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Phosphorylation of Non-NMDA Glutamate Receptor Ion Channels

Implications for Synaptic Plasticity and Their Membrane Topology
  • Thomas R. Soderling
Part of the The Receptors book series (REC)

Abstract

Modulation of physiological functions by protein phosphorylation is perhaps the most common form of cellular regulation, since up to 30% of cellular proteins can be phosphorylated (Levenson et al., 1990). Cyclic adenosine monophosphate (cAMP)-dependent protein phosphorylation was pioneered in the area of glycogen metabolism (reviewed in Krebs, 1993) in the 1950s and 1960s by Edwin Krebs and Edmond Fischer. However, it was well known from the work of Earl Sutherland (reviewed in Robison et al., 1971) that the second messenger cAMP altered many physiological processes in addition to glycogen metabolism. Thus, once the cAMP-dependent protein kinase A (PKA) was purified, it was quickly determined this kinase was multifunctional and could phosphorylate numerous proteins outside of glycogen metabolism. Other multifunctional Ser/Thr protein kinases were later characterized (e.g., casein kinases, protein kinase C [PKC], and Ca++/calmodulin-dependent protein kinase II [CaM-kinase II]), and identification of new protein kinases, including tyrosine-specific protein kinases, and their substrates proliferated during the 1970–1980s (reviewed in Hanks, 1988).

