Hippocampal Kainate Receptors

Vitamins and Hormones

Volumn 82, Issue , 2010, Pages 167-184

  Bloss, Erik B ^a   Hunter, Richard G ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Corticosteroids; Epileptogenesis; Hippocampus; Kainate receptors; Mossy fibers

Indexed keywords

GLUTAMIC ACID; KAINIC ACID RECEPTOR;

ANIMAL; EPILEPSY; HIPPOCAMPUS; HUMAN; MENTAL DISEASE; METABOLISM; NERVE CELL PLASTICITY; RAT; REVIEW;

ANIMALS; EPILEPSY; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; MENTAL DISORDERS; NEURONAL PLASTICITY; RATS; RECEPTORS, KAINIC ACID;

EID: 77955897319     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0083-6729(10)82009-6     Document Type: Chapter

References (71)

1. Ahmad, Y., Bhatia, M.S., Mediratta, P.K., Sharma, K.K., Negi, H., Chosdol, K., Sinha, S., Association between the ionotropic glutamate receptor kainate3 (GRIK3) Ser310Ala polymorphism and schizophrenia in the Indian population. World J. Biol. Psychiatry., 2009, 1–4.
2. Bahn, S., Volk, B., Wisden, W., Kainate receptor gene expression in the developing rat brain. J. Neurosci. 14 (1994), 5525–5547.
3. Ben-Ari, Y., Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14 (1985), 375–403.
4. Benes, F.M., Todtenkopf, M.S., Kostoulakos, P., GluR5, 6, 7 subunit immunoreactivity on apical pyramidal cell dendrites in hippocampus of schizophrenics and manic depressives. Hippocampus 11 (2001), 482–491.
5. Beneyto, M., Kristiansen, L.V., Oni-Orisan, A., McCullumsmith, R.E., Meador-Woodruff, J.H., Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 32 (2007), 1888–1902.
6. Bettler, B., Mulle, C., Review: Neurotransmitter receptors. II. AMPA and kainate receptors. Neuropharmacology 34 (1995), 123–139.
7. Blackwood, D.H., Pickard, B.J., Thomson, P.A., Evans, K.L., Porteous, D.J., Muir, W.J., Are some genetic risk factors common to schizophrenia, bipolar disorder and depression? Evidence from DISC1, GRIK4 and NRG1. Neurotox. Res. 11 (2007), 73–83.
8. Bortolotto, Z.A., Clarke, V.R., Delany, C.M., Parry, M.C., Smolders, I., Vignes, M., Ho, K.H., Miu, P., Brinton, B.T., Fantaske, R., Ogden, A., Gates, M., et al. Kainate receptors are involved in synaptic plasticity. Nature 402 (1999), 297–301.
9. Bortolotto, Z.A., Lauri, S., Isaac, J.T., Collingridge, G.L., Kainate receptors and the induction of mossy fibre long-term potentiation. Philos. Trans. R Soc. Lond. B Biol. Sci. 358 (2003), 657–666.
10. Castillo, P.E., Malenka, R.C., Nicoll, R.A., Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388 (1997), 182–186.
11. Clarke, V.R., Ballyk, B.A., Hoo, K.H., Mandelzys, A., Pellizzari, A., Bath, C.P., Thomas, J., Sharpe, E.F., Davies, C.H., Ornstein, P.L., Schoepp, D.D., Kamboj, R.K., et al. A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389 (1997), 599–603.
12. Contractor, A., Sailer, A.W., Darstein, M., Maron, C., Xu, J., Swanson, G.T., Heinemann, S.F., Loss of kainate receptor-mediated heterosynaptic facilitation of mossy-fiber synapses in KA2−/− mice. J. Neurosci. 23 (2003), 422–429.
13. Contractor, A., Swanson, G., Heinemann, S.F., Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29 (2001), 209–216.
14. Contractor, A., Swanson, G.T., Sailer, A., O'Gorman, S., Heinemann, S.F., Identification of the kainate receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. J. Neurosci. 20 (2000), 8269–8278.
15. Cossart, R., Esclapez, M., Hirsch, J.C., Bernard, C., Ben-Ari, Y., GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat. Neurosci. 1 (1998), 470–478.
16. Darstein, M., Petralia, R.S., Swanson, G.T., Wenthold, R.J., Heinemann, S.F., Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J. Neurosci. 23 (2003), 8013–8019.
