Hostname: page-component-848d4c4894-8bljj Total loading time: 0 Render date: 2024-06-29T22:49:38.808Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of glutamate and its analogs on intracellular calcium levels in the developing retina

Published online by Cambridge University Press:  02 June 2009

Rachel O.L. Wong
Rachel O.L. Wong
Affiliation:
Vision, Touch and Hearing Research Centre, Departments of Physiology and Pharmacology, University of Queensland, Brisbane, QLD 4072, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

Stimulation of neuronal cells by the excitatory amino acid, glutamate, often leads to a rise in cytosolic free calcium concentration ([Ca2+]$sub/sub$), which can affect cell survival and differentiation. The early appearance of endogenous glutamate in the embryonic rabbit retina suggests that it may be involved in intercellular signalling during development. Thus, the effect of glutamate on the [Ca2+]$sub/sub$ of cells in the fetal and neonatal rabbit retina was examined using Ca2+ imaging techniques, which enabled the responses of large numbers of morphologically identified classes of cell to be compared directly. Ganglion cells and amacrine cells, the first retinal neurons to differentiate, showed a rise in [Ca2+]$sub/sub$ in the presence of glutamate from the earliest age studied (embryonic day 20; E20). These responses were mediated by non-NMDA (non-N-methyl-D-aspartate) receptors. NMDA stimulated ganglion cells and amacrine cells only several days later, at about E24. Moreover, whilst most, if not all, putative ganglion cells responded to NMDA, only a subset of putative amacrine cells were sensitive to NMDA throughout development. Photoreceptors, bipolar cells, horizontal cells, and Müller cells differentiate later than the ganglion cells and amacrine cells. Between E20 and birth, cells in the ventricular zone are largely the precursors of these cell types. During this period, 50–60% of ventricular cells responded to glutamate with an increase in [Ca2+]$sub/sub$, upon activation of ionotropic non-NMDA receptors. At no age studied were these ventricular cells, or their differentiated counterparts, stimulated by NMDA. After birth, most cells in the inner nuclear layer were sensitive to non-NMDA receptor agonists, but photoreceptors showed no response. Taken together, the results suggests that NMDA and non-NMDA receptors may adopt separate roles during retinal development, and that non-NMDA receptors, rather than NMDA receptors, may be involved in developmental processes in the ventricular zone.

Keywords

NMDA receptorsNon-NMDA receptorsCalcium imagingRabbit retina
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 5 , September 1995 , pp. 907 - 917
Copyright
Copyright © Cambridge University Press 1995

