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Functional Properties of Kainate Receptors

  • James E. Huettner
Part of the The Receptors book series (REC)

Abstract

Kainic acid was first isolated from seaweed more than 40 yr ago (see McGeer et al., 1978 for a review of early work). By the mid-1970s, the excitatory and neurotoxic actions of kainate were well established, and the hypothesis that kainate acted on a specific subset of excitatory amino acid receptors had been developed (Watkins and Evans, 1981). More recent work has shown that kainate can activate several different receptor subtypes, including α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) receptors (Patneau and Mayer, 1991), kainate receptors (Agrawal and Evans, 1986; Huettner, 1990), and lower-mol wt kainate binding proteins in some species (see Henley, 1994). The current definition of these subtypes stems from a comparison of physiological responses evoked at native receptors to the behavior of cloned receptor subunits expressed in heterologous cells. AMPA receptors are formed by the subunits GluR1–4, also known as GluR-A-D (Boulter et al., 1990; Keinänen et al., 1990; Nakanishi et al., 1990). A large body of evidence indicates that postsynaptic AMPA receptors mediate fast excitatory transmission throughout most of the central nervous system (CNS) (reviewed by Collingridge and Lester, 1989; Monaghan et al., 1989). Kainate activates these receptors with lower affinity than AMPA, glutamate, or quisqualate, but kainate produces a much larger steady-state current than the other agonists (Patneau and Mayer, 1991).

Keywords

Glutamate Receptor AMPA Receptor Mossy Fiber Kainic Acid Domoic Acid 
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References