Keywords

Glutamate Receptor Glycogen Metabolism Membrane Topology Glutamate Receptor Subunit Regulatory Phosphorylation Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Bennett, J. A. and Dingledine, R. (1995) Topology profile for a glutamate receptor: three transmembrane domains and a channel-lining reentrance membrane loop. Neuron 14, 373–384.PubMedCrossRefGoogle Scholar
  2. Bettler, B., Egebjerg, J., Sharma, G., Pecht, G., Hermans-Borgmeyer, I., Moll, C., Stevens, C. F., and Heinemann, S. (1992) Cloning of a putative glutamate receptor: a low affinity kainate-binding subunit. Neuron 8, 257–265.PubMedCrossRefGoogle Scholar
  3. Blackstone, C., Murphy, T. H., Moss, S. J., Baraban, J. M., and Huganir, R. L. (1994) Cyclic AMP and synaptic activity-dependent phosphorylation of AMPA-preferring glutamate receptors. J. Neurosci. 14, 7585–7593.PubMedGoogle Scholar
  4. Bliss, T. V. P. and Collingridge, G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31–39.PubMedCrossRefGoogle Scholar
  5. Boulter, J., Hollmann, M., O’Shea-Greenfield, A., Hrtley, M., Deneris, E., Maron, C., and Heinemann, S. (1990) Molecular cloning and functional expression of glutamate receptor subunit genes. Science 249, 1033–1037.PubMedCrossRefGoogle Scholar
  6. Browning, M. D. and Dudek, E. (1992) Activators of protein kinase C increase the phosphorylation of the synapsins at sites phosphorylated by cAMP-dependent and Ca2+/calmodulin-dependent protein kinase in the rat hippocampal slice. Synapse 10, 62–70.PubMedCrossRefGoogle Scholar
  7. Carr, D. W., Stofko-Hahn, R. E., Fraser, I. D. C., Cone, R. D., and Scott, J. D. (1992) Localization of the cAMP-dependent protein kinase to the postsynaptic densities by A-kinase anchoring proteins: characterization of AKAP 79. J. Biol. Chem. 267, 16,816–16,823.Google Scholar
  8. Chen, L. and Huang, L. Y. M. (1992) Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356, 521–523.PubMedCrossRefGoogle Scholar
  9. Colombini, M., Blachly-Dyson, E., and Forte, M. (1996) VDAC, a channel in the outer mitochondrial membrane, in Ion Channels, vol. 4 (Narahashi, T., ed.), Plenum, New York, pp. 169–202.Google Scholar
  10. Davies, S. A., Lester, R. A. J., Reymann, K. G., and Collingridge, G. L. (1989) Temporally distinct pre- and post-synaptic mechanisms maintain long-term potentiation. Nature 338, 500–503.PubMedCrossRefGoogle Scholar
  11. Fukunaga, K., Soderling, T. R., and Miyamoto, E. (1992) Activation of Ca2+/calmodulin-dependent protein kinase II and protein kinase C by glutamate in cultured rat hippocampal neurons. J. Biol. Chem. 267, 22,527–22,533.Google Scholar
  12. Fukunaga, K., Stoppini, L., Miyamoto, E., and Muller, D. (1993) Long-term potentiation is associated with an increased activity of Ca2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 268, 7863–7867.PubMedGoogle Scholar
  13. Gallagher, P., Henneberry, J., Wilson, I., Sambrook, J., and Gething, M. J. (1988) Addition of carbohydrate side chains at novel sites on influenza virus hemagglutinin can modulate the folding, transport, and activity of the molecule. J. Cell Biol. 107, 2059–2073.PubMedCrossRefGoogle Scholar
  14. Ginty, D. D., Kornhauser, J. M., Thompson, M. A., Bading, H., Mayo, K. E., Takahashi, J. S., and Greenberg, M. E. (1993) Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260, 238–241.PubMedCrossRefGoogle Scholar
  15. Greengard, P., Jen, J., Nairn, A. C., and Stevens, C. F. (1991) Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science 253, 1135–1138.PubMedCrossRefGoogle Scholar
  16. Hanks, S. K., Quinn, A. M., and Hunter, T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42–52.PubMedCrossRefGoogle Scholar
  17. Hanson, P. I., and Schulman, H. (1992) Neuronal Ca2+/calmodulin-dependent protein kinases. Annu. Rev. Biochem. 61, 559–601.PubMedCrossRefGoogle Scholar
  18. Hollmann, M., Maron, C., and Heinemann, S. (1994) N-glycosylation site tagging suggests a three transmembrane domain topology for the glutamate receptor GluR1. Neuron 13, 1331–1343.PubMedCrossRefGoogle Scholar
  19. Ito, I., Hidaka, H., and Sugiyama, H. (1991) Effects of KN-62, a specific inhibitor of calcium/calmodulin-dependent protein kinase II, on a long-term potentiation in the rat hippocampus. Neurosci. Lett. 121, 1119–1121.CrossRefGoogle Scholar
  20. Keinanen, K., Wisden, W., Sommer, B., Werner, P., Herb, A., Verdoorn, T. A., Sakmann, B., and Seeburg, P. H. (1990) A family of AMPA-selective glutamate receptors. Science 249, 556–560.PubMedCrossRefGoogle Scholar
  21. Keller, B. U., Hollmann, M., Heinemann, S., and Konnerth, A. (1992) Calcium influx through subunits GluR1GluR3 of kainate/AMPA receptor channels is regulated by cAMP dependent protein kinase. EMBO J. 11, 891–896.PubMedGoogle Scholar