17. Djurovic, S., Kahler, A.K., Kulle, B., Jonsson, E.G., Agartz, I., Le Hellard, S., Hall, H., Jakobsen, K.D., Hansen, T., Melle, I., Werge, T., Steen, V.M., et al. A possible association between schizophrenia and GRIK3 polymorphisms in a multicenter sample of Scandinavian origin (SCOPE). Schizophr. Res. 107 (2009), 242–248.
18. Egebjerg, J., Bettler, B., Hermans-Borgmeyer, I., Heinemann, S., Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351 (1991), 745–748.
19. Fogarty, D.J., Perez-Cerda, F., Matute, C., KA1-like kainate receptor subunit immunoreactivity in neurons and glia using a novel anti-peptide antibody. Brain Res. Mol. Brain Res. 81 (2000), 164–176.
20. Gaiarsa, J.L., Zagrean, L., Ben-Ari, Y., Neonatal irradiation prevents the formation of hippocampal mossy fibers and the epileptic action of kainate on rat CA3 pyramidal neurons. J. Neurophysiol. 71 (1994), 204–215.
21. Gryder, D.S., Rogawski, M.A., Selective antagonism of GluR5 kainate-receptor-mediated synaptic currents by topiramate in rat basolateral amygdala neurons. J. Neurosci. 23 (2003), 7069–7074.
22. Herb, A., Burnashev, N., Werner, P., Sakmann, B., Wisden, W., Seeburg, P.H., The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8 (1992), 775–785.
23. Hollmann, M., Heinemann, S., Cloned glutamate receptors. Annu. Rev. Neurosci. 17 (1994), 31–108.
24. Hunter, R.G., Bellani, R., Bloss, E., Costa, A., McCarthy, K., McEwen, B.S., Regulation of kainate receptor subunit mRNA by stress and corticosteroids in the rat hippocampus. PLoS ONE, 4, 2009, e4328.
25. Ito, I., Sugiyama, H., Roles of glutamate receptors in long-term potentiation at hippocampal mossy fiber synapses. Neuroreport 2 (1991), 333–336.
26. Jamain, S., Betancur, C., Quach, H., Philippe, A., Fellous, M., Giros, B., Gillberg, C., Leboyer, M., Bourgeron, T., Linkage and association of the glutamate receptor 6 gene with autism. Mol. Psychiatry. 7 (2002), 302–310.
27. Jane, D.E., Lodge, D., Collingridge, G.L., Kainate receptors: Pharmacology, function and therapeutic potential. Neuropharmacology 56 (2009), 90–113.
28. Jiang, H.X., Guan, Q.H., Pei, D.S., Zhang, G.Y., Functional cooperation between KA2 and GluR6 subunits is involved in the ischemic brain injury. J. Neurosci. Res. 85 (2007), 2960–2970.
29. Joels, M., Bosma, A., Hendriksen, H., Diegenbach, P., Kamphuis, W., Corticosteroid actions on the expression of kainate receptor subunit mRNAs in rat hippocampus. Brain Res. Mol. Brain Res. 37 (1996), 15–20.
30. Kaminski, R.M., Banerjee, M., Rogawski, M.A., Topiramate selectively protects against seizures induced by ATPA, a GluR5 kainate receptor agonist. Neuropharmacology 46 (2004), 1097–1104.
31. Kamiya, H., Ozawa, S., Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse. J. Physiol. 523:Pt 3 (2000), 653–665.
32. Khalilov, I., Hirsch, J., Cossart, R., Ben-Ari, Y., Paradoxical anti-epileptic effects of a GluR5 agonist of kainate receptors. J. Neurophysiol. 88 (2002), 523–527.
33. Laje, G., Paddock, S., Manji, H., Rush, A.J., Wilson, A.F., Charney, D., McMahon, F.J., Genetic markers of suicidal ideation emerging during citalopram treatment of major depression. Am. J. Psychiatry. 164 (2007), 1530–1538.
34. Lauri, S.E., Bortolotto, Z.A., Nistico, R., Bleakman, D., Ornstein, P.L., Lodge, D., Isaac, J.T., Collingridge, G.L., A role for Ca2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus. Neuron 39 (2003), 327–341.
35. Loscher, W., Lehmann, H., Behl, B., Seemann, D., Teschendorf, H.J., Hofmann, H.P., Lubisch, W., Hoger, T., Lemaire, H.G., Gross, G., A new pyrrolyl-quinoxalinedione series of non-NMDA glutamate receptor antagonists: Pharmacological characterization and comparison with NBQX and valproate in the kindling model of epilepsy. Eur. J. Neurosci. 11 (1999), 250–262.