  1. Agrawal, S. G. and Evans, R. H. (1986) The primary afferent depolarizing action of kainate in the rat. Br. J. Pharmacol 87, 345–355.PubMedGoogle Scholar
  2. Ault, B. and Hildebrand, L. M. (1993) Activation of nociceptive reflexes by peripheral kainate receptors. J. Pharmacol Exp. Ther. 265, 927–932.PubMedGoogle Scholar
  3. Bahn, S., Volk, B., and Wisden, W. (1994) Kainate receptor gene expression in the developing rat brain. J. Neurosci.14, 5525–5547.PubMedGoogle Scholar
  4. Barres, B., Koroshetz, W. J., Swartz, K. J., Chun, L. L. Y., and Corey, D. P. (1990) Ion channel expression by white matter glia: the 0–2A glial progenitor cell. Neuron 4, 507–524.PubMedCrossRefGoogle Scholar
  5. Bekkers, J. M. and Stevens, C. F. (1989) NMDA and non-NMDA receptors are colo-calized at individual excitatory synapses in cultured rat hippocampus. Nature 341,230–233.PubMedCrossRefGoogle Scholar
  6. Ben-Ari, Y. and Gho, M. (1988) Long-lasting modification of the synaptic properties of rat CA3 hippocampal neurones induced by kainic acid. J. Physiol (London) 404, 365–384.PubMedGoogle Scholar
  7. Bennett, J. A. and Dingledine, R. (1995) Topology profile for a glutamate receptor: three transmembrane domains and a channel-lining reentrant membrane loop. Neuron 14, 373–384.PubMedCrossRefGoogle Scholar
  8. Bergold, P. J., Casaccia-Bonnefil, P., Xiu-Liu, Z., and Federoff, H. J. (1993) Transsynaptic neuronal loss induced in hippocampal slice cultures by a herpes simplex virus vector expressing the GluR6 subunit of the kainate receptor. Proc. Natl. Acad. Sci. USA 90, 6165–6169.PubMedCrossRefGoogle Scholar
  9. Bernard, A. and Khrestchatisky, M. (1994) Assessing the extent of RNA editing in the TMII regions of GluR5 and GluR6 kainate receptors during rat brain development. J. Neurochem. 62, 2057–2060.PubMedCrossRefGoogle Scholar
  10. Bettler, B., Boulter, J., Hermans-Borgmeyer, I., O’Shea-Greenfield, A., Deneris, E., Moll, C, Borgmeyer, U., Hollmann, M., and Heinemann, S. (1990) Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5, 583–595.PubMedCrossRefGoogle Scholar
  11. 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
  12. Boulter, J., Hollmann, M., O’Shea-Greenfield, A., Hartley, 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
  13. Burnashev, N., Moyner, H., Seeburg, P. H., and Sakmann, B. (1992) Divalent ion permeability of AMP A receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189–198.PubMedCrossRefGoogle Scholar
  14. Chittajallu, R., Vignes, M., Dev, K. K., Barnes, J. M., Collingridge, G. L., and Henley, J. M. (1996) Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 379, 78–81.PubMedCrossRefGoogle Scholar
  15. Collingridge, G. L. and Lester, R. A. (1989) Excitatory amino acid receptors in the vertebrate CNS. Pharmacol. Rev. 41, 143–210.PubMedGoogle Scholar
  16. Coyle, J. T. (1983) Neurotoxic action of kainic acid. J. Neurochem. 41, 1–11.PubMedCrossRefGoogle Scholar
  17. Davies, J., Evans, R. H., Francis, A. A., and Watkins, J. C. (1979) Excitatory amino acid receptors and synaptic excitation in the mammalian CNS. J. Physiol. (Paris) 75,641–654.Google Scholar
  18. Dingledine, R., Hume, R. I., and Heinemann, S. F. (1992) Structural determinants of barium permeation and rectification in non-NMDA glutamate receptor channels. J. Neurosci. 12, 4080–4087.PubMedGoogle Scholar
  19. Dodd, J. and Jessell, T. M. (1985) Lactoseries carbohydrates specify subsets of dorsal root ganglion neurons projecting to the superficial dorsal horn of rat spinal cord. J. Neurosci. 5, 3278–3294.PubMedGoogle Scholar
  20. Donevan, S. D. and Rogawski, M. A. (1993) GYKI 52466, a 2,3-benzodiazepine, is a highly selective, noncompetitive antagonist of AMPA/kainate receptor responses. Neuron 10,51–59.PubMedCrossRefGoogle Scholar
  21. Donevan, S. D., Yamaguchi, S., and Rogawski, M. A. (1994) Non-N-methyl-D-aspartate receptor antagonism by 3-N-substituted 2,3-benzodiazepines: relationship to anticonvulsant activity. J. Pharmacol. Exp. Ther. 271, 25–29.PubMedGoogle Scholar
  22. Egebjerg, J., Bettler, B., Hermans-Borgmeyer, I., and Heinemann, S. (1991) Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351, 745–748.PubMedCrossRefGoogle Scholar
  23. Egebjerg, J. and Heinemann, S. F. (1993) Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc. Natl. Acad. Sci. USA 90, 755–759.PubMedCrossRefGoogle Scholar
  24. Evans, R. H., Evans, S. J., Pook, P. C, and Sunter, D. C. (1987) A comparison of excitatory amino acid antagonists acting at primary afferent C fibres and motoneurones of the isolated spinal cord of the rat. Br. J. Pharmacol. 91, 531–537.PubMedGoogle Scholar
