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Signalling Mechanisms — from Transcription Factors to Oxidative Stress pp 115–124Cite as

Modulation of the Ampa/Kainate Receptors by Protein Kinase C

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Part of the book series: NATO ASI Series ((ASIH,volume 92))

Abstract

Glutamate is the major excitatory neurotransmitter in the brain, and glutamate receptors mediate rapid excitatory synaptic transmission in the CNS. Glutamate activates ionotropic receptors and receptors coupled to guanine nucleotide-binding proteins (Schoepp and Conn, 1993; Schoepfer et al., 1994). Based on ligand binding assays, and on molecular biological and electrophysiological properties, the mammalian ionotropic glutamate receptors were subdivided into three classes: the N-methyl-D-aspartate (NMDA), S-α-amino-3-hydroxy-5-methyl-4-isoxazole-propionie acid (AMPA) and kainate receptors. The activity of these receptors is modulated during neuronal plasticity, most likely by phosphorylation (Raymond et al., 1993a). In this chapter we will review the basic structure of the non-NMDA ionotropic glutamate receptors, and the modulation of the channel activity by protein kinase C-dependent mechanisms. Finally, the role of these receptors and PKC in long term depression in the cerebellum is also discussed.

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References

  • Bettler B, Egejerg J, Harma G, Pecht G, Hermans-Borgmeyer I, Moll C, Stevens CF, Heinemann S (1992) Cloning of a putative glutamate receptor: a low affinity kainate-binding subunit. Neuron 8: 257–265.

    Article  PubMed  CAS  Google Scholar 

  • Bleakman D, Rusin KI, Chard PS, Glaum SR, Miller RJ (1992) Metabotropic glutamate receptors potentiate ionotropic glutamate responses in the rat dorsal horn. Mol Pharmacol 42:192–196.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Brorson JR, Bleakman D, Chard PS, Miller RJ (1992) calcium directly permeates kainate/α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors in cultured cerebellar Purkinje neurons. Mol Pharmacol 41: 603–608.

    PubMed  CAS  Google Scholar 

  • Browning MD, Dudek E (1992) Activators of protein kinase C increase the phosphorylation of the synapsins at sites of phosphorylation by cAMP-dependent and Ca2+/calmodulin-dependent protein kinase in the rat hippocampal slice. Synapse 10: 62–70.

    Article  PubMed  CAS  Google Scholar 

  • Burnashev N, Khodorova A, Jonas P, Helm PJ, Wisden W, Monyer H, Seeburg PH, Sakmann B (1992) Calcium permeable AMPA-kainate receptors in fusiform cerebellar glial cells. Science 256: 1566–1570.

    Article  PubMed  CAS  Google Scholar 

  • Carvalho AP, Ferreira IL, Carvalho AL, Duarte CB (1994) Glutamate receptor modulation of [3H]GABA release and intracellular calcium in cultured chick retina cells. Ann N Y Acad Sci. (in press)

    Google Scholar 

  • Chen L, Huang L-Y (1992) Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356: 521–523.

    Article  PubMed  CAS  Google Scholar 

  • Crepel F, Krupa M (1988) Activation of protein kinase C induces a long-term depression of glutamate sensitivity of cerebellar Purkinje cells. Brain Res 458: 397–410.

    Article  PubMed  CAS  Google Scholar 

  • Dildy-Mayfield JE, Harris RA (1994) Activation of protein kinase C inhibits kainate-induced currents in oocytes expressing glutamate receptor subunits. J Neurochem 62: 1639–1642.

    Article  PubMed  CAS  Google Scholar 

  • Duarte CB, Ferreira IL, Santos PF, Oliveira CR, Carvalho AP (1992) Ca2+-dependent release of [3H]GABA in cultured chick retina cells. Brain Res 591: 27–32.

    Article  PubMed  CAS  Google Scholar 

  • Duarte CB, Ferreira IL, Santos PF, Oliveira CR, Carvalho AP (1993) Glutamate increases the [Ca2+]i but stimulates [Ca2+]i independent release of [3H]GABA in cultured chick retina cells. Brain Res 611: 130–138.

