Kainate Receptors Are the Key to Understanding Synaptic Plasticity, Learning and Memory (Review)

Glutamatergic signaling is one of the main types of excitatory synaptic transmission in the brain. It plays a key role in the normal brain function and the cognitive performance. Glutamatergic signaling failure is associated with brain disorders; therefore this system is considered an essential target of therapeutic interventions. Glutamatergic synaptic transmission is mediated by a set of ionotropic and metabotropic glutamate receptors including the kainate receptors. These receptors (both ionotropic and metabotropic) are involved in the process of synaptic transmission by modulating the excitation/inhibition balance. The modulatory effect of kainate receptors is mediated by the mechanisms that involve the presynaptic and postsynaptic endings, the rhythmic activity of the neural network, the function of the astroglial network, and the neuron-glial interaction. Thus, a dysfunction of kainate receptors can lead to deviations in the balance between excitation and inhibition, disorders of the neuronal networks, and even epileptiform manifestations. The present report reviews the major mechanisms of ionotropic and metabotropic activation of kainate receptors involved in the regulation of synaptic transmission, plasticity, learning and memory.

1. Watkins J.C., Jane D.E. The glutamate story. Br J Pharmacol 2006; 147(Suppl 1): S100–S108, https://doi.org/10.1038/sj.bjp.0706444.
2. Lomeli H., Sprengel R., Laurie D.J., Köhr G., Herb A., Seeburg P.H., Wisden W. The rat delta-1 and delta-2 subunits extend the excitatory amino acid receptor family. FEBS Lett 1993; 315(3): 318–322, https://doi.org/10.1016/0014-5793(93)81186-4.
3. Gouaux E. Structure and function of AMPA receptors. J Physiol 2004; 554(2): 249–253, https://doi.org/10.1113/jphysiol.2003.054320.
4. Dingledine R., Borges K., Bowie D., Traynelis S.F. The glutamate receptor ion channels. Pharmacol Rev 1999; 51(1): 7–61.
5. Collingridge G.L., Olsen R.W., Peters J., Spedding M. A nomenclature for ligand-gated ion channels. Neuropharmacology 2009; 56(1): 2–5, https://doi.org/10.1016/j.neuropharm.2008.06.063.
6. Ferrer-Montiel A.V., Montal M. Pentameric subunit stoichiometry of a neuronal glutamate receptor. Proc Natl Acad Sci USA 1996; 93(7): 2741–2744, https://doi.org/10.1073/pnas.93.7.2741.
7. Atlason P.T., Scholefield C.L., Eaves R.J., Mayo-Martin M.B., Jane D.E., Molnár E. Mapping the ligand binding sites of kainate receptors: molecular determinants of subunit-selective binding of the antagonist [3H]UBP310. Mol Pharmacol 2010; 78(6): 1036–1045, https://doi.org/10.1124/mol.110.067934.
8. Lerma J., Marques J.M. Kainate receptors in health and disease. Neuron 2013; 80(2): 292–311, https://doi.org/10.1016/j.neuron.2013.09.045.
9. Contractor A., Mulle C., Swanson G.T. Kainate receptors coming of age: milestones of two decades of research. Trends Neurosci 2011; 34(3): 154–163, https://doi.org/10.1016/j.tins.2010.12.002.
10. Nadler J.V. Kainic acid: neurophysiological and neurotoxic actions. Life Sci 1979; 24(4): 289–299, https://doi.org/10.1016/0024-3205(79)90325-4.
11. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985; 14(2): 375–403, https://doi.org/10.1016/0306-4522(85)90299-4.
12. Swanson G.T., Sakai R. Ligands for ionotropic glutamate receptors. Prog Mol Subcell Biol 2009; 46: 123–157, https://doi.org/10.1007/978-3-540-87895-7_5.
13. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 1994; 17(1): 31–108, https://doi.org/10.1146/annurev.ne.17.030194.000335.
14. Ben-Ari Y., Cossart R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 2000; 23(11): 580–587, https://doi.org/10.1016/s0166-2236(00)01659-3.
15. Zhang X.M., Zhu J. Kainic acid-induced neurotoxicity: targeting glial responses and glia-derived cytokines. Curr Neuropharmacol 2011; 9(2): 388–398, https://doi.org/10.2174/157015911795596540.
16. Jane D.E., Lodge D., Collingridge G.L. Kainate receptors: pharmacology, function and therapeutic potential. Neuropharmacology 2009; 56(1): 90–113, https://doi.org/10.1016/j.neuropharm.2008.08.023.