  25. Fisher, R. S. and Alger, B. E. (1984) Electrophysiological mechanisms of kainic acid-induced epileptiform activity in the rat hippocampal slice. J. Neurosci. 4,1312–1323.PubMedGoogle Scholar
  26. Fitzgerald, M. and Woolf, C. J. (1981) Effects of cutaneous nerve and intraspinal conditioning on C-fibre afferent terminal excitability in decerebrate spinal rats. J. Physiol. 318, 25–39.PubMedGoogle Scholar
  27. Gaiarsa, J.-L., Zagrean, L., and Ben-Ari, Y. (1994) Neonatal irradiation prevents the formation of hippocampal mossy fibers and the epileptic action of kainate on rat CA3 pyramidal neurons. J. Neurophysiol. 71,204–215.PubMedGoogle Scholar
  28. Garthwaite, J. and Garthwaite, G. (1983) The mechanism of kainic acid neurotoxicity. Nature 305, 138–140.PubMedCrossRefGoogle Scholar
  29. Good, P. F., Huntley, G. W., Rogers, S. W., Heinemann, S. F., and Morrison, J. H. (1993) Organization and quantitative analysis of kainate receptor subunit GluR5–7 immuno-reactivity in monkey hippocampus. Brain Res. 624, 347–353.PubMedCrossRefGoogle Scholar
  30. Greenamyre, J. T. and Young, A. B. (1989) Synaptic localization of striatal NMDA, quisqualate and kainate receptors. Neurosci. Lett. 101, 133–137.PubMedCrossRefGoogle Scholar
  31. Hampson, D. R., Huie, D., and Wenthold, R. J. (1987) Solubilization of kainic acid binding sites from rat brain. J. Neurochem. 49, 1209–1215.PubMedCrossRefGoogle Scholar
  32. Henley, J. M., Ambrosini, A., Rodriguez-Ithurralde, D., Sudan, H., Brackley, P., Kerry, C, Mellor, I, Abutidze, K., Usherwood, P. N. R., and Barnard, E. A. (1992) Purified unitary kainate/α-amino-3-hydroxy-5-methylisooxazole propionate (AMPA) and kainate/AMPA/N-methyl-D-aspartate receptors with interchangeable subunits. Proc. Natl. Acad. Sci. USA 89, 4806–4810.PubMedCrossRefGoogle Scholar
  33. Henley, J. M. (1994) Kainate binding proteins: phylogeny, structures and possible functions. Trends Pharmacol. Sci. 15, 182–190.PubMedCrossRefGoogle Scholar
  34. Hentall, I. D. and Fields, H. L. (1979) Segmental and descending influences on single intraspinal C-fibres. J. Neurophysiol. 42, 1527–1537.PubMedGoogle Scholar
  35. Herb, A., Burnashev, N, Werner, P., Sakmann, B., Wisden, W., and Seeburg, P. H. (1992) The KA2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8, 775–785.PubMedCrossRefGoogle Scholar
  36. 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
  37. Huettner, J. E. (1990) Glutamate receptor channels in rat DRG neurons: activation by kainate and quisqualate and blockade of desensitization by Con A. Neuron 5,255–266.PubMedCrossRefGoogle Scholar
  38. Hume, R. I., Dingledine, R., and Heinemann, S. F. (1991) Identification of a site in glutamate receptor subunits that controls calcium permeability. Science 253, 1028–1031.PubMedCrossRefGoogle Scholar
  39. Huntley, G. W., Rogers, S. W., Moran, T., Janssen, W., Archin, N., Vickers, J. C, Cauley, K., Heinemann, S. F., and Morrison, J. H. (1993) Selective distribution of kainate receptor subunits immunoreactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. J. Neurosci. 13, 2965–2981.PubMedGoogle Scholar
  40. Ito, I., Tanabe, C, Kohda, A., and Sugiyama, H. (1990) Allosteric potentiation of quisqualate receptors by a nootropic drug, aniracetam. J. Physiol. (London) 424,533–543.PubMedGoogle Scholar
  41. Johansen, T. H., Drejer, J., Wätjen, F., and Nielsen, E. Ø. (1993) A novel non-NMDA antagonist shows selective displacement of low-affinity [3H]kainate binding. Eur. J. Pharmacol. 246, 195–204.PubMedCrossRefGoogle Scholar
  42. Jonas, P. and Sakmann, B. (1992) Glutamate receptor channels in isolated patches from CA 1 and CA3 pyramidal cells of rat hippocampal slices. J. Physiol. (London) 455, 143–171.PubMedGoogle Scholar
  43. Kashiwabuchi, N., Ikeda, K., Araki, K., Hirano, T., Shibuki, K., Takayama, C, Inoue, Y., Kutsuwada, T., Yagi, T., Kang, Y., Aizawa, S., and Mishina M. (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluRδ2 mutant mice. Cell 81, 245–252.PubMedCrossRefGoogle Scholar
  44. Keinänen, 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
  45. Köhler, M., Burnashev, N., Sakmann, B., and Seeburg, P. H. (1993) Determinants of Ca2+ permeability in both TM1 and TM2 of high-affinity kainate receptor channels: diversity by RNA editing. Neuron 10, 491–500.PubMedCrossRefGoogle Scholar