    Article  PubMed  CAS  Google Scholar 

  • Duarte CB, Santos PF, Carvalho AP (1994) Mechanisms of [Ca2+]i by glutamate receptor agonists in cultured chick retina cells, (submitted)

    Google Scholar 

  • Egebjerg J, Bettler B, Hermans-Borgmeyer I, Heinemann S (1991) Cloning of a cDNA for a glutamate receptor activated by kamate but not by AMPA. Nature 351:745–748.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Henley JM, Barnard E (1991) Comparison of solubilised kainate and α-amino-3-hyroxy-5-methylisoxazolepropionate binding sites in chick cerebellum. J. Neurochem. 56: 702–705.

    Article  PubMed  CAS  Google Scholar 

  • Herb A, Burnashev N, Werner P, Sakmann B, Wisden W, Seeburg PH (1992) The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels wih distantly related subunits. Neuron 8: 775–785.

    Article  PubMed  CAS  Google Scholar 

  • Hescheler J, Schultz G (1993) G-proteins involved in the calcium channel signalling system. Curr Opin Neurobiol 3: 360–367.

    Article  PubMed  CAS  Google Scholar 

  • Hollmann M, O’Shea-Greenfield A, Rogers SW, Heinemann S (1989) Cloning by functional expression of a member of the glutamate receptor family. Nature 342: 643–648.

    Article  PubMed  CAS  Google Scholar 

  • Hollmann M, Hartley M, Heinemann S (1991) Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252: 1028–1031.

    Article  Google Scholar 

  • Huganir RL, Greengard P (1990) Regulation of neurotransmitter receptor desensitization by protein phosphorylation. Neuron 5: 555–567.

    Article  PubMed  CAS  Google Scholar 

  • Ito M (1989) Long-term potentiation. Ann Rev Neurosci 12: 85–102.

    Article  PubMed  CAS  Google Scholar 

  • Ito M, Karachot L (1992) Protein kinases and phosphatase inhibitors mediating long-term desensitization of glutamate receptors in cerebellar Purkinje cells. Neurosci Res 14: 27–38.

    Article  PubMed  CAS  Google Scholar 

  • Keinänen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMPA-selective glutamate receptors. Science 249: 556–560.

    Article  PubMed  Google Scholar 

  • Kelso SR, Nelson TE, Lkwiard JP (1992) Protein kinase C-mediated enhancement of NMDA currents in Xenopus oocytes. J Physiol (Lond) 449: 705–718.

    CAS  Google Scholar 

  • Linden DJ, Connor JA (1991) Participation of postsynaptic PKC in cerebellar long-term depression in culture. Science 254: 1656–1659.

    Article  PubMed  CAS  Google Scholar 

  • Linden DL, Connor JA (1993) Cellular mechanisms of long-term depression in the cerebellum. Curr Opin Neurobiol 3: 410–406.

    Article  Google Scholar 

  • Lomeli H, Wisden W, Kohler M, Keinanen K, Sommer B, Seeburg PH (1992) High-afinity kainate and domoate receptors in rat brain. FEBS Lett 307: 139–143.

    Article  PubMed  CAS  Google Scholar 

  • Mayer ML, Miller RJ (1990) Excitatory amino acid receptors, second messengers and regulation of intracellular Ca2+ in mamalian neurons. Trends Pharmacol Sci 11: 254–260.

    Article  PubMed  CAS  Google Scholar 

  • Mayer ML, Westbrook L (1987) Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurons. J. Physiol (Lond) 394: 501–527.

    CAS  Google Scholar 

  • McCleskey EW, Fox AP, Feldman D, Tsien RW (1986) Different types of calcium channels. J Exp Biol 124; 177–190.

    PubMed  CAS  Google Scholar 

  • McGlade-McCulloh E, Yamamoto H, Tan S-E, Brickey DA, Soderling TR (1993) Phosphorylation and regulation of glutamate receptors by caltium/calmodulin-dependent protein kinase II. Nature 362: 640–642.