17. 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 1991; 351(6329): 745–748, https://doi.org/10.1038/351745a0.
18. 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 1992; 8(4): 775–785, https://doi.org/10.1016/0896-6273(92)90098-x.
19. Ren Z., Riley N.J., Garcia E.P., Sanders J.M., Swanson G.T., Marshall J. Multiple trafficking signals regulate kainate receptor KA2 subunit surface expression. J Neurosci 2003; 23(16): 6608–6616.
20. Rozas J.L., Paternain A.V., Lerma J. Noncanonical signaling by ionotropic kainate receptors. Neuron 2003; 39(3): 543–553, https://doi.org/10.1016/s0896-6273(03)00436-7.
21. Köhler M., Burnashev N., Sakmann B., Seeburg P.H. Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron 1993; 10(3): 491–500, https://doi.org/10.1016/0896-6273(93)90336-p.
22. Wisden W., Seeburg P.H. A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 1993; 13(8): 3582–3598.
23. Bahn S., Volk B., Wisden W. Kainate receptor gene expression in the developing rat brain. J Neurosci 1994; 14(9): 5525–5547.
24. Lauri S.E., Delany C., J Clarke V.R., Bortolotto Z.A., Ornstein P.L., Isaac J.T.R., Collingridge G.L. Synaptic activation of a presynaptic kainate receptor facilitates AMPA receptor-mediated synaptic transmission at hippocampal mossy fibre synapses. Neuropharmacology 2001; 41(8): 907–915, https://doi.org/10.1016/s0028-3908(01)00152-6.
25. Kullmann M. Presynaptic kainate receptors in the hippocampus: slowly emerging from obscurity. Neuron 2001; 32(4): 561–564, https://doi.org/10.1016/s0896-6273(01)00507-4.
26. Castillo P.E., Malenka R.C., Nicoll R.A. Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 1997; 388(6638): 182–186, https://doi.org/10.1038/40645.
27. Vignes M., Collingridge G.L. The synaptic activation of kainate receptors. Nature 1997; 388(6638): 179–182, https://doi.org/10.1038/40639.
28. Rodríguez-Moreno A., Herreras O., Lerma J. Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 1997; 19(4): 893–901, https://doi.org/10.1016/s0896-6273(00)80970-8.
29. 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 2000; 20(22): 8269–8278.
30. Mulle C., Sailer A., Pérez-Otaño 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 1998; 392(6676): 601–605, https://doi.org/10.1038/33408.
31. Simmons R.M., Li D.L., Hoo K.H., Deverill M., Ornstein P.L., Iyengar S. Kainate GluR5 receptor subtype mediates the nociceptive response to formalin in the rat. Neuropharmacology 1998; 37(1): 25–36, https://doi.org/10.1016/s0028-3908(97)00188-3.
32. Alt A., Weiss B., Ornstein P.L., Gleason S.D., Bleakman D., Stratford R.E. Jr., Witkin J.M. Anxiolytic-like effects through a GLUK5 kainate receptor mechanism. Neuropharmacology 2007; 52(7): 1482–1487, https://doi.org/10.1016/j.neuropharm.2007.02.005.
33. Pinheiro P.S., Mulle C. Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 2008; 9(6): 423–436, https://doi.org/10.1038/nrn2379.
34. Contractor A., Swanson G.T. Kainate receptors. In: Gereau R.W., Swanson G.T. (editors). The glutamate receptors. Humana Press; 2008; p. 99–158.
35. Jiang L., Xu J., Nedergaard M., Kang J. A kainate receptor increases the efficacy of GABAergic synapses. Neuron 2001; 30(2): 503–513.
36. Lerma J. Kainate receptor physiology. Curr Opin Pharmacol 2006; 6(1): 89–97, https://doi.org/10.1016/j.coph.2005.08.004.
37. Huettner J.E. Kainate receptors and synaptic transmission. Prog Neurobiol 2003; 70(5): 387–407, https://doi.org/10.1016/s0301-0082(03)00122-9.
38. Campbell S.L., Mathew S.S., Hablitz J.J. Pre- and postsynaptic effects of kainate on layer II/III pyramidal cells in rat neocortex. Neuropharmacology 2007; 53(1): 37–47, https://doi.org/10.1016/j.neuropharm.2007.04.008.
39. Contractor A., Swanson G., Heinemann SF. Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 2001; 29(1): 209–216, https://doi.org/10.1016/s0896-6273(01)00191-x.