  46. Lerma, J., Paternain, A. V., Naranjo, J. R., and Mellström, B. (1993) Functional kainate selective glutamate receptors in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 90, 11,688–11,692.CrossRefGoogle Scholar
  47. Lomeli, H., Wisden, W., Köhler, M., Keinänen, K., Sommer, B., and Seeburg, P. H. (1992) High-affinity kainate and domoate receptors in rat brain. FEBS Lett. 307, 139–143.PubMedCrossRefGoogle Scholar
  48. Malva, J. O., Ambrósio, A. F., Cunha, R. A., Ribeiro, J. A., Carvalho, A. P., and Carvalho, C. M. (1995) A functionally active pre-synaptic high-affinity kainate receptor in the rat hippocampal CA3 subregion. Neurosci. Lett. 185, 83–86.PubMedCrossRefGoogle Scholar
  49. McGale, E. H. F., Pye, I. F., Stonier, C, Hutchinson, E. C, and Aber, G. M. (1977) Studies of the inter-relationship between cerebrospinal fluid and plasma amino acid concentrations in normal individuals. J. Neurochem. 29, 291–297.PubMedCrossRefGoogle Scholar
  50. McGeer, E. G., Olney, J. W., and McGeer, P. L., eds. (1978) Kainic Acid as a Tool in Neurobiology. Raven, NY.Google Scholar
  51. Monaghan, D. T. and Cotman, C. W. (1982) The distribution of [3H]kainic acid binding sites in the rat CNS as determined by autoradiography. Brain Res. 252, 91–100.PubMedCrossRefGoogle Scholar
  52. Monaghan, D. T., Bridges, R. J., and Cotman, C. W. (1989) The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the CNS. Annu. Rev. Pharmacol. Toxicol. 29, 365–402.PubMedCrossRefGoogle Scholar
  53. Nadler, J. V., Perry, B. W., and Cotman, C. W. (1978) Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 271, 676,677.CrossRefGoogle Scholar
  54. Nakanishi, N., Shneider, N. A., and Axel, R. (1990) A family of glutamate receptor genes: evidence for the formation of heteromultimeric receptors with distinct channel properties. Neuron 5, 569–581.PubMedCrossRefGoogle Scholar
  55. Ozaki, M., Aitken, P. G., and Nadler, J. V. (1988) Mossy fiber lesion reduces the probability that kainic acid will provoke CA3 hippocampal pyramidal cell bursting. Brain Res. 440, 352–356.CrossRefGoogle Scholar
  56. Partin, K. M., Patneau, D. K., Winters, C. A., Mayer, M. L., and Buonanno, A. (1993) Selective modulation of desensitization at AMPA vs kainate receptors by cyclo-thiazide and concanavalin A. Neuron 11, 1069–1082.PubMedCrossRefGoogle Scholar
  57. Partin, K. M., Bowie, D., and Mayer, M. L. (1995) Structural determinants of allosteric regulation in alternatively spliced AMPA receptors. Neuron 14, 833–843.PubMedCrossRefGoogle Scholar
  58. Paternain, A. V., Morales, M., and Lerma, J. (1995) Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14, 185–189.PubMedCrossRefGoogle Scholar
  59. Patneau, D. K. and Mayer, M. L. (1991) Kinetic analysis of interactions between kainate and AMPA: evidence for activation of a single receptor in mouse hippocampal neurons. Neuron 6, 785–798.PubMedCrossRefGoogle Scholar
  60. Patneau, D. K., Vyklicky, L. Jr., and Mayer, M. L. (1993) Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. J. Neurosci. 13, 3496–3509.PubMedGoogle Scholar
  61. Patneau, D. K., Wright, P. W., Winters, C, Mayer, M. L., and Gallo, V. (1994) Glial cells of the oligodendrocyte lineage express both kainite — and AMPA-preferring subtypes of glutamate receptor. Neuron 12, 357–371.PubMedCrossRefGoogle Scholar
  62. Perl, T. M., Bédard, L., Kosatsky, T., Hockin, J. C, Todd, E., and Remis, R. S. (1990) An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. N Engl. J. Med. 322, 1775–1780.PubMedCrossRefGoogle Scholar
  63. Petralia, R. S., Wang, Y.-X., and Wenthold, R. J. (1994) Histological and ultra-structural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 349, 85–110.PubMedCrossRefGoogle Scholar
  64. Pook, P., Brugger, F., Hawkins, N. S., Clark, K. C, Watkins, J. C, and Evans, R. H. (1993) A comparison of the actions of agonists and antagonists at non-NMDA receptors of C-fibres and motoneurones of the immature rat spinal cord in vitro. Br. J. Pharmacol. 108, 179–184.PubMedGoogle Scholar
  65. Puchalski, R. B., Louis, J.-C., Brose, N., Traynelis, S. F., Egebjerg, J., Kukekov, V., Wenthold, R. J., Rogers, S. W., Lin, F., Moran, T., Morrison, J. H., and Heinemann, S. F. (1994) Selective RNA editing and subunit assembly of native glutamate receptors. Neuron 13, 131–147.PubMedCrossRefGoogle Scholar
  66. 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
  67. Regan L. J., Dodd, J., Barondes S. H., and Jessell, T. M. (1986) Selective expression of endogenous lactose-binding lectins and lactoseries glycoconjugates in subsets of rat sensory neurons. Proc. Natl. Acad. Sci. USA 83, 2248–2252.PubMedCrossRefGoogle Scholar