    Article  PubMed  CAS  Google Scholar 

  • Messing RO, Carpenter CL, Greenberg DA (1988) Inhibition of calcium flux and calcium channel antagonist binding in the PC-12 neural cell line by phosbol esters and protein kinase C. Biochem Biophys Res Commun 136: 1049–1056.

    Article  Google Scholar 

  • Mintz I, Venema V, Swiderek K, Lee T, Bean B, Adams M (1992) P-type calcium channels blocked by the spider toin ω-Aga IVA. Nature 355: 827–829.

    Article  PubMed  CAS  Google Scholar 

  • Moran O, Dascal N (1989) Protein kinase C modulates neurotransmitter responses in Xenopus oocytes injected with rat brain RNA. Mol Brain Res 5:193–202.

    Article  PubMed  CAS  Google Scholar 

  • Mori-Okamoto K, Tatsuno J (1993) Intracellular mechanisms underlying the supression of AMPA responses by trans-ACPD in cultured chick Purkinje neurons. Mol Cell Neurosciences 4: 375–386.

    Article  CAS  Google Scholar 

  • Nakanishi N, Shneider NA, Axel R (1990) A family of glutamate receptor genes: evidence for the formation of heteromeric receptors with distinct channel properties. Neuron 5: 569–581.

    Article  PubMed  CAS  Google Scholar 

  • Prat AG, Bertorello AM, Ausiello DA, Cantiello HF (1993) Activation of epithelial Na+ channels by protein kinase A requires actin filaments. Am J Cell Physiol 265: C224–233

    CAS  Google Scholar 

  • Rane S, Dunlap K (1988) Kinase C activator 1,2-oleylacetyl-glycerol attenuates voltage-dependent calcium current in sensory neurons. Proc Natl Acad Sci USA 83: 184–188.

    Article  Google Scholar 

  • Raymond LA, Blackstone CD, Huganir RL (1993a) Phosphorylation of amino acid neurotransmitter receptors in synaptic plasticity. Trends Neurosci 16: 147–153.

    Article  PubMed  CAS  Google Scholar 

  • Raymond LA, Blackstone CD, Huganir RL (1993b) Phosphorylation and modulation of recombinant Glu R6 glutamate receptors by cAMP-dependent protein kinase. Nature 361: 637–641.

    Article  PubMed  CAS  Google Scholar 

  • Sakimura K, Monta T, Kushiya E, Mishina M (1992) Primary structure and expression of the gamma 2 subunit of the glutamate receptor channel selective for kainate. Neuron 8: 267–274.

    Article  PubMed  CAS  Google Scholar 

  • Sather WA, Tanabe T, Zhang J-F, Mori Y, Adams M, Tsien RW (1993) Distinctive biophysical and pharmacological poperties of class A (BI) calcium channel α1 subunits. Neuron 11: 291–303.

    Article  PubMed  CAS  Google Scholar 

  • Schoepfer R, Monyer H, Sommer B, Wisden W, Sprengel R, Kuner T, Lomeli H, Herb A, Köhler M, Burnashev N, Günther W, Ruppersberg P, Seeburg P (1994) Molecular biology of glutamate receptors. Prog Neurobiol 42: 353–357.

    Article  PubMed  CAS  Google Scholar 

  • Schoepp DD, Conn PJ (1993) Metabotropic glutamate receptors in brain function and pathology. Trends Pharmacol Sci 14: 13–20.

    Article  PubMed  CAS  Google Scholar 

  • Seeburg PH (1993) The molecular biology of mammalian glutamate receptor chanels. Trends Neurosci 16: 359–365.

    Article  PubMed  CAS  Google Scholar 

  • Shigemoto R, Abe T, Nomura S, Nakanishi S, Hirano T (1994) Antibodies inactivating mGluRl metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron 12: 1245–1255.

    Article  PubMed  CAS  Google Scholar 

  • Sigei E, Baur R (1988) Activation of protein kinase C differentially modulates neuronal Na+, Ca2+, and y-aminobutyrate type A channels. Proc Natl Acad Sci USA 85: 6192–6196.