  22. Kelly, P. T., McGuiness, T. L., and Greengard, P. (1984) Evidence that the major postsynaptic density protein is a component of a Ca2+/calmodulin-dependent protein kinase. Proc. Natl Acad. Sci. USA 81, 945–949.PubMedCrossRefGoogle Scholar
  23. Kennedy, M. B., Bennett, M. K., and Erondu, N. G. (1983) Biochemical and immunochemical evidence that the “major postsynaptic density protein” is a subunit of calmodulin-dependent protein kinase. Proc. Natl. Acad. Sci. USA 80, 7357–7361.PubMedCrossRefGoogle Scholar
  24. Knapp, A. G. and Dowling, J. E. (1987) Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437–439.PubMedCrossRefGoogle Scholar
  25. Kolaj, M., Cerne, R., Cheng, G., Brickey, D. A., and Randic, M. (1994) Alpha sub-unit of calcium/calmodulin-dependent protein kinase enhances excitatory amino acid and synaptic responses of rat spinal dorsal horn neurons. J. Neurophysiol. 72, 2525–2531.PubMedGoogle Scholar
  26. Krebs, E. G. (1993) Nobel lecture. Protein phosphorylation and cellular regulation I. Biosci. Rep. 13, 127–142.PubMedCrossRefGoogle Scholar
  27. Kullmann, D. M., Perkel, D. J., Manabe, T., and Nicoll, R. A. (1992) Ca2+ entry via postsynaptic voltage-sensitive Ca2+ channels can transiently potentiate excitatory synaptic transmission in the hippocampus. Neuron 9, 1175–1183.PubMedCrossRefGoogle Scholar
  28. Levenson, R. M., Anderson, G. M., Cohn, J. A., and Blackshear, P. J. (1990) Giant two-dimensional gel electrophoresis: methodological update and comparison with intermediate-format gel systems. Electrophoresis 11, 269–279.PubMedCrossRefGoogle Scholar
  29. Liman, E. R., Knapp, A. G., and Dowling, J. E. (1989) Enhancement of kainate-gated currents in retinal horizontal cells by cAMP-dependent protein kinase. Brain Res. 481, 399–402.PubMedCrossRefGoogle Scholar
  30. Liu, Y. C., and Storm, D. R. (1990) Regulation of free calmodulin levels by neuromodulin: neuron growth and regeneration. Trends Pharmacol. Sci. 11, 107–111.PubMedCrossRefGoogle Scholar
  31. Lledo, P. M., Hjelmstad, G., Mukherji, S., Soderling, T. R., Malenka, R. C., and Nicoll, R. A. (1995) CaM-kinase II and LTP enhance synaptic transmission by the same mechanism. Proc. Natl. Acad. Sci. USA 92, 11,175–11,179.CrossRefGoogle Scholar
  32. Lynch, G., Larson, J., Kelso, S., Barrionuevo, G., and Schottler, F. (1983) Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305, 719–721.PubMedCrossRefGoogle Scholar
  33. MacDonald, R. L. and Olsen, R. W. (1994) GABAA receptor channels. Annu. Rev. Neurosci. 17, 569–602.PubMedCrossRefGoogle Scholar
  34. MacNicol, N. and Schulman, H. (1992) Cross-talk between protein kinase C and multifunctional Ca2+/calmodulin-dependent protein kinase. J. Biol Chem. 267, 12,197–12,201.Google Scholar
  35. Malenka, R. C. (1991) The role of postsynaptic calcium in the induction of long-term potentiation. Mol. Neurobiol. 5, 289–295.PubMedCrossRefGoogle Scholar
  36. Malinow, R., Schulman, H., and Tsien, R. W. (1989) Inhibition of postsynaptic pKC or CaM-KII blocks induction but not expression of LTP. Science 245, 862–866.PubMedCrossRefGoogle Scholar
  37. McGlade-McCulloh, E., Yamamoto, H., Tan, S. E., Brickey, D. A., and Soderling, T. R. (1993) Phosphorylation and regulation of glutamate receptors by calcium/calmodulin-dependent protein kinase II. Nature 362, 640–642.PubMedCrossRefGoogle Scholar
  38. Moln’ar, E., Baude, A., Patel, P. B., Somogyi, P., and McLlhinney, R. A. (1993) Biochemical and immunocytochemical characterization of antipeptide antibodies to a cloned GluR1 glutamate receptor subunit. Neurosci. 53, 307–326.CrossRefGoogle Scholar
  39. Nakazawa, K., Mikawa, S., Hashikawa, T., and Ito, M. (1995) Transient and persistent phosphorylations of AMPA-type glutamate receptor subunits in cerebellar purkinje cells. Neuron 15, 697–709.PubMedCrossRefGoogle Scholar
  40. Ortega, A., and Teichberg, V. I. (1990) Phosphorylation of the 49-kDA putative subunit of the chick cerebellar kainate receptor and its regulation by kainatergic ligands. J. Biol. Chem. 265, 21,404–21,406.Google Scholar
  41. Petralia, R. S. and Wenthold, R. J. (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318, 329–354.PubMedCrossRefGoogle Scholar
  42. Pettit, D. L., Perlman, S., and Malinow, R. (1994) Potentiated transmission and prevention of further LTP by increased CaM-KII activity in postsynaptic hippocampal slice neurons. Science 266, 1881–1885.PubMedCrossRefGoogle Scholar
  43. Raymond, L. A., Blackstone, C. D., and Huganir, R. L. (1993) Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature 361, 637–641.PubMedCrossRefGoogle Scholar
  44. Reymann, K. G. (1993) Mechanisms underlying synaptic long-term potentiation in the hippocampus: focus on postsynaptic glutamate receptors and protein kinases. Functional Neurol. (Suppl. 8), 7–32.Google Scholar
