AMPA receptors as a molecular target in epilepsy therapy

Acta Neurologica Scandinavica

Volumn 127, Issue SUPPL.197, 2013, Pages 9-18

  Rogawski, M A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AMPA receptor; Competitive AMPA receptor antagonist; Epilepsy; Neuronal synchronization; NMDA receptor; Non competitive AMPA receptor antagonist; Seizures

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 2 [5 (4 DIMETHYLSULFAMOYLPHENYL) 6,7,8,9 TETRAHYDRO 8 METHYL 2 OXO 1H PYRROLO[3,2 H]ISOQUINOLIN 3 YLIMINOXY] 4 HYDROXYBUTYRIC ACID; 6 (1 IMIDAZOLYL) 7 NITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR; BECAMPANEL; CP 465022; FANAPANEL; GLUTAMIC ACID; GYKI 47261; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PERAMPANEL; RO 48 8587; RPR 117824; TALAMPANEL; TEZAMPANEL; UNCLASSIFIED DRUG; YM 928; ZONAMPANEL;

BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CENTRAL NERVOUS SYSTEM; DISEASE MODEL; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG HALF LIFE; DRUG TARGETING; EPILEPSY; EPILEPTIC DISCHARGE; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; MOLECULAR DYNAMICS; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PROTEIN LOCALIZATION; RECEPTOR BLOCKING; REVIEW; SYNAPSE;

EID: 84875077324     PISSN: 00016314     EISSN: 16000404     Source Type: Journal    
DOI: 10.1111/ane.12099     Document Type: Review

References (83)