36. McEwen, B.S., Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol. Rev. 87 (2007), 873–904.
37. Min, M.Y., Melyan, Z., Kullmann, D.M., Synaptically released glutamate reduces gamma-aminobutyric acid (GABA)ergic inhibition in the hippocampus via kainate receptors. Proc. Natl. Acad. Sci. USA 96 (1999), 9932–9937.
38. Monaghan, D.T., Cotman, C.W., The distribution of [3H]kainic acid binding sites in rat CNS as determined by autoradiography. Brain Res. 252 (1982), 91–100.
39. Mulle, C., Sailer, A., Perez-Otano, I., Dickinson-Anson, H., Castillo, P.E., Bureau, I., Maron, C., Gage, F.H., Mann, J.R., Bettler, B., Heinemann, S.F., Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392 (1998), 601–605.
40. Nadler, J.V., Evenson, D.A., Smith, E.M., Evidence from lesion studies for epileptogenic and non-epileptogenic neurotoxic interactions between kainic acid and excitatory innervation. Brain Res. 205 (1981), 405–410.
41. O'Neill, M.J., Bogaert, L., Hicks, C.A., Bond, A., Ward, M.A., Ebinger, G., Ornstein, P.L., Michotte, Y., Lodge, D., LY377770, a novel iGlu5 kainate receptor antagonist with neuroprotective effects in global and focal cerebral ischaemia. Neuropharmacology 39 (2000), 1575–1588.
42. Paddock, S., Laje, G., Charney, D., Rush, A.J., Wilson, A.F., Sorant, A.J., Lipsky, R., Wisniewski, S.R., Manji, H., McMahon, F.J., Association of GRIK4 with outcome of antidepressant treatment in the STAR*D cohort. Am. J. Psychiatry 164 (2007), 1181–1188.
43. Paternain, A.V., Herrera, M.T., Nieto, M.A., Lerma, J., GluR5 and GluR6 kainate receptor subunits coexist in hippocampal neurons and coassemble to form functional receptors. J. Neurosci. 20 (2000), 196–205.
44. Petralia, R.S., Wang, Y.X., Wenthold, R.J., Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 349 (1994), 85–110.
45. Pickard, B.S., Malloy, M.P., Christoforou, A., Thomson, P.A., Evans, K.L., Morris, S.W., Hampson, M., Porteous, D.J., Blackwood, D.H., Muir, W.J., Cytogenetic and genetic evidence supports a role for the kainate-type glutamate receptor gene, GRIK4, in schizophrenia and bipolar disorder. Mol. Psychiatry 11 (2006), 847–857.
46. Pinheiro, P.S., Perrais, D., Coussen, F., Barhanin, J., Bettler, B., Mann, J.R., Malva, J.O., Heinemann, S.F., Mulle, C., GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. USA 104 (2007), 12181–12186.
47. Represa, A., Tremblay, E., Ben-Ari, Y., Kainate binding sites in the hippocampal mossy fibers: Localization and plasticity. Neuroscience 20 (1987), 739–748.
48. Robinson, J.H., Deadwyler, S.A., Kainic acid produces depolarization of CA3 pyramidal cells in the vitro hippocampal slice. Brain Res. 221 (1981), 117–127.
49. Rodriguez-Moreno, A., Herreras, O., Lerma, J., Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19 (1997), 893–901.
50. Rogawski, M.A., Molecular targets versus models for new antiepileptic drug discovery. Epilepsy Res. 68 (2006), 22–28.
51. Sapolsky, R.M., Stress, glucocorticoids, and damage to the nervous system: The current state of confusion. Stress 1 (1996), 1–19.
52. Schiffer, H.H., Heinemann, S.F., Association of the human kainate receptor GluR7 gene (GRIK3) with recurrent major depressive disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 144B (2007), 20–26.
53. Schiffer, H.H., Heinemann, S.F., Association of the human kainate receptor GluR7 gene (GRIK3) with recurrent major depressive disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 144 (2007), 20–26.
54. Schiffer, H.H., Swanson, G.T., Heinemann, S.F., Rat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 19 (1997), 1141–1146.
