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Glutamate and GABA receptors in vertebrate glial cells

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Abstract

Glial cells of the central nervous system express receptors for the main inhibitory and excitatory neurotransmitters, GABA and glutamate. The glial GABA and glutamate receptors share many properties with the neuronal GABAA and kainate/quisqualate receptors, but are molecularly and, in some aspects, pharmacologically distinct from their neuronal counterparts. The functional role of these receptors is as yet speculative: They have been proposed to control proliferation of astrocytes, serve to balance ion changes at GABAergic synapses, or they could enable the glial cell to detect neuronal synaptic activity.

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References

  • Ahmed Z., Lewis C. A., and Faber D. S. (1990) Glutamate stimulates release of Ca2+ from internal stores in astroglia.Brain Res. 516, 165–169.

    Article  PubMed  CAS  Google Scholar 

  • Backus K. H., Kettenmann H., and Schachner M. (1988) Effect of benzodiazepines and pentobarbital on the GABA-induced depolarization in cultured astrocytes.Glia 1, 132–140.

    Article  PubMed  CAS  Google Scholar 

  • Backus K. H., Kettenmann H., and Schachner M. (1989) Pharmacological characterization of the glutamate receptor in cultured astrocytes.J. Neurosci. Res. 22, 274–282.

    Article  PubMed  CAS  Google Scholar 

  • Barnard E. A. and Henley J. M. (1990) The non-NMDA receptors: Types, protein structure and molecular biology.TIPS 11, 500–507.

    PubMed  CAS  Google Scholar 

  • Barres B. A., Koroshetz W. J., Chun L. L. Y., and Corey D. P. (1990a) Ion channel expression by white-matter glia: The type-1 astrocyte.Neuron 5, 527–544.

    Article  PubMed  CAS  Google Scholar 

  • Barres B. A., Koroshetz W. J., Swartz K. J., Chun L. L. Y., and Corey D. P. (1990b) Ion channel expression by white matter glia: The O-2A glial progenitor cell.Neuron 4, 507–524.

    Article  PubMed  CAS  Google Scholar 

  • Berger T., Walz W., Schnitzer J., and Kettenmann H. (1991a) GABA and glutamate-activated currents in glial cells of the mouse corpus callosum slice.J. Neurosci. Res., in press.

  • Berger T., Schnitzer J., and Kettenmann H. (1991b) Developmental changes in the membrane current pattern, K buffer capacity, and morphology of glial cells in the corpus callosum sclice.J. Neurosci. 11, 3008–3024.

    PubMed  CAS  Google Scholar 

  • Blankenfeld G. von, Ymer S., Pritchett D. B., Sontheimer H., Ewert M., Seeburg P. H., and Kettenmann H. (1990) Differential benzodiazepine pharmacology of mammalian recombinant GABAA receptors.Neurosci. Lett. 115, 269–273.

    Article  Google Scholar 

  • Blankenfeld G. von, Trotter J., and Kettenmann H. (1991) Expression and developmental regulation of a GABAA receptor in cultured murine cells of the oligodendrocyte lineage.Eur. J. Neurosci. 3, 310–316.

    Article  Google Scholar 

  • Bormann J. and Kettenmann H. (1988) Patch-clamp study of γ-aminobutyric acid receptor Cl− channels in cultured astrocytes.Proc. Natl. Acad. Sci. USA 85, 9336–9340.

    Article  PubMed  CAS  Google Scholar 

  • Bowman C. L. and Kimelberg H. K. (1984) Excitatory amino acid directly depolarize rat brain astrocytes in primary culture.Nature 311, 656–659.

    Article  PubMed  CAS  Google Scholar 

  • Brew H. and Attwell D. (1987) Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells.Nature 327, 707–709.

    Article  PubMed  CAS  Google Scholar 

  • Chan P. H. and Chu L. (1989) Ketamine protects cultured astrocytes from glutamate-induced swelling.Brain Res. 487, 380–383.