1. Rogawski MA, Löscher W. The neurobiology of antiepileptic drugs. Nat Rev Neurosci 2004;5:553-64.
2. Jefferys JGR, Jiruska P, De Curtis M, Avoli M. Limbic network synchronization and temporal lobe epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, eds. Jasper's basic mechanisms of the epilepsies, 4th edn. Bethesda, MD: National Center for Biotechnology Information (US), 2012. Available from: http://www.ncbi.nlm.nih.gov/books/NBK98158/.
3. Haas HL, Jefferys JG. Low-calcium field burst discharges of CA1 pyramidal neurones in rat hippocampal slices. J Physiol 1984;354:185-201.
4. Taylor CP. How do seizures begin? Clues from hippocampal slices. Trends Neurosci 1988;11:375-7.
5. Jefferys JG, Traub RD. Electrophysiological substrates for focal epilepsies. Prog Brain Res 1998;116:351-8.
6. Miles R, Wong RK. Single neurones can initiate synchronized population discharge in the hippocampus. Nature 1983;306:371-3.
7. Traub RD, Wong RKS. Cellular mechanism of neuronal synchronization in epilepsy. Science 1982;216:745-7.
8. Miles R, Wong RKS. Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol 1987;388:611-29.
9. Miles R, Wong RKS. Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J Physiol 1986;373:397-418.
10. Timofeev I, Bazhenov M, Seigneur J, Sejnowski T. Neuronal synchronization and thalamocortical rhythms in sleep, wake and epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, eds. Jasper's basic mechanisms of the epilepsies, 4th edn. Bethesda, MD: National Center for Biotechnology Information (US), 2012. Available from: http://www.ncbi.nlm.nih.gov/books/NBK98144/.
11. Honoré T, Davies SN, Drejer J et al. Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. Science 1988;241:701-3.
12. McBain CJ, Boden P, Hill RG. The kainate/quisqualate receptor antagonist, CNQX, blocks the fast component of spontaneous epileptiform activity in organotypic cultures of rat hippocampus. Neurosci Lett 1988;93:341-5.
13. Neuman RS, Ben-Ari Y, Cherubini E. Antagonism of spontaneous and evoked bursts by 6-cyano-7-nitroquinoxaline-2, 3-dione (CNQX) in the CA3 region of the in vitro hippocampus. Brain Res 1988;474:201-3.
14. Lee W-L, Hablitz JJ. Involvement of non-NMDA receptors in picrotoxin-induced epileptiform activity in the hippocampus. Neurosci Lett 1989;107:129-34.
15. Traub RD, Miles R, Jefferys JG. Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after-discharges in the guinea-pig hippocampal slice. J Physiol 1993;461:525-47.
16. Hwa GGC, Avoli M. The involvement of excitatory amino acids in neocortical epileptogenesis: NMDA and non-NMDA receptors. Exp Brain Res 1991;86:248-56.
17. Hwa GGC, Avoli M, Oliver A, Villemure JG. Bicuculline-induced epileptogenesis in the human neocortex maintained in vitro. Exp Brain Res 1991;83:329-39.
18. Jones RS, Lambert JD. Synchronous discharges in the rat entorhinal cortex in vitro: site of initiation and the role of excitatory amino acid receptors. Neuroscience 1990;34:657-70.
19. Collingridge GL, Lester RA. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol Rev 1989;41:143-210.
20. Anggono V, Huganir RL. Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 2012;22:461-9.
21. Fleming JJ, England PM. AMPA receptors and synaptic plasticity: a chemist's perspective. Nat Chem Biol 2010;6:89-97.
22. Isaac JT, Ashby MC, McBain CJ. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007;54:859-71.
23. 2+ permeable AMPA receptor induced long-term potentiation requires PI3/MAP kinases but not Ca/CaM-dependent kinase II. PLoS ONE 2009;4:e4339.
24. Citri A, Malenka RC. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 2008;33:18-41.
25. Kapus G, Székely JI, Durand J, Ruiz A, Tarnawa I. AMPA receptor antagonists, GYKI 52466 and NBQX, do not block the induction of long-term potentiation at therapeutically relevant concentrations. Brain Res Bull 2000;52:511-7.
26. Parada J, Czuczwar SJ, Turski WA. NBQX does not affect learning and memory tasks in mice: a comparison with D-CPPene and ifenprodil. Brain Res Cogn Brain Res 1992;1:67-71.
27. Pitsikas N, Rigamonti AE, Cella SG, Muller EE. The non-NMDA receptor antagonist NBQX does not affect rats performance in the object recognition task. Pharmacol Res 2002;45:43-6.
28. Parada-Turska J, Turski WA. Excitatory amino acid antagonists and memory: effect of drugs acting at N-methyl-D-aspartate receptors in learning and memory tasks. Neuropharmacology 1990;29:1111-6.
29. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 2007;30:126-34.
30. Shepherd JD. Memory, plasticity and sleep - a role for calcium permeable AMPA receptors? Front Mol Neurosci 2012;5:49.
31. Jackson AC, Nicoll RA. The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 2011;70:178-99.
32. Menuz K, Stroud RM, Nicoll RA, Hays FA. TARP auxiliary subunits switch AMPA receptor antagonists into partial agonists. Science 2007;318:815-7.
33. Cokić B, Stein V. Stargazin modulates AMPA receptor antagonism. Neuropharmacology 2008;54:1062-70.
34. Kato AS, Gill MB, Yu H, Nisenbaum ES, Bredt DS. TARPs differentially decorate AMPA receptors to specify neuropharmacology. Trends Neurosci 2010;33:241-8.
35. Gryder DS, Castaneda DC, Rogawski MA. Evidence for low GluR2 AMPA receptor subunit expression at synapses in the rat basolateral amygdala. J Neurochem 2005;94:1728-38.
36. Beneyto M, Meador-Woodruff JH. Expression of transcripts encoding AMPA receptor subunits and associated postsynaptic proteins in the macaque brain. J Comp Neurol 2004;468:530-54.
37. Lu W, Shi Y, Jackson AC et al. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 2009;62:254-68.
38. Derkach VA, Oh MC, Guire ES, Soderling TR. Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 2007;8:101-13.
39. Ashby MC, de la Rue SA, Ralph GS, Uney J, Collingridge GL, Henley JM. Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J Neurosci 2004;24:5172-6.
40. Catarzi D, Colotta V, Varano F. Competitive AMPA receptor antagonists. Med Res Rev 2007;27:239-78.