40. 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., Ornstein P.L., Lodge D., Bleakman D., Collingridge G.L. Kainate receptors are involved in synaptic plasticity. Nature 1999; 402(6759): 297–301, https://doi.org/10.1038/46290.
41. Lauri S.E., Bortolotto Z.A., Bleakman D., Ornstein P.L., Lodge D., Isaac J.T., Collingridge G.L. A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP. Neuron 2001; 32(4): 697–709, https://doi.org/10.1016/s0896-6273(01)00511-6.
42. Schmitz D., Mellor J., Nicoll R.A. Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 2001; 291(5510): 1972–1976, https://doi.org/10.1126/science.1057105.
43. 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 2003; 39(2): 327–341, https://doi.org/10.1016/s0896-6273(03)00369-6.
44. Scott R., Lalic T., Kullmann D.M., Capogna M., Rusakov D.A. Target-cell specificity of kainate autoreceptor and Ca2+-store dependent short-term plasticity at hippocampal mossy fiber synapses. J Neurosci 2008; 28(49): 13139–13149, https://doi.org/10.1523/jneurosci.2932-08.2008.
45. Voglis G., Tavernarakis N. The role of synaptic ion channels in synaptic plasticity. EMBO Rep 2006; 7(11): 1104–1110, https://doi.org/10.1038/sj.embor.7400830.
46. Mathew S.S., Pozzo-Miller L., Hablitz J.J. Kainate modulates presynaptic GABA release from two vesicle pools. J Neurosci 2008; 28(3): 725–731, https://doi.org/10.1523/jneurosci.3625-07.2008.
47. 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 1999; 96(17) 9932–9937, https://doi.org/10.1073/pnas.96.17.9932.
48. Kerchner G.A., Wang G.D., Qiu C.S., Huettner J.E., Zhuo M. Direct presynaptic regulation of GABA/glycine release by kainate receptors in the dorsal horn: an ionotropic mechanism. Neuron 2001; 32(3): 477–488, https://doi.org/10.1016/s0896-6273(01)00479-2.
49. Frerking M., Petersen C.C., Nicoll R.A. Mechanisms underlying kainate receptor-mediated disinhibition in the hippocampus. Proc Natl Acad Sci USA 1999; 96(22): 12917–12922, https://doi.org/10.1073/pnas.96.22.12917.
50. 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 1998; 1(6): 470–478, https://doi.org/10.1038/2185.
51. Frerking M., Malenka R.C., Nicoll R.A. Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1998; 1(6): 479–486, https://doi.org/10.1038/2194.
52. Semyanov A., Kullmann D.M. Kainate receptor-dependent axonal depolarization and action potential initiation in interneurons. Nat Neurosci 2001; 4(7): 718–723, https://doi.org/10.1038/89506.
53. Kamiya H., Ozawa S. Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse. J Physiol 2000; 523(Pt 3): 653–665, https://doi.org/10.1111/j.1469-7793.2000.t01-1-00653.x.
54. Schmitz D., Frerking M., Nicoll R.A. synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 2000; 27(2): 327–238, https://doi.org/10.1016/s0896-6273(00)00040-4.
55. 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 1998; 37(10–11): 1269–1277, https://doi.org/10.1016/s0028-3908(98)00148-8.
56. Chittajallu R., Vignes M., Dev K.K., Barnes J.M., Collingridge G.L., Henley J.M. Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 1996; 379(6560): 78–81, https://doi.org/10.1038/379078a0.
57. Kamiya H., Ozawa S. Kainate receptor-mediated inhibition of presynaptic Ca2+ influx and EPSP in area CA1 of the rat hippocampus. J Physiol 1998; 509(Pt 3): 833–845, https://doi.org/10.1111/j.1469-7793.1998.833bm.x.
58. Kerchner G.A., Wilding T.J., Li P., Zhuo M., Huettner J.E. Presynaptic kainate receptors regulate spinal sensory transmission. J Neurosci 2001; 21(1): 59–66.
59. Rodríguez-Moreno A., Sihra T.S. Presynaptic kainate receptor-mediated facilitation of glutamate release involves Ca2+-calmodulin and PKA in cerebrocortical synaptosomes. FEBS Lett 2013; 587(6): 788–792, https://doi.org/10.1016/j.febslet.2013.01.071.
60. Fisahn A., Yamada M., Duttaroy A., Gan J.W., Deng C.X., McBain C.J., Wess J. Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 2002; 33(4): 615–624, https://doi.org/10.1016/s0896-6273(02)00587-1.