55. Schmitz, D., Frerking, M., Nicoll, R.A., Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27 (2000), 327–338.
56. Schmitz, D., Mellor, J., Frerking, M., Nicoll, R.A., Presynaptic kainate receptors at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. USA 98 (2001), 11003–11008.
57. Schmitz, D., Mellor, J., Nicoll, R.A., Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291 (2001), 1972–1976.
58. Shaltiel, G., Maeng, S., Malkesman, O., Pearson, B., Schloesser, R.J., Tragon, T., Rogawski, M., Gasior, M., Luckenbaugh, D., Chen, G., Manji, H.K., Evidence for the involvement of the kainate receptor subunit GluR6 (GRIK2) in mediating behavioral displays related to behavioral symptoms of mania. Mol. Psychiatry 13 (2008), 858–872.
59. Shuang, M., Liu, J., Jia, M.X., Yang, J.Z., Wu, S.P., Gong, X.H., Ling, Y.S., Ruan, Y., Yang, X.L., Zhang, D., Family-based association study between autism and glutamate receptor 6 gene in Chinese Han trios. Am. J. Med. Genet. B Neuropsychiatr. Genet. 131B (2004), 48–50.
60. Siegel, S.J., Janssen, W.G., Tullai, J.W., Rogers, S.W., Moran, T., Heinemann, S.F., Morrison, J.H., Distribution of the excitatory amino acid receptor subunits GluR2(4) in monkey hippocampus and colocalization with subunits GluR5–7 and NMDAR1. J. Neurosci. 15 (1995), 2707–2719.
61. Smolders, I., Bortolotto, Z.A., Clarke, V.R., Warre, R., Khan, G.M., O'Neill, M.J., Ornstein, P.L., Bleakman, D., Ogden, A., Weiss, B., Stables, J.P., Ho, K.H., et al. Antagonists of GLU(K5)-containing kainate receptors prevent pilocarpine-induced limbic seizures. Nat. Neurosci. 5 (2002), 796–804.
62. Sommer, B., Burnashev, N., Verdoorn, T.A., Keinanen, K., Sakmann, B., Seeburg, P.H., A glutamate receptor channel with high affinity for domoate and kainate. EMBO J. 11 (1992), 1651–1656.
63. Strutz-Seebohm, N., Seebohm, G., Shumilina, E., Mack, A.F., Wagner, H.J., Lampert, A., Grahammer, F., Henke, G., Just, L., Skutella, T., Hollmann, M., Lang, F., Glucocorticoid adrenal steroids and glucocorticoid-inducible kinase isoforms in the regulation of GluR6 expression. J. Physiol. 565 (2005), 391–401.
64. Swanson, G.T., Green, T., Sakai, R., Contractor, A., Che, W., Kamiya, H., Heinemann, S.F., Differential activation of individual subunits in heteromeric kainate receptors. Neuron 34 (2002), 589–598.
65. Telfeian, A.E., Federoff, H.J., Leone, P., During, M.J., Williamson, A., Overexpression of GluR6 in rat hippocampus produces seizures and spontaneous nonsynaptic bursting in vitro. Neurobiol. Dis. 7 (2000), 362–374.
66. Vignes, M., Clarke, V.R., Parry, M.J., Bleakman, D., Lodge, D., Ornstein, P.L., Collingridge, G.L., The GluR5 subtype of kainate receptor regulates excitatory synaptic transmission in areas CA1 and CA3 of the rat hippocampus. Neuropharmacology 37 (1998), 1269–1277.
67. Vincent, P., Mulle, C., Kainate receptors in epilepsy and excitotoxicity. Neuroscience 158 (2009), 309–323.
68. Watanabe, M., Fukaya, M., Sakimura, K., Manabe, T., Mishina, M., Inoue, Y., Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur. J. Neurosci. 10 (1998), 478–487.
69. Watanabe, Y., Weiland, N.G., McEwen, B.S., Effects of adrenal steroid manipulations and repeated restraint stress on dynorphin mRNA levels and excitatory amino acid receptor binding in hippocampus. Brain Res. 680 (1995), 217–225.
70. Werner, P., Voigt, M., Keinanen, K., Wisden, W., Seeburg, P.H., Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 351 (1991), 742–744.
71. Woo, T.U., Shrestha, K., Amstrong, C., Minns, M.M., Walsh, J.P., Benes, F.M., Differential alterations of kainate receptor subunits in inhibitory interneurons in the anterior cingulate cortex in schizophrenia and bipolar disorder. Schizophr. Res. 96 (2007), 46–61.