  68. Represa, A., Tremblay, E., and Ben-Ari, Y. (1987) Kainate binding sites in the hippocampal mossy fibers: localization and plasticity. Neuroscience 20, 739–748.PubMedCrossRefGoogle Scholar
  69. Robinson, J. H. and Deadwyler, S. A. (1981) Kainic acid produces depolarization of CA3 pyramidal cells in the in vitro hippocampal slice. Brain Res. 221, 117–127.PubMedCrossRefGoogle Scholar
  70. Sakimura, K., Morita, T., Kushiya, E., and Mishina, M. (1992) Primary structure and expression of the γ2 subunit of the glutamate receptor channel selective for kainate. Neuron 8, 267–274.PubMedCrossRefGoogle Scholar
  71. Schaumburg, H. H., Byck, R., Gerstl, R., and Mashman, J. H. (1969) Monosodium L-glutamate: its pharmacology and role in the Chinese restaurant syndrome. Science 163, 826–828.PubMedCrossRefGoogle Scholar
  72. Sommer, B., Kohler, M., Sprengel, R., and Seeburg, P. H. (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11–19.PubMedCrossRefGoogle Scholar
  73. Sommer, B., Burnashev, N., Verdoorn, T. A., Keinänen, K., Sakmann, B., and Seeburg, P. H. (1992) A glutamate receptor channel with high-affinity for domoate and kainate. EMBO J. 11, 1651–1656.PubMedGoogle Scholar
  74. Spruston, N., Jonas, P., and Sakmann, B. (1995) Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J. Physiol (London) 482, 325–352.PubMedGoogle Scholar
  75. Stern-Bach, Y., Bettler, B., Hartley, M., Sheppard, P. O., O’Hara, P. J., and Heinemann, S. F. (1995) Agonist selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino acid-binding proteins. Neuron 13,1345–1357.CrossRefGoogle Scholar
  76. Unnerstall, J. R. and Wamsley, J. K. (1983) Autoradiographic localization of high-affinity [3H]kainic acid binding sites in the rat forebrain. Eur. J. Pharmacol. 86, 361–371.PubMedCrossRefGoogle Scholar
  77. Verdoorn, T. A., Johansen, T. H., Drejer, J., and Nielsen, E. Ø. (1994) Selective block of recombinant glur6 receptors by NS-102, a novel non-NMDA receptor antagonist. Eur. J. Pharmacol 269,43–49.PubMedCrossRefGoogle Scholar
  78. 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
  79. Watkins, J. C. and Evans, R. H. (1981) Excitatory amino acid transmitters. Annu. Rev. Pharmacol Toxicol 21, 165–204.PubMedCrossRefGoogle Scholar
  80. Wenthold, R. J., Trumpy, V. A., Zhu, W.-S., and Petralia, R. S. (1994) Biochemical and assembly properties of GluR6 and KA2, two members of the kainate receptor family, determined with subunit specific antibodies. J. Biol. Chem. 269, 1332–1339.PubMedGoogle Scholar
  81. Werner, P., Voigt, M., Keinänen, K., Wisden, W., and Seeburg, P. H. (1991) Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 351, 742–744.PubMedCrossRefGoogle Scholar
  82. Westbrook, G. L. and Lothman, E. W. (1983) Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res. 273, 97–109.PubMedCrossRefGoogle Scholar
  83. Wilding, T. J. and Huettner, J. E. (1995) Differential antagonism of a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-preferring and kainate preferring receptors by 2,3-benzodiazepines. Mol. Pharmacol. 47, 582–587.PubMedGoogle Scholar
  84. Wisden, W. and Seeburg, P. H. (1993) A complex mosaic of high-affinity kainate receptors in rat brain. J. Neurosci. 13, 3582–3598.PubMedGoogle Scholar
  85. Wolf, G. and Keilhoff, G. (1983) Kainate resistant neurons in peripheral ganglia of the rat. Neurosci. Lett. 43, 1–5.PubMedCrossRefGoogle Scholar
  86. Wong, L. A. and Mayer, M. L. (1993) Differential modulation by cyclothiazide and con-canavalin A of desensitization at native a-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid — and kainate-preferring glutamate receptors. Mol. Pharmacol. 44, 504–510.PubMedGoogle Scholar
  87. Wong, L. A., Mayer, M. L., Jane, D. E., and Watkins, J. C. (1994) Willardines differentiate agonist binding sites for kainate- vs AMPA-preferring glutamate receptors in DRG and hippocampal neurons. J. Neurosci.14, 3881–3897.PubMedGoogle Scholar
  88. Yamada, K. A. and Tang, C.-M. (1993) Benzothiadiazines inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents. J. Neurosci. 13,3904–3915.PubMedGoogle Scholar
  89. Zorumski, C. F., Yamada, K. A., Price, M. T., and Olney, J. W. (1993) A benzodiazepine recognition site associated with the non-NMDA glutamate receptor. Neuron 10,61–67.PubMedCrossRefGoogle Scholar

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© Humana Press Inc. 1997

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  • James E. Huettner

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