61. Maingret F., Lauri S.E., Taira T., Isaac J.T. Profound regulation of neonatal CA1 rat hippocampal GABAergic transmission by functionally distinct kainate receptor populations. J Physiol 2005; 567(Pt 1): 131–142, https://doi.org/10.1113/jphysiol.2005.089474.
62. Rodríguez-Moreno A., López-García J.C., Lerma J. Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc Natl Acad Sci USA 2000; 97(3): 1293–1298, https://doi.org/10.1073/pnas.97.3.1293.
63. Schmitz D., Mellor J., Frerking M., Nicoll R.A. Presynaptic kainate receptors at hippocampal mossy fiber synapses. Proc Natl Acad Sci USA 2001; 98(20): 11003–11008, https://doi.org/10.1073/pnas.191351498.
64. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004; 44(1): 5–21, https://doi.org/10.1016/j.neuron.2004.09.012.
65. Park M., Penick E.C., Edwards J.G., Kauer J.A., Ehlers M.D. Recycling endosomes supply AMPA receptors for LTP. Science 2004; 305(5692): 1972–1975, https://doi.org/10.1126/science.1102026.
66. Selak S., Paternain A.V., Aller M.I., Picó E., Rivera R., Lerma J. A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 2009; 63(3): 357–371, https://doi.org/10.1016/j.neuron.2009.07.017.
67. Petrovic M.M., Viana da Silva S., Clement J.P., Vyklicky L., Mulle C., González-González I.M., Henley J.M. Metabotropic action of postsynaptic kainate receptors triggers hippocampal long-term potentiation. Nat Neurosci 2017; 20(4): 529–539, https://doi.org/10.1038/nn.4505.
68. Rodrigues R.J., Lerma J. Metabotropic signaling by kainate receptors. Wiley Interdisciplinary Reviews: Membrane Transport and Signaling 2012; 1(4): 399–410, https://doi.org/10.1002/wmts.35.
69. Nicoll R.A., Mellor J., Frerking M., Schmitz D. Kainate receptors and synaptic plasticity. Nature 2000; 406(6799): 957, https://doi.org/10.1038/35023075.
70. Li P., Wilding T.J., Kim S.J., Calejesan A.A., Huettner J.E., Zhuo M. Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature 1999; 397(6715): 161–164, https://doi.org/10.1038/16469.
71. Kidd F.L., Isaac J.T. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 1999; 400(6744): 569–573, https://doi.org/10.1038/23040.
72. Bureau I., Dieudonne S., Coussen F., Mulle C. Kainate receptor-mediated synaptic currents in cerebellar Golgi cells are not shaped by diffusion of glutamate. Proc Natl Acad Sci USA 2000; 97(12): 6838–6843, https://doi.org/10.1073/pnas.97.12.6838.
73. West P.J., Dalpé-Charron A., Wilcox K.S. Differential contribution of kainate receptors to excitatory postsynaptic currents in superficial layer neurons of the rat medial entorhinal cortex. Neuroscience 2007; 146(3): 1000–1012, https://doi.org/10.1016/j.neuroscience.2007.02.035.
74. González-González I.M., Henley J.M. Postsynaptic kainate receptor recycling and surface expression are regulated by metabotropic autoreceptor signalling. Traffic 2013; 14(7): 810–822, https://doi.org/10.1111/tra.12071.
75. Tashiro A., Dunaevsky A., Blazeski R., Mason C.A., Yuste R. Bidirectional regulation of hippocampal mossy fiber filopodial motility by kainate receptors: a two-step model of synaptogenesis. Neuron 2003; 38(5): 773–784, https://doi.org/10.1016/s0896-6273(03)00299-x.
76. Martin S., Bouschet T., Jenkins E.L., Nishimune A., Henley J.M. Bidirectional regulation of kainate receptor surface expression in hippocampal neurons. J Biol Chem 2008; 283(52): 36435–36440, https://doi.org/10.1074/jbc.m806447200.
77. Suzuki F., Makiura Y., Guilhem D., Sørensen J.C., Onteniente B. Correlated axonal sprouting and dendritic spine formation during kainate-induced neuronal morphogenesis in the dentate gyrus of adult mice. Exp Neurol 1997; 145(1): 203–213, https://doi.org/10.1006/exnr.1997.6469.
78. Prekeris R., Foletti D.L., Scheller R.H. Dynamics of tubulovesicular recycling endosomes in hippocampal neurons. J Neurosci 1999; 19(23): 10324–10337.
