.B. (1991). Taurine: Retinal function. Brain Research Reviews 16, 151169.CrossRefGoogle ScholarPubMed
Lugo-García, N. & Blanco, R.E. (1991). Localization of GAD- and GABA-like immunoreactivity in ground squirrel retina: retrograde labelling demonstrates GAD-positive ganglion cells. Brain Research 564, 1926.Google Scholar
Madtes, P.C. Jr. & Redburn, D.A. (1982). [3H]-GABA binding in developing rabbit retina. Neurochemistry Research 7, 495503.Google Scholar
Mandel, P. & Pasantes-Morales, H. (1976). Taurine: A putative neurotransmitter. Advances in Biochemical Psychopharmacology 15, 141164.Google ScholarPubMed
Marc, R.E. & Liu, W.-L.S. (1985). [3H] glycine-accumulating neurons of the human retina. Journal of Comparative Neurology 232, 241260.Google Scholar
Masland, R.H. (1977). Maturation of function in the developing rabbit retina. Journal of Comparative Neurology 175, 275286.Google Scholar
McArdle, C.B., Dowling, J.E. & Masland, R.H. (1977). Development of outer segments and synapses in the rabbit retina. Journal of Comparative Neurology 175, 253274.Google Scholar
Merchenthaler, L., Gallyas, F. & Liposits, Z. (1989). Silver intensification in immunocytochemistry. In Techniques in Immunocyto-chemistry, ed. Bullock, G. R. & Petrusz, P., pp. 217252. New York: Academic Press.Google Scholar
Messersmith, E.K. & Redburn, D.A. (1992). Gamma-aminobutyric acid immunoreactivity in multiple cells types of the developing rabbit retina. Visual Neuroscience 8, 201211.CrossRefGoogle ScholarPubMed
Messersmith, E.K. & Redburn, D.A. (1993). The role of GABA during development of the outer retina in the rabbit. Neurochemistry Research 18, 463470.Google Scholar
Moscona, A.A. & Piddington, R. (1966). Stimulation by hydrocortione of premature changes in the developmental pattern of glutamine synthetase in embryonic retina. Biochimica et Biophysica Acta 121, 409411.Google Scholar
Nakamura, Y., McGuire, B.A. & Sterling, P. (1980). Interplexiform cell in cat retina: Identification by uptake of gamma-[3H]amino-butyric acid and serial reconstruction. Proceedings of the National Academy of Sciences of the U.S.A. 77, 658661.CrossRefGoogle Scholar
Osborne, N.N., Patel, S., Beaton, D.W. & Neuhoff, V. (1986). GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell and Tissue Research 243, 117123.CrossRefGoogle ScholarPubMed
Ottersen, O.P. (1987). Postembedding light- and electron-microscopic immunocytochemistry of amino acids: Description of a new model system allowing identical conditions for specificity testing and tissue processing. Experimental Brain Research 69, 167174.CrossRefGoogle ScholarPubMed
Pasantes-Morales, H. (1985). Taurine function in excitable tissues: The retina as a model. Retinal Transmitters and Modulators: Models for the Brain, ed. Pasantes-Morales, H., pp. 3362. Boca Raton, Florida: CRC Press, Inc.Google Scholar
Politi, L.E., Dreyer, E.B. & Lipton, S.A. (1992). Activation of voltage or ligand-gated calcium channels induces neurite retraction. Society for Neuroscience Abstracts 18, 42.Google Scholar
Pourcho, R.G. (1977). Distribution of [35S] taurine in mouse retina after intravitreal and intravascular injection. Experimental Eye Research 25, 119127.Google Scholar
Pourcho, R.G. (1981). Autoradiographic localization of [3H] muscimol in the cat retina. Brain Research 215, 187199.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1983). Neuronal subpopulations in cat retina which accumulate the GABA agonist, [3H] muscimol: A combined Golgi and autoradiographic study. Journal of Comparative Neurology 219, 2435.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1987 a). A combined Golgi and autoradiographic study of 3H-glycine-accumulating cone bipolar cells in the cat retina. Journal of Neuroscience 7, 11781188.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1987 b). Visualization of endogenous glycine in cat retina: An immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 11891197.Google Scholar
Pow, D.V. (1993). immunocytochemistry of amino acids in the rodent pituitary using extremely specific, very high litre antisera. Journal of Neuroendocrinology 5, 349356.Google Scholar
Pow, D.V. & Crook, D.K. (1993). Extremely high litre polyclonal antisera againsl small neurolransmiller molecules: Rapid produclion, characterisation and use in light- and eleclron-microscopic immu-nocylochemislry. Journal of Neuroscience Methods 48, 5163.CrossRefGoogle Scholar