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

REFERENCES

Altshuler, D., Lo Turco, J.J., Rush, J. & Cepko, C. (1993). Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 119, 1317–1318.CrossRefGoogle 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, 144–146.CrossRefGoogle Scholar
Choi, D.W. (1988). Glutamate neurotoxicity and disease of the nervous system. Neuron 1, 623–634.Google Scholar
Collins, F., Schmidt, M.F., Guthrie, P.B. & Kater, S.B. (1991). Sustained increase in intracellular calcium promotes neuronal survival. Journal of Neuroscience 1991, 2582–2587.CrossRefGoogle Scholar
Constantine-Paton, M., Cline, H.T. & Debski, E. (1990). Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annual Reviews in Neuroscience 13, 129–154.Google Scholar
Dacheux, R.F. & Miller, R.F. (1981a). 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, 307–326.Google Scholar
Dacheux, R.F. & Miller, R.F. (1981b). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. II. Amacrine cells. Journal of Comparative Neurology 198, 327–334.CrossRefGoogle ScholarPubMed
Fawcett, J.W., O'Leary, D.D.M. & Cowen, W.M. (1984). Activity and the control of ganglion cell death in the rat retina. Proceedings of the National Academy of Sciences of the U.S.A. 81, 5589–5593.CrossRefGoogle ScholarPubMed
Greiner, J.V. & Weidman, T.A. (1982). Embryogenesis of the rabbit retina. Experimental Eye Research 34, 749–765.CrossRefGoogle ScholarPubMed
Grynkiewicz, G., Poenie, M. & Tsien, R.Y. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. Journal of Biological Chemistry 260, 3440–3450.Google Scholar
Hahm, J.O., Langdon, R.B. & Sur, M. (1991). Disruption of retino-geniculate afferent segregation by antagonists to NMDA receptors. Nature 351, 568–570.CrossRefGoogle Scholar
Honore, T., Davies, S.N., Drejer, J., Fletcher, E.J., Jacobsen, P., Lodge, D. & Nielsen, F.E. (1988). Quinoxalinediones: Potent competitive non-NMDA glutamate receptor antagonists. Science 241, 701–703.CrossRefGoogle ScholarPubMed
Kater, S.B. & Mills, L.R. (1991). Regulation of growth cone behaviour by calcium. Journal of Neuroscience 11, 891–899.CrossRefGoogle ScholarPubMed
Komura, H. & Rakic, P. (1993). Modulation of neuronal migration by NMDA receptors. Science 260, 95–97.CrossRefGoogle Scholar
Kriegstein, A., Davies, M.B.F. & Lo Turco, J. (1994). GABA and glutamate depolarize cerebral cortical progenitor cells and inhibit DNA synthesis. Society for Neuroscience Abstracts 20, 458.Google Scholar
Lau, K.C., So, K.-F. & Tay, D. (1992). APV prevents the elimination of transient dendritic spines on a population of retinai ganglion cells. Brain Research 595, 171–174.Google Scholar
Lauder, J.M. (1993). Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends in Neuroscience 16, 233–240.CrossRefGoogle ScholarPubMed
Lei, S., Zhang, D., Abele, A.E. & Lipton, S.A. (1992). Blockade of NMDA receptor-mediated mobilization of intracellular Ca2+ prevents neurotoxicity. Brain Research 598, 196–202.CrossRefGoogle ScholarPubMed
Lipton, S.A. (1986). Blockade of electrical activity promotes the death of mammalian retinal ganglion cells in culture. Proceedings of the National Academy of Sciences of the U.S.A. 83, 9774–9778.Google Scholar
Lipton, S.A. & Kater, S.B. (1989). Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends in Neuroscience 12, 265–270.CrossRefGoogle ScholarPubMed
Lo Turco, J.J. & Kriegstein, A.R. (1991). Clusters of coupled neuroblasts in embryonic neocortex. Science 252, 563–566.Google Scholar
Masland, R.H. (1977). Maturation of function in the developing rabbit retina. Journal of Comparative Neurology 175, 275–286.Google Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399–425.Google Scholar
Massey, S.C. & Miller, R.F. (1990). N-methyl-D-aspartate receptors of ganglion cells in rabbit retina. Journal of Neurophysiology 63, 16–30.CrossRefGoogle ScholarPubMed
Mattson, M.P. (1988). Neurotransmitters in the regulation of neuronal cytoarchitecture. Brain Research Reviews 13, 179–212.CrossRefGoogle Scholar
Mattson, M.P., Dou, P. & Kater, S.B. (1988). Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. Journal of Neuroscience 8, 2087–2100.CrossRefGoogle ScholarPubMed
Mattson, M.P. & Hauser, K.F. (1991). Spatial and temporal integration of neurotransmitter signals in the development of neural circuitry. Neurochemistry International 19, 17–24.CrossRefGoogle 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, 253–274.CrossRefGoogle ScholarPubMed