    Article  PubMed  CAS  Google Scholar 

  • Chan P. H., Chu L., and Chen S. (1990) Effects of MK-801 on glutamate-induced swelling of astrocytes in primary cell culture.J. Neurosci. Res. 25, 87–93.

    Article  PubMed  CAS  Google Scholar 

  • Chvátal A. and Kettenmann H. (1991) Effect of steroids on GABA induced currents in cultured mouse astrocytes.Pflügers Arch. 419, 263–266.

    Article  PubMed  Google Scholar 

  • Condorelli D. F., Ingrao F., Magri G., Bruno V., Nicoletti F., and Avola R. (1989) Activation of excitatory amino acid receptors reduces thymidine incorporation and cell proliferation rate in primary cultures of astrocytes.Glia 2, 67–69.

    Article  PubMed  CAS  Google Scholar 

  • Cornell-Bell A. H. and Finkbeiner S. M. (1991) Ca++ waves in astrocytes.Cell Calcium 12, 185–204.

    Article  PubMed  CAS  Google Scholar 

  • Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., and Smith S. J. (1990a) Glutamate-induces calcium waves in cultured astrocytes: Long-range glial signaling.Science 247, 470–473.

    Article  PubMed  CAS  Google Scholar 

  • Cornell-Bell A. H., Thomas P. G., and Smith S. J. (1990b) The excitatory neurotransmitter glutamate causes filopodia formation in cultured hippocampal astrocytes.Glia 3, 322–334.

    Article  PubMed  CAS  Google Scholar 

  • Enkvist M. O., Holopainen I., and Akerman K. E. O. (1988) The effect of K and glutamate receptor agonists on the membrane potential of suspensions of primary cultures of rat astrocytes as measured with a cyanine dye, DiS-C-(5).Brain Res. 462, 67–75.

    Article  PubMed  CAS  Google Scholar 

  • Gallo V., Suergiu R., Giovannini C., and Levi G. (1987a) Glutamate receptor subtypes in cultured cerebellar neurons: Modulation of glutamate and gamma-aminobutyric acid release.J. Neurochem. 49, 1801–1809.

    Article  PubMed  CAS  Google Scholar 

  • Gallo V., Suergiu R., and Levi G. (1987b) Functional evaluation of glutamate receptor subtypes in cultured cerebellar neurones and astrocytes.Eur. J. Pharmacol. 138, 293–297.

    Article  PubMed  CAS  Google Scholar 

  • Gilbert P., Kettenmann H., and Schachner M. (1984) γ-Aminobutyric acid directly depolarizes cultured oligodendrocytes.J. Neurosci. 4, 561–569.

    PubMed  CAS  Google Scholar 

  • Glaum S. R., Holzwarth J. A., and Miller R. J. (1990) Glutamate receptors activate Ca2+ mobilization and Ca2+ influx into astrocytes.Proc. Natl Acad. Sci. USA 87, 3454–3458.

    Article  PubMed  CAS  Google Scholar 

  • Gregor P., Mano I., Maoz I., McKeown M., and Teichberg V. I. (1989) Molecular structure of the chick cerebellar kainate-binding subunit of a putative glutamate receptor.Nature 342, 689–692.

    Article  PubMed  CAS  Google Scholar 

  • Hatten M. E. (1990) Riding the glial monorail: A common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain.Trends Neurosci. 13, 179–184.

    Article  PubMed  CAS  Google Scholar 

  • Henn F. A., Goldstein M. N., and Hamberger A. (1974) Uptake of the neurotransmitter candidate glutamate by glial.Nature 249, 663, 664.

    Article  PubMed  CAS  Google Scholar 

  • Hoppe D. and Kettenmann H. (1989) GABA triggers a Cl− efflux from cultured mouse oligodendrocytes.Neurosci. Lett. 97, 334–339.

    Article  PubMed  CAS  Google Scholar 

  • Hösli A. L., Andres P. F., and Hösli E. (1978) Neuronglia interactions: Indirect effect of GABA on cultured glial cells.Exp. Brain Res. 33, 425–434.

