Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-17T09:05:51.055Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential expression of glutamate receptor genes (GluR1-5) in the rat retina

Published online by Cambridge University Press:  02 June 2009

Thomas E. Hughes ,
Irm Hermans-Borgmeyer  and
Steve Heinemann
Thomas E. Hughes
Affiliation:
Department of Neurosciences 0608, University of California at San Diego, La Jolla
Irm Hermans-Borgmeyer
Affiliation:
Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, San Diego
Steve Heinemann
Affiliation:
Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, San Diego
Get access Rights & Permissions [Opens in a new window]

Abstract

The recent isolation of at least five different cDNAs encoding functional subunits of glutamate receptors (GluR1 to GluR5) has revealed a diversity whose function is not understood. To learn more about how these different receptor subunits are used in the brain, we undertook an in situ hybridization study of the retina to define how the different glutamate receptor genes are expressed. We chose the retina because the glutamate sensitivities of its different cell types have been characterized, and these different neurons reside in different laminae.

Hybridization of [35S]UTP-labeled cRNA probes with transverse sections and freshly dissociated cells reveals that all five receptor subunits are expressed in the retina. Hybridization signal is detected in different, but overlapping, sets of cells in the retina. GluR1, GluR2, and GluR5 are expressed by many somata, and GluR4 by a few, in the outer third of the inner nuclear layer, where the horizontal cells reside. Transcripts for GluR1, GluR2, and GluR5 are found in the somata within the middle third of the inner nuclear layer, which is where the bipolar cell somata are located, and GluR2 probes label freshly dissociated rod bipolar cells. All of the probes produce labeling over the cells at the inner edge of the inner nuclear layer, which are probably amacrine cells, as well as over the cell bodies in the ganglion cell layer.

Keywords

GlutamateGlutamatereceptorsRetinaRod bipolar cells
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 1 , January 1992 , pp. 49 - 55
Copyright
Copyright © Cambridge University Press 1992