McDonald, J.W. & Johnston, M.V. (1990). Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Research Reviews 15, 41–70.CrossRefGoogle ScholarPubMed
Messersmith, E.K. & Redburn, D.A. (1990). Kainic acid lesioning alters development of the outer plexiform layer in neonatal rabbit retina. International Journal of Developmental Neuroscience 8, 447–461.CrossRefGoogle ScholarPubMed
Palmer, E., Monaghan, D.T. & Cotman, C.W. (1989). Trans-ACPD, a selective agonist of the phosphoinositide-coupled excitatory amino acid receptor. European Journal of Pharmacology 166, 585–587.CrossRefGoogle ScholarPubMed
Pow, D.V. & Robinson, S.R. (1994). Glutamate in some retinal neurons is derived solely from glia. Neuroscience 60, 355–366.Google Scholar
Pow, D.V., Crook, D.K. & Wong, R.O.L. (1994). Early appearance and transient expression of putative amino acid neurotransmitters and related molecules in the developing rabbit retina: An immuno-cytochemical study. Visual Neuroscience 11, 1115–1134.CrossRefGoogle 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, 61–66.CrossRefGoogle ScholarPubMed
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, Vol. 3, ed. Cronly-Dillon, J.R., pp. 69–128. U.K.: MacMillan.Google Scholar
Robinson, S.R., Horsburgh, G.M., Dreher, B. & McCall, M.J. (1987). Changes in the numbers of retinal ganglion cells and optic nerve axons in the developing albino rabbit. Developmental Brain Research 35, 161–174.Google Scholar
Rörig, B. & Grantyn, R. (1993). Glutamatergic and GABAergic synaptic currents in ganglion cells from isolated retinae of pigmented rats during postnatal development. Developmental Brain Research 74, 98–110.CrossRefGoogle ScholarPubMed
Schoepp, D.D., Johnson, B.G., Smith, E.C. & Quaid, LA. (1990). Stereoselectivity and mode of inhibition of phosphoinositide-coupled excitatory amino acid receptors by 2-amino-3 phosphonopropionic acid. Molecular Pharmacology 38, 222–228.Google ScholarPubMed
Shuttleworth, T.J. & Thompson, J.L. (1991). Effect of temperature on receptor-activated changes in [Ca2+]$sub/sub$ and their determination using fluorescent probes. Journal of Biological Chemistry 266, 1410–1414.CrossRefGoogle Scholar
Spitzer, N.C. (1994). Spontaneous Ca2+ spikes and waves in embryonic neurons: Signaling systems for differentiation. Trends in Neuroscience 17, 115–118.CrossRefGoogle ScholarPubMed
Stone, J., Egan, M. & Rapaport, D.H. (1985). The site of commencement of retinal maturation in the rabbit. Vision Research 25, 309–317.CrossRefGoogle ScholarPubMed
Sucher, N.J., Lei, S.Z. & Lipton, S.A. (1991a). Calcium channel antagonists attenuate NMDA receptor-mediated neurotoxicity of retinal ganglion cells in culture. Brain Research 297, 297–302.CrossRefGoogle Scholar
Sucher, N.J., Aizenman, E. & Lipton, S.A. (1991b). N-methyl-D-aspartate antagonists prevent kainate neurotoxicity in rat retinal ganglion cells in vitro. Journal of Neuroscience 11, 966–971.Google Scholar
Sugiyama, H., Ito, I. & Hirono, C. (1987). A new type of glutamate receptor linked to inositol phospholipid metabolism. Nature 325, 531–533.CrossRefGoogle ScholarPubMed
Tsien, R.W. & Tsien, R.Y. (1990). Calcium channels, stores and oscillations. Annual Review of Cell Biology 6, 715–760.Google Scholar
Walsh, C. & Polley, E.H. (1985). The topography of ganglion cell production in the cat's retina. Journal of Neuroscience 5, 741–750.CrossRefGoogle ScholarPubMed
Wong, R.O.L. (1990). Differential growth and remodelling of ganglion cell dendrites in the postnatal rabbit retina. Journal of Comparative Neurology 294, 109–132.Google Scholar
Wong, R.O.L. (1995). Cholinergic regulation of [Ca2+]$sub/sub$ during cell division and differentiation in the mammalian retina. Journal of Neuroscience 15, 2696–2706.CrossRefGoogle Scholar
Yamashita, M. & Fukuda, Y. (1993). Calcium channels and GABA receptors in the early embryonic chick retina. Journal of Neurobiology 24, 1600–1614.Google Scholar
Yuste, R. & Katz, L.C. (1991). Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6, 333–344.CrossRefGoogle ScholarPubMed
Zimmerman, R.P., Polley, E.H. & Fortney, R.L. (1988). Cell birthdays and the rate of differentiation of ganglion and horizontal cells of the developing cat's retina. Journal of Comparative Neurology 274, 77–90.Google Scholar
Zorumski, C.F. & Liu, L.T. (1992). Properties of vertebrate glutamate receptors: Calcium mobilization and desensitization. Progress in Neurobiology 39, 295–336.Google Scholar