  45. Robison, G. A., Butcher, R. W., and Sutherland, E. W. (1971) Cyclic AMP. Academic, New York.Google Scholar
  46. Roche, K. W., O’Brien, R. J., Mammen, A. L., Bernhardt, J., and Huganir, R. L. (1996) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16, 1179–1188.PubMedCrossRefGoogle Scholar
  47. Roche, K. W., Raymond, L. A., Blackstone, C., and Huganir, R. L. (1994a) Transmembrane topology of the glutamate receptor subunit GluR6. J. Biol. Chem. 269, 11,679–11,682.Google Scholar
  48. Roche, K. W., Tingley, W., and Huganir, R. L. (1994b) Glutamate receptor phosphorylation and synaptic plasticity. Curr. Opin. Neurobiol. 4, 383–388.PubMedCrossRefGoogle Scholar
  49. Rosenmund, C., Carr, D. W., Dergeson, S. E., Nilaver, G., Scott, J. D., and Westbrook, G. L. (1994) Anchoring of protein kinase A is required for modulation of AMPA/ kainate receptors on hippocampal neurons. Nature 368, 853–856.PubMedCrossRefGoogle Scholar
  50. Silva, A. J., Paylor, R., Wehner, J. M., and Tonegawa, S. (1992a) Impaired spatial learning in a-calcium-calmodulin kinase II mutant mice. Science 257, 206–209.PubMedCrossRefGoogle Scholar
  51. Silva, A. J., Stevens, C. F., Tonegawa, S., and Wang, Y. (1992b) Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice. Science 257, 201–206.PubMedCrossRefGoogle Scholar
  52. Slatin, S. L., Qiu, X. Q., Jakes, K. S., and Finkelstein, A. (1994) Identification of a translocated protein segment in a voltage-dependent channel. Nature 371, 158–161.PubMedCrossRefGoogle Scholar
  53. Soderling, T. R. (1995) Calcium-dependent protein kinases in learning and memory, in Advances in Second Messenger and Phosphoprotein Research, vol. 30 (Means, A. R., ed.), Raven, New York, pp. 175–189.Google Scholar
  54. Stern-Bach, Y., Bettler, B., Hartley, M., Sheppard, P. O., O’Hare, P. J., and Heinemann, S. F. (1994) Agonist selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino acid-binding proteins. Neuron 13, 1345–1357.PubMedCrossRefGoogle Scholar
  55. Susuki, T., Okumura-Noji, K., Ogura, A., Kudo, Y., and Tanaka, R. (1992) Antibody specific for the Thr-286-autophosphorylated alpha subunit of Ca2+/calmodulin-dependent protein kinase II. Proc. Natl. Acad. Sci. USA 89, 109–113.CrossRefGoogle Scholar
  56. Swope, S. L., Moss, S. J., Blackstone, C. D., and Huganir, R. L. (1992) Phosphorylation of ligand-gated ion channels: a possible mode of synaptic plasticity. FASEB J. 6, 2514–2523.PubMedGoogle Scholar
  57. Tan, S. E., Wenthold, R. J., and Soderling, T. R. (1994) Phosphorylation of AMPA-type glutamate receptors by calcium/calmodulin-dependent protein kinase II and protein kinase C in cultured hippocampal neurons. J. Neurosci. 14, 1123–1129.PubMedGoogle Scholar
  58. Taverna, F., Wang, L. Y., MacDonald, J. F., and Hampson, D. R. (1994) A transmembrane model for an ionotropic glutamate receptor predicted on the basis of the location of asparagine-linked oligosaccharides. J. Biol Chem. 269, 14,159–14,164.Google Scholar
  59. Tingley, W. G., Roche, K. W., Thompson, A. K., and Huganir, R. L. (1993) Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364, 70–73.PubMedCrossRefGoogle Scholar
  60. Urushihara, H., Tohda, M., and Nomura, Y. (1992) Selective potentiation of N-methyl-D-aspartate-induced current by protein kinase C in Xenopus oocytes injected with rat brain RNA. J. Biol Chem. 267, 11,697–11,700.Google Scholar
  61. Wang, L. Y., Dudek, E. M., Browning, M. D., and MacDonald, J. F. (1994) Modulation of AMPA/kainate receptors in cultured murine hippocampal neurones by protein kinase C. J. Physiol 475(3), 431–437.PubMedGoogle Scholar
  62. Wang, L. Y., Salter, M. W., and MacDonald, J. F. (1991) Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 253, 1132–1135.PubMedCrossRefGoogle Scholar
  63. Wang, L. Y., Taverna, F. A., Huang, X. P., MacDonald, J. F., and Hampson, D. R. (1993) Phosphorylation and modulation of a kainate receptor (GluR6) by cAMP-dependent protein kinase. Science 259, 1173–1175.PubMedCrossRefGoogle Scholar
  64. Wyllie, D. J. A. and Nicoll, R. A. (1994) A role for protein kinases and phosphatases in the Ca2+-induced enhancement of hippocampal AMPA receptor-mediated synaptic responses. Neuron 13, 635–643.PubMedCrossRefGoogle Scholar
  65. Yakel, J. L., Vissavajhala, P., Derkach, V. A., Brickey, D. A., and Soderling, T. R. (1995) Identification of a Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in non-N-methyl-D-aspartate glutamate receptors. Proc. Natl Acad. Sci. USA 92, 1376–1380.PubMedCrossRefGoogle Scholar

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© Humana Press Inc. 1997

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  • Thomas R. Soderling

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