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

Aizenman, E., Karschin, A. & Lipton, S.A. (1989). Two pharmacological classes of quisqualate-induced electrical responses in rat retinal ganglion cells in vitro. European Journal of Pharmacology 174, 9–22.CrossRefGoogle ScholarPubMed
Bettler, B., Boulter, J., Hermans-Borgmeyer, I., O'shea-Green-Field, A., Deneris, E.S., Moll, C., Borgmeyer, U., Hollmann, M. & Heinemann, S. (1990). Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5, 583–595.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society B 255, 109–184.Google Scholar
Boycott, B.B. & Kolb, H. (1973). The connections between bipolar cells and photoreceptors in the retina of the domestic cat. Journal of Comparative Neurology 148, 115–140.CrossRefGoogle ScholarPubMed
Boulter, J., Hollmann, M., O'shea-Greenfield, A., Hartley, M., Deneris, E., Maron, C. & Heinemann, S. (1990). Molecular cloning and functional expression of glutamate receptor subunit genes. Science 249, 1033–1037.CrossRefGoogle ScholarPubMed
Changeux, J.-P., Giraudat, J. & Dennis, N. (1987). The nicotinic acetylcholine receptor: Molecular architecture of a ligand-regulated ion channel. Trends in Biochemical Sciences 8, 459–465.Google Scholar
Deneris, E.S., Boulter, J., Swanson, L.W., Patrick, J. & Heinemann, S. (1989). Beta3: A new member of nicotinic acetylcholine receptor gene family is expressed in brain. Journal of Biological Chemistry 264, 6268–6272.CrossRefGoogle Scholar
Deneris, E., Connolly, J., Duvoisin, R. & Rogers, S.W. (1991). Pharmacological and functional diversity of neuronal nicotinic acetylcholine receptors. Trends in Pharmacological Sciences 12, 34–41.CrossRefGoogle ScholarPubMed
Dingledine, R., Myers, S.J. & Nicholas, R.A. (1990). Molecular biology of mammalian amino acid receptors. FASEB Journal 4, 2636–2645.Google ScholarPubMed
Dixon, D.B. & Copenhagen, D.R. (1990). Light evoked glutamatergic inputs to amacrine cells in the tiger salamander retina. Society for Neuroscience Abstracts 16, 713.Google Scholar
Dowling, J.E. (1987). The Retina: An approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Egebjerg, J., Bettler, B., Hermans-Borgmeyer, I. & Heinemann, S. (1991). Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351, 745–748.CrossRefGoogle Scholar
Gilbertson, T.A., Scobey, R. & Wilson, M. (1991). Permeation of calcium ions through non-NMDA glutamate channels in retinal bipolar cells. Science 251, 1613–1615.CrossRefGoogle ScholarPubMed
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433–442.CrossRefGoogle ScholarPubMed
Hollmann, M., O'shea-Greenfield, A., Rogers, S. & Heinemann, S. (1989). Cloning by functional expression of a member of the glutamate receptor family. Nature 342, 643–648.CrossRefGoogle ScholarPubMed
Hollmann, M., Hartley, M. & Heinemann, S. (1991). Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851–853.CrossRefGoogle ScholarPubMed
Huba, R. & Hofmann, H.-D. (1988). Tetanus toxin binding to isolated and cultured rat retinal glial cells. Glia 1, 156–164.CrossRefGoogle ScholarPubMed
Ishida, A., Kaneko, A. & Tachibana, M. (1984). Responses Of Solitary Retinal Horizontal Cells From Carassius Auratus To L-Glutamate And Related Amino Acids. Journal of Physiology 348, 255–270.CrossRefGoogle ScholarPubMed
Karschin, A. & Wässle, H. (1990). Voltage-gated and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860–876.CrossRefGoogle Scholar
Keinanen, K., Wisden, W., Sommer, B., Werner, P., Herb, A., Verdoorn, T.A., Sakmann, B. & Seeburg, P.H. (1990). A family of AMPA-selective glutamate receptors. Science 249, 556–560.CrossRefGoogle ScholarPubMed
Knapp, A.G., Schmidt, K.F. & Dowling, J.E. (1990). Dopamine Modulates The Kinetics Of Ion Channels Gated By Excitatory Amino Acids In Retinal Horizontal Cells. Proceedings of the National Academy of Science of the U.S.A. 87, 767–771.CrossRefGoogle ScholarPubMed
Lasater, E.M., Dowling, J.E. & Ripps, H. (1984). Pharmacological Properties Of Isolated Horizontal And Bipolar Cells From The Skate Retina. Journal of Neuroscience 4, 1966–1975.CrossRefGoogle ScholarPubMed
Liman, E.R., Knapp, A.G. & Dowling, J.E. (1989). Enhancement of kainate-gated currents in retinal horizontal cells by cyclic AMP-dependent protein kinase. Brain Research 481, 399–402.CrossRefGoogle ScholarPubMed
Lin, D.M., Blazynski, C., Redburn, D.A. & Massey, S.C. (1991). Acetylcholine release from the rabbit retina mediated by kainate receptors. Journal of Neuroscience 11, 111–122.CrossRefGoogle Scholar
Lin, D.M. & Massey, S.C. (1991). Acetylcholine release from the rabbit retina mediated by NMDA receptors. Journal of Neuroscience 11, 123–133.CrossRefGoogle Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N. & Chader, J., pp. 399–425. Oxford, England: Pergamon 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 Neurosciences 9, 211–218.CrossRefGoogle Scholar
Monaghan, D.T., Bridges, R.J. & Cotman, C.W. (1989). The excitatory amino acid receptors: Their classes, pharmacology, and distinct properties in the function of the central nervous system. Annual Review of Pharmacology and Toxicology 29, 365–402.CrossRefGoogle ScholarPubMed
Nakanishi, N., Schneider, N.A. & Axel, R. (1990). A family of glutamate receptor genes—evidence for the formation of heteromultimeric receptors with distinct channel properties. Neuron 5, 569–581.CrossRefGoogle Scholar
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269–271.CrossRefGoogle ScholarPubMed
O'dell, T.J. & Christensen, B.N. (1986). N-methyl-d-aspartate receptors co-exist with kainate and quisqualate receptors on single isolated cat-fish horizontal cells. Brain Research 381, 359–362.CrossRefGoogle Scholar
O'dell, T.J. & Christensen, B.N. (1989). A voltage-clamp study of isolated stingray horizontal cell non-NMDA excitatory amino acid receptors. Journal of Neurophysiology 61, 162–172.CrossRefGoogle ScholarPubMed
Olson, R.W. & Tobin, A.J. (1990). Molecular biology of GABAA receptors. FASEB Journal 4, 1468–1480.Google Scholar
Rogers, S.W., Hughes, T.E., Hollmann, M., Gasic, G.P., Deneris, E.S. & Heinemann, S. (1991). The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain. Journal of Neuroscience 11, 2713–2724.CrossRefGoogle ScholarPubMed
Sarthy, P.V. & Lam, D.M.-K. (1979). Isolated cells from a mammalian retina. Brain Research 176, 208–212.CrossRefGoogle ScholarPubMed
Schofield, P.R., Shivers, B.D. & Seeburg, P.H. (1990). The role of receptor subtype diversity in the CNS. Trends in Neuroscience 13, 8–11.CrossRefGoogle ScholarPubMed
Sommer, B., Keinänen, K., Verdoorn, T.A., Wisden, W., Burnashev, N., Herb, A., Kohler, M., Takagi, T., Sakmann, B. & Seeburg, P.H. (1990). Flip and flop: A cell-specific functional switch in glutamate-operated channels of the CNS. Science 249, 1580–1585.CrossRefGoogle ScholarPubMed
Sucher, N.J., Wong, L.A. & Lipton, S.A. (1990). Redox modulation of NMDA receptor-mediated Ca2+ flux in mammalian central neurons. NeuroReport 1, 29–32.CrossRefGoogle ScholarPubMed
Wässle, H., Yamashita, M., Greferath, U., Grünert, U. & Müller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99–112.CrossRefGoogle ScholarPubMed
Yamashita, M. & Wässle, H. (1990). Responses of dissociated rod bipolar cells of the rat retina to 2-amino-4-phosphonobutyric acid (APB). Society for Neuroscience Abstracts 16, 712.Google Scholar