    Article  PubMed  Google Scholar 

  • Hösli A. L., Andres P. F., and Hösli E. (1979) Action of amino acid transmitters on cultured glial cells of the mammalian peripheral and central nervous system.J. Physiol. 75, 655–659.

    Google Scholar 

  • Jensen A. M. and Chiu S. Y. (1990) Fluorescence measurement of changes in intracellular calcium induced by excitatory amino acids in cultured cortical astrocytes.J. Neurosci. 10, 1165–1175.

    PubMed  CAS  Google Scholar 

  • Kettenmann H. (1990) Chloride channels and carriers in cultured glial cells, inChloride Channels and Carriers in Nerve, Muscle, and Glial Cells (Alvarez-Leefmans F. J. and Russell J. M., eds.), Plenum, New York, pp. 193–208.

    Google Scholar 

  • Kettenmann H., Backus K. H., and Schachner M. (1984) Aspartate, glutamate and gamma-aminobutyric acid directly depolarize cultured astrocytes.Neurosci. Lett. 52, 25–29.

    Article  PubMed  CAS  Google Scholar 

  • Kettenmann H., Backus K. H., and Schachner M. (1987) γ-Aminobutyric acid opens Cl− channels in cultured astrocytes.Brain Res. 404, 1–9.

    Article  PubMed  CAS  Google Scholar 

  • Kettenmann H. and Schachner M. (1985) Pharmacological properties of GABA, glutamate and aspartate induced depolarizations in cultured astrocytes.J. Neurosci. 5, 3295–3301.

    PubMed  CAS  Google Scholar 

  • Kimelberg H. K. (1990) Chloride transport across glial membranes, inChloride Channels and Carriers in Nerve, Muscle, and Glial Cells (Alvarez-Leefmans F. J. and Russell J. M., eds.), Plenum, New York, pp. 159–191.

    Google Scholar 

  • Kimelberg H. K., Goderie S. K., Higman S., Pang S., and Waniewski R. A. (1990) Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures.J. Neurosci. 10, 1583–1591.

    PubMed  CAS  Google Scholar 

  • Krnjevic K. and Schwartz S. (1967) Some properties of unresponsive cells in the cerebral cortex.Exp. Brain Res. 3, 306–319.

    Article  PubMed  CAS  Google Scholar 

  • MacVicar B. A., Tse F. W., Crichton S. A., and Kettenmann H. (1989) GABA-activated Cl− channels in astrocytes of hippocampal slices.J. Neurosci. 9, 3577–3583.

    PubMed  CAS  Google Scholar 

  • Malchow R. P., Qian H. H., and Ripps H. (1989) gamma-Aminobutyric acid (GABA)-induced currents of skate Muller (glial) cells are mediated by neuronal-like GABAA receptors.Proc. Natl. Acad. Sci. USA 86, 4226–4230.

    Article  Google Scholar 

  • Müller C. M. and Best J. (1989) Ocular dominance plasticity in adult cat visual cortex after transplantation of cultured astrocytes.Nature 342, 427–430.

    Article  PubMed  Google Scholar 

  • Nicoletti F., Magri G., Ingrao F., Bruno V., Catania M. V., Dell'Albani P., Condorelli D. F., and Avola R. (1990) Excitatory amino acids stimulate inositol phospholipid hydrolysis and reduce proliferation in cultured astrocytes.J. Neurochem. 54, 771–777.

    Article  PubMed  CAS  Google Scholar 

  • Ortega A., Eshar N., and Teichberg V. I. (1991) Properties of kainate receptor/channels on cultured Bergmann glia.Neurosci. 41, 335–349.

    Article  CAS  Google Scholar 

  • Pearce B., Albrecht J., Morrow C., and Murphy S. (1986) Astrocyte glutamate receptor activation promotes inositol phospholipid turnover and calcium flux.Neurosci. Lett. 72, 335–340.