Pow, D.V. & Robinson, S.R. (1994). Glutamale in some relinal neurones is derived solely from glia. Neuroscience 60, 355366.CrossRefGoogle ScholarPubMed
Priestley, J.V. & Cuello, A.C. (1983). Electron-microscopic immunocytochemistry for CNS transmillers and transmitter markers. In Immunohistochemistry, ed. Cuello, A.C., pp. 273322. Chichester: John Wiley.Google Scholar
Rassin, D.K. (1982). Taurine, cysteinesulfinic acid decarboxylase and glutamic acid in brain. Advances in Experimental Medicine and Biology 139, 257268.CrossRefGoogle Scholar
Redburn, D.A. (1992). Development of GABAergic neurons in the mammalian retina. Progress in Brain Research 90, 133147.Google Scholar
Redburn, D.A., Blanchard, V. & Messersmith, E.K. (1991). Picrotoxin disrupts development of the cone photoreceptor distribution in rabbit retina. Investigative Ophthalmology and Visual Science (Suppl.) 32, 925.Google Scholar
Redburn, D.A., Agarwal, S.H., Messersmith, E.K. & Mitchell, C.K. (1992). Development of the glutamate system in rabbit retina. Neurochemistry Research 17, 6166.Google Scholar
Redburn, D.A. & Madtes, P. Jr. (1986). Postnatal development of 3H-GABA-accumulating cells in rabbit retina. Journal of Comparative Neurology 243, 4157.Google Scholar
Reichenbach, A., Schnitzer, J., Friedrich, A., Knothe, A.-K. & Henke, A. (1991). Development of the rabbit retina: II Müller cells. Journal of Comparative Neurology 311, 3344.Google Scholar
Riepe, R.E. & Norenberg, M.D. (1978). Glutamine synthetase in the developing rat retina: An immunohistochemical study. Experimental Eye Research 27, 435444.Google Scholar
Robinson, S.R. (1991). Development of the mammalian retina. In Neuroanatomy of the Visual Pathways and their Development, ed. Dreher, B. & Robinson, S.R.Vision and Visual Dysfunction (Series), Vol. 3, ed. Cronly-Dillon, J.R., pp. 69138. U.K.: Macmillan.Google Scholar
Sakatani, K., Black, J.A. & Kocsis, J.D. (1992). Transient presence and functional interaction of endogenous GABA and GABAA receptors in developing rat optic nerve. Proceedings of the Royal Society B (London) 247, 155161.Google ScholarPubMed
Schnitzer, J. (1988). Immunocytochemical studies on the development of astrocytes, Müller (glial) cells, and oligodendrocytes in the rabbit retina. Developmental Brain Research 44, 5972.Google Scholar
Schnitzer, J. & Rusoff, A.C. (1984). Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. Journal of Neuroscience 4, 29482955.CrossRefGoogle ScholarPubMed
Vandesande, F. (1983). Peroxidase-antiperoxidase techniques. In Immunohistochemistry, ed. Cuello, A.C., pp. 101119. Chichester: John Wiley.Google Scholar
Van Leeuwen, F.W. (1980). Immunocytochemical specificity for peptides with special reference to arginine-vasopressin and oxytocin. Journal of Histochemistry and Cytochemistry 28, 479482.Google Scholar
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49100.Google Scholar
Versaux-Botteri, C., Pocket, R. & Nguyen-Legros, J. (1989). Immunohistochemical localization of GABA-containing neurons during postnatal development of the rat retina. Investigative Ophthalmology and Visual Science 30, 652659.Google Scholar
Voaden, M.J., Lake, N., Marshall, J. & Morjaria, B. (1977). Studies on the distribution of taurine and other neuroactive amino acids in the retina. Experimental Eye Research 25, 249257.CrossRefGoogle ScholarPubMed
Walsh, C. & Polley, E.H., (1985). The topography of ganglion cell production in the cat's retina. Journal of Neuroscience 5, 741750.Google Scholar
Wässle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 4354.Google Scholar
Yazulla, S. (1991). The mismatch problem for GABAergic amacrine cells in goldfish retina: Resolution and other issues. Neurochemistry Research 16, 327339.Google Scholar
Young, R.W. (1985). Cell differentiation in the retina of the mouse. Anatomical Research III, 199205.CrossRefGoogle Scholar
Yu, B.-C., Watt, C.B., Lam, D.M.K. & Fry, K.R. (1988). GABAergic ganglion cells in the rabbit retina. Brain Research 439, 376382.Google Scholar
Zimmerman, R.P., Polley, E.H. & Fortney, R.L. (1988). Cell birthdays and rate of differentiation of ganglion and horizontal cells of the developing cat's retina. Journal of Comparative Neurology 274, 7790.Google Scholar