79. Cooney J.R., Hurlburt J.L., Selig D.K., Harris K.M., Fiala J.C. Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. J Neurosci 2002; 22(6): 2215–2224.
80. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009; 10(8): 513–525, https://doi.org/10.1038/nrm2728.
81. Hutagalung A.H., Novick P.J. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011; 91(1): 119–149, https://doi.org/10.1152/physrev.00059.2009.
82. Martin S., Henley J.M. Activity-dependent endocytic sorting of kainate receptors to recycling or degradation pathways. EMBO J 2004; 23(24): 4749–4759, https://doi.org/10.1038/sj.emboj.7600483.
83. Miyazaki K., Ross W.N. Ca2+ sparks and puffs are generated and interact in rat hippocampal CA1 pyramidal neuron dendrites. J Neurosci 2013; 33(45): 17777–17788, https://doi.org/10.1523/JNEUROSCI.2735-13.2013.
84. Rose C.R., Konnerth A. Stores not just for storage. Neuron 2001; 31(4): 519–522, https://doi.org/10.1016/s0896-6273(01)00402-0.
85. Melyan Z., Wheal H.V., Lancaster B. Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 2002; 34(1): 107–114, https://doi.org/10.1016/s0896-6273(02)00624-4.
86. Bortolotto Z.A., Nistico R., More J.C., Jane D.E., Collingridge G.L. Kainate receptors and mossy fiber LTP. Neurotoxicology 2005; 26(5): 769–777, https://doi.org/10.1016/j.neuro.2005.02.004.
87. Li H., Rogawski M.A. GluR5 kainate receptor mediated synaptic transmission in rat basolateral amygdala in vitro. Neuropharmacology 1998; 37(10–11): 1279–1286, https://doi.org/10.1016/s0028-3908(98)00109-9.
88. Yeckel M.F., Kapur A., Johnston D. Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat Neurosci 1999; 2(7): 625–633, http://dx.doi.org/10.1038/10180.
89. Ali A.B. Involvement of post-synaptic kainate receptors during synaptic transmission between unitary connections in rat neocortex. Eur J Neurosci 2003; 17(11): 2344–2350, https://doi.org/10.1046/j.1460-9568.2003.02677.x.
90. Eder M., Becker K., Rammes G., Schierloh A., Azad S.C., Zieglgänsberger W., Dodt H.U. Distribution and properties of functional postsynaptic kainate receptors on neocortical layer V pyramidal neurons. J Neurosci 2003; 23(16): 6660–6670.
91. Beed P.S., Salmen B., Schmitz D. GluK2-mediated excitability within the superficial layers of the entorhinal cortex. PLoS One 2009; 4(5): e5576, https://doi.org/10.1371/journal.pone.0005576.
92. Brand-Schieber E., Lowery S.L., Werner P. Select ionotropic glutamate AMPA/kainate receptors are expressed at the astrocyte-vessel interface. Brain Res 2004; 1007(1–2): 178–182, https://doi.org/10.1016/j.brainres.2003.12.051.
93. Gutiérrez-Igarza K., Fogarty D.J., Pérez-Cerdá F, Doñate-Oliver F., Albus K., Matute C. Localization of AMPA-selective glutamate receptor subunits in the adult cat visual cortex. Vis Neurosci 1996; 13(1): 61–72, https://doi.org/10.1017/s0952523800007136.
94. Vargas J.R., Takahashi D.K., Thomson K.E., Wilcox K.S. The expression of kainate receptor subunits in hippocampal astrocytes after experimentally induced status epilepticus. J Neuropathol Exp Neurol 2013; 72(10): 919–932, https://doi.org/10.1097/nen.0b013e3182a4b266.
95. Berger T., Walz W., Schnitzer J., Kettenmann H. GABA- and glutamate-activated currents in glial cells of the mouse corpus callosum slice. J Neurosci Res 1992; 31(1): 21–27, https://doi.org/10.1002/jnr.490310104.
96. García-Barcina J.M., Matute C. Expression of kainate-selective glutamate receptor subunits in glial cells of the adult bovine white matter. Eur J Neurosci 1996; 8(11): 2379–2387, https://doi.org/10.1111/j.1460-9568.1996.tb01201.x.
97. Barres B.A., Koroshetz W.J., Swartz K.J., Chun L.L., Corey D.P. Ion channel expression by white matter glia: the O-2A glial progenitor cell. Neuron 1990; 4(4): 507–524, https://doi.org/10.1016/0896-6273(90)90109-s.