    Article  PubMed  CAS  Google Scholar 

  • Pearce B., Morrow C., and Murphy S. (1990) Further characterisation of excitatory amino acid receptors coupled to phosphoinositide metabolism in astrocytes.Neurosci. Lett. 113, 298–303.

    Article  PubMed  CAS  Google Scholar 

  • Robertson P. L., Bruno G. R., and Datta S. C. (1990) Glutamate-stimulated, guanine nucleotide-mediated phosphoinositide turnover in astrocytes is inhibited by cyclic AMP.J. Neurochem. 55, 1727–1733.

    Article  PubMed  CAS  Google Scholar 

  • Schoepp D., Bockaert J., and Sladeczek F. (1990) Pharmacological and functional characteristics of metabotropic excitatory amino acid receptors.TIPS 11, 508–515.

    PubMed  CAS  Google Scholar 

  • Schon F. and Kelly J. S. (1975) Selective uptake of (3H) beta-alanine by glia: Association with the uptake system for GABA.Brain Res. 86, 243–257.

    Article  PubMed  CAS  Google Scholar 

  • Sontheimer H., Kettenmann H., Backus K. H., and Schachner M. (1988) Glutamate opens Na+/K+ channels in cultured astrocytes.Gliu 1, 328–336.

    Article  CAS  Google Scholar 

  • Steinhäuser C., Berger T., Jabs R., Frotscher M., and Kettenmann H. (1991a) Voltage- and ligand-gated membrane current pattern of identified glial cells in the hippocampal slice, inSlow Activity Changes in the Brain (Haschke W. and Speckmann E.-J., eds.), Birkhäuser, Boston, in press.

    Google Scholar 

  • Steinhäuser C., Berger T., Frotscher M., and Kettenmann H. (1991b) Heterogeneity in the membrane current pattern of identified glial cells in the hippocampal slice: A combined patch-clamp and ultrastructural study (submitted for publication).

  • Sugiyama H., Ito I., and Hirono C. (1987) A new type of glutamate receptor linked to inositol phospholipid metabolism.Nature 325, 531–533.

    Article  PubMed  CAS  Google Scholar 

  • Tang C. M. and Orkand R. K. (1986) Glutamate depolarization of glial cells in Necturus optic nerve.Neurosci. Lett. 63, 300–304.

    Article  PubMed  CAS  Google Scholar 

  • Usowicz M. M., Gallo V., and Cull-Candy S. G. (1989) Multiple conductance channels in type-2 cerebellar astrocytes activated by excitatory amino acids.Nature 339, 380–383.

    Article  PubMed  CAS  Google Scholar 

  • Ventimiglia R., Grierson J. P., Gallombardo P., Sweetnam P. M., Tallman J. F., and Geller H. M. (1990) Cultured rat neurons and astrocytes express immunologically related epitopes of the GABAA/benzodiazepine receptor.Neurosci. Lett. 115, 131–136.

    Article  PubMed  CAS  Google Scholar 

  • Wisden W., McNaughton L. A., Darlison M. G., Hunt S. P., and Barnard E. A. (1989) Differential distribution of GABA receptor mRNAs in bovine cerebellum-localization of 2 mRNA in Bergmann glia layer.Neurosci. Lett. 106, 7–12.

    Article  PubMed  CAS  Google Scholar 

  • Wyllie D. J. A., Symonds C. J., and Cull-Candy S. G. (1991) Activation of glutamate receptors and glutamate uptake in identified macroglial cells in rat cerebellar cultures.J. Physiol. 432, 235–255.

    PubMed  CAS  Google Scholar 

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  1. Department of Neurobiology, University of Heidelberg, Im Neuenheimer Feld 345, 6900, Heidelberg, FRG

    Gabriela v. Blankenfeld & Helmut Kettenmann

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  1. Gabriela v. Blankenfeld
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  2. Helmut Kettenmann
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v. Blankenfeld, G., Kettenmann, H. Glutamate and GABA receptors in vertebrate glial cells. Mol Neurobiol 5, 31–43 (1991). https://doi.org/10.1007/BF02935611

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