    Article  Google Scholar 

  • Soderling TR, Tan SE, McGlade-McCulloh E, Yamamoto H, Fukunaga K (1993) Excitatory interactions between glutamate receptors and protein kinases. J Neurobiol 25: 304–311.

    Article  Google Scholar 

  • Somogyi P, Eshhar N, Teichberg VI, Roberts JD (1990) Subcellular localization of a putative kainate receptor in Bergman glial cells using a monoclonal antibody in the chick and fish cerebellar cortex. Neurosci. 35: 9–30.

    Article  CAS  Google Scholar 

  • Sommer B, Burnashev N, Verdoorn TA, Keinänen K, Sakmann B, Seeburg PH (1992) A glutamate receptor channel with high affinity for domoate and kainate. EMBO J 11:1651–1656.

    PubMed  CAS  Google Scholar 

  • Swope SL, Moss SJ, Blackstone CD, Huganir RL (1992) Phosphorylation of ligand-gated ion channels: a possible mode of synaptic plasticity. FASEB J 6: 2514–2523.

    PubMed  CAS  Google Scholar 

  • Taverna FA, Hampson DR (1994) Properties of a recombinant kainate receptor expressed in baculovirus-infected insect cells. Eur J Pharmacol 266: 181–186.

    Article  PubMed  CAS  Google Scholar 

  • Wang L-Y, Taverna FA, Huang X-P, MacDonald JF, Hampson DR (1993) Phosphorylation and modulation of a kainate receptor (GluR6) by cAMP-dependent protein kinase. Science 259: 1173–1175.

    Article  PubMed  CAS  Google Scholar 

  • Weeler D, Randall A, Tsien RW (1994) roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 264: 107–111.

    Article  Google Scholar 

  • Wenthold RJ, Yokotani N, Doi K, Wada K (1992) Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. J Biol Chem 267: 501–507.

    PubMed  CAS  Google Scholar 

  • Werner P, Voigt M, Keinänen K, Wisden W, Seeburg PH (1991) Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 351: 742–744.

    Article  PubMed  CAS  Google Scholar 

  • Worley PF, Baraban JM, Colvin JS, Snyder S (1987) Inositol trisphosphate receptor localization in brain: variable stoichiometry with protein kinase C. Nature 325: 159–161.

    Article  PubMed  CAS  Google Scholar 

  • Verdoorn TA, Burnashev N, Monyer H, Seeburg PH, Sakmann B (1991) Structural determinate of ion flow through recombinant glutamate receptor channels. Science 252: 1715–1718.

    Article  PubMed  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. Center for Neurosciences of Coimbra, Department of Zoology, University of Coimbra, 3049, Coimbra Codex, Portugal

    Carlos B. Duarte & Arsélio P. Carvalho

  2. Center for Neurosciences of Coimbra, Department of Biochemistry, University of Coimbra, 3049, Coimbra Codex, Portugal

    Ana L. Carvalho

Authors
  1. Carlos B. Duarte
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  2. Ana L. Carvalho
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  3. Arsélio P. Carvalho
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Editor information

Editors and Affiliations

  1. Department of Molecular and Cell Biology, University of California, 251 Life Science Addition, 94720, Berkeley, CA, USA

    Lester Packer

  2. Centre for Biomembranes and Lipid Enzymology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Karel W. A. Wirtz

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© 1995 Springer-Verlag Berlin Heidelberg

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Duarte, C.B., Carvalho, A.L., Carvalho, A.P. (1995). Modulation of the Ampa/Kainate Receptors by Protein Kinase C. In: Packer, L., Wirtz, K.W.A. (eds) Signalling Mechanisms — from Transcription Factors to Oxidative Stress. NATO ASI Series, vol 92. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79675-3_11

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  • DOI: https://doi.org/10.1007/978-3-642-79675-3_11

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-79677-7

  • Online ISBN: 978-3-642-79675-3

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