98. Tekkök S.B., Faddis B.T., Goldberg M.P. AMPA/kainate receptors mediate axonal morphological disruption in hypoxic white matter. Neurosci Lett 2005; 382(3): 275–279, https://doi.org/10.1016/j.neulet.2005.03.054.
99. Borges K., Kettenmann H. Blockade of K+ channels induced by AMPA/kainate receptor activation in mouse oligodendrocyte precursor cells is mediated by Na+ entry. J Neurosci Res 1995; 42(4): 579–593, https://doi.org/10.1002/jnr.490420416.
100. Alberdi E., Sánchez-Gómez M.V., Matute C. Calcium and glial cell death. Cell Calcium 2005; 38(3–4): 417–425, https://doi.org/10.1016/j.ceca.2005.06.020.
101. Alberdi E., Sánchez-Gómez M.V., Torre I., Domercq M., Pérez-Samartín A., Pérez-Cerdá F., Matute C. Activation of kainate receptors sensitizes oligodendrocytes to complement attack. J Neurosci 2006; 26(12): 3220–3228, https://doi.org/10.1523/jneurosci.3780-05.2006.
102. Frerking M. When astrocytes signal, kainate receptors respond. Proc Natl Acad Sci USA 2004; 101(9): 2649–2650, https://doi.org/10.1073/pnas.0400474101.
103. Liu Q.S., Xu Q., Arcuino G., Kang J., Nedergaard M. Astrocyte-mediated activation of neuronal kainate receptors. Proc Natl Acad Sci USA 2004; 101(9): 3172–3177, https://doi.org/10.1073/pnas.0306731101.
104. Verkhratsky A., Kirchhoff F. Glutamate-mediated neuronal-glial transmission. J Anat 2007; 210(6): 651–660, https://doi.org/10.1111/j.1469-7580.2007.00734.x.
105. Gallo V., Zhou J.M., McBain C.J., Wright P., Knutson P.L., Armstrong R.C. Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block. J Neurosci 1996; 16(8): 2659–2670.
106. Buhl E.H., Tamás G., Fisahn A. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol 1998; 513(Pt 1): 117–126, https://doi.org/10.1111/j.1469-7793.1998.117by.x.
107. Hormuzdi S.G., Pais I., LeBeau F.E., Towers S.K., Rozov A., Buhl E.H., Whittington M.A., Monyer H. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 2001; 31(3): 487–495, https://doi.org/10.1016/s0896-6273(01)00387-7.
108. Fisahn A., Contractor A., Traub R.D., Buhl E.H., Heinemann S.F., McBain C.J. Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J Neurosci 2004; 24(43): 9658–9668, https://doi.org/10.1523/jneurosci.2973-04.2004.
109. Nadler J.V. Minireview. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 1981; 29(20): 2031–2042, https://doi.org/10.1016/0024-3205(81)90659-7.
110. Stanger H.L., Alford R., Jane D.E., Cunningham M.O. The role of containing kainate receptors in entorhinal cortex gamma frequency oscillations. Neural Plast 2008; 2008: 1–12, https://doi.org/10.1155/2008/401645.
111. Sander T., Hildmann T., Kretz R., Fürst R., Sailer U., Bauer G., Schmitz B., Beck-Mannagetta G., Wienker T.F., Janz D. Allelic association of juvenile absence epilepsy with a GluR5 kainate receptor gene (GRIK1) polymorphism. Am J Med Genet 1997; 4(74): 416–421, https://doi.org/10.1002/(sici)1096-8628(19970725)74:4416::aid-ajmg133.0.co;2-l.
112. Khalilov I., Hirsch J., Cossart R., Ben-Ari Y. Paradoxical anti-epileptic effects of a GluR5 agonist of kainate receptors. J Neurophysiol 2002; 1(88): 523–527.
113. Izzi C., Barbon A., Kretz R., Sander T., Barlati S. Sequencing of the GRIK1 gene in patients with juvenile absence epilepsy does not reveal mutations affecting receptor structure. Am J Med Genet 2002; 3(114): 354–359, https://doi.org/10.1002/ajmg.10254.

Popov A.V., Kushnireva L.A., Doronin M.S., Henley J.M. Kainate Receptors Are the Key to Understanding Synaptic Plasticity, Learning and Memory (Review). Sovremennye tehnologii v medicine 2017; 9(4): 228, https://doi.org/10.17691/stm2017.9.4.28