41. Kew JN, Kemp JA. Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology 2005;179:4-29.
42. Lodge D, Danysz W, Parsons CG, eds. Ionotropic glutamate receptors as therapeutic targets. Johnson City, TN: F.P. Graham Publishing Co., 2002.
43. Drejer J, Honoré T. New quinoxalinediones show potent antagonism of quisqualate responses in cultured mouse cortical neurons. Neurosci Lett 1988;87:104-8.
44. Mano I, Lamed Y, Teichberg VI. A Venus flytrap mechanism for activation and desensitization of α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors. J Biol Chem 1996;271:15299-302.
45. Armstrong N, Gouaux E. Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: crystal structures of the GluR2 ligand binding core. Neuron 2000;28:165-81.
46. Sheardown MJ, Nielsen EØ, Hansen AJ, Jacobsen P, Honoré T. 2, 3-Dihydroxy-6-nitro-7-sulfamoyl-benzo(F)quinoxaline: a neuroprotectant for cerebral ischemia. Science 1990;247:571-4.
47. Chapman AG, Smith SE, Meldrum BS. The anticonvulsant effect of the non-NMDA antagonists, NBQX and GYKI 52466, in mice. Epilepsy Res 1991;9:92-6.
48. Taylor CP, Vartanian MG. Probenecid pretreatment enhances anticonvulsant action of NBQX in mice. Eur J Pharmacol 1992;213:151-3.
49. Yamaguchi S, Donevan SD, Rogawski MA. Anticonvulsant activity of AMPA/kainate antagonists: comparison of GYKI 52466 and NBOX in maximal electroshock and chemoconvulsant seizure models. Epilepsy Res 1993;15:179-84.
50. Namba T, Morimoto K, Sato K, Yamada N, Kuroda S. Antiepileptogenic and anticonvulsant effects of NBQX, a selective AMPA receptor antagonist, in the rat kindling model of epilepsy. Brain Res 1994;638:36-44.
51. Takahashi M, Kohara A, Shishikura J et al. YM872: a selective, potent and highly water-soluble α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor antagonist. CNS Drug Rev 2002;8:337-52.
52. Hara H, Yamada N, Kodama M, Matsumoto Y, Wake Y, Kuroda S. Effect of YM872, a selective and highly water-soluble AMPA receptor antagonist, in the rat kindling and rekindling model of epilepsy. Eur J Pharmacol 2006;531:59-65.
53. Shimizu-Sasamata M, Kawasaki-Yatsugi S, Okada M et al. YM90K: pharmacological characterization as a selective and potent α-amino-3-hydroxy-5-methylisoxazole-4-propionate/kainate receptor antagonist. J Pharmacol Exp Ther 1996;276:84-92.
54. Kodama M, Yamada N, Sato K et al. Effects of YM90K, a selective AMPA receptor antagonist, on amygdala-kindling and long-term hippocampal potentiation in the rat. Eur J Pharmacol 1999;374:11-9.
55. Turski L, Huth A, Sheardown M et al. ZK200775: a phosphonate quinoxalinedione AMPA antagonist for neuroprotection in stroke and trauma. Proc Natl Acad Sci USA 1998;95:10960-5.
56. Mattes H, Carcache D, Kalkman HO, Koller M. α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) antagonists: from bench to bedside. J Med Chem 2010;53:5367-82.
57. Mignani S, Bohme GA, Birraux G et al. 9-Carboxymethyl-5H, 10H-imidazo(1, 2-a)indeno(1, 2-e)pyrazin-4-one-2-carbocylic acid (RPR117824): selective anticonvulsive and neuroprotective AMPA antagonist. Bioorg Med Chem 2002;10:1627-37.
58. Krampfl K, Schlesinger F, Cordes AL, Bufler J. Molecular analysis of the interaction of the pyrazine derivatives RPR119990 and RPR117824 with human AMPA-type glutamate receptor channels. Neuropharmacology 2006;50:479-90.
59. Nielsen EØ, Varming T, Mathiesen C et al. SPD 502: a water-soluble and in vivo long-lasting AMPA antagonist with neuroprotective activity. J Pharmacol Exp Ther 1999;289:1492-501.
60. Pitkänen A, Mathiesen C, Rønn LC, Møller A, Nissinen J. Effect of novel AMPA antagonist, NS1209, on status epilepticus. An experimental study in rat. Epilepsy Res 2007;74:45-54.
61. Koller M, Lingenhoehl K, Schmutz M et al. Quinazolinedione sulfonamides: a novel class of competitive AMPA receptor antagonists with oral activity. Bioorg Med Chem Lett 2011;21:3358-61.
62. Orain D, Ofner S, Koller M et al. 6-Amino quinazolinedione sulfonamides as orally active competitive AMPA receptor antagonists. Bioorg Med Chem Lett 2012;22:996-9.
63. Bialer M, Johannessen SI, Kupferberg HJ, Levy RH, Perucca E, Tomson T. Progress report on new antiepileptic drugs: a summary of the Eighth Eilat Conference (EILAT VIII). Epilepsy Res 2007;73:1-52.
64. Ornstein PL, Arnold MB, Augenstein NK, Lodge D, Leander JD, Schoepp DD. (3SR, 4aRS, 6RS, 8aRS)-6-(2-(1H-tetrazol-5-yl)ethyl)decahydroisoquinoline-3-carboxylic acid: a structurally novel, systemically active, competitive AMPA receptor antagonist. J Med Chem 1993;36:2046-8.
65. Schoepp DD, Lodge D, Bleakman D et al. In vitro and in vivo antagonism of AMPA receptor activation by (3S, 4aR, 6R, 8aR)-6-(2-(1(2)H-tetrazole-5-yl) ethyl) decahydroisoquinoline-3-carboxylic acid. Neuropharmacology 1995;34:1159-68.
66. Sólyom S, Tarnawa I. Non-competitive AMPA antagonists of 2, 3-benzodiazepine type. Curr Pharm Des 2002;8:913-39.
67. Donevan SD, Rogawski MA. GYKI 52466, a 2, 3-benzodiazepine, is a highly selective, noncompetitive antagonist of AMPA/kainate receptor responses. Neuron 1993;10:51-9.
68. Ritz M, Wang C, Micale N, Ettari R, Niu L. Mechanism of inhibition of the GluA2 AMPA receptor channel opening: the role of 4-methyl versus 4-carbonyl group on the diazepine ring of 2, 3-benzodiazepine derivatives. ACS Chem Neurosci 2011;2:506-13.
69. Smith SE, Dürmüller N, Meldrum BS. The non-N-methyl-D-aspartate receptor antagonists, GYKI 52466 and NBQX are anticonvulsant in two animal models of reflex epilepsy. Eur J Pharmacol 1991;201:179-83.
70. Dürmüller N, Craggs M, Meldrum BS. The effect of the non-NMDA receptor antagonist GYKI 52466 and NBQX and the competitive NMDA receptor antagonist D-CPPene on the development of amygdala kindling and on amygdala-kindled seizures. Epilepsy Res 1994;17:167-74.
71. Danielsson I, Su K, Kauer L et al. Talampanel and human cortical excitability: EEG and TMS. Epilepsia 2004;45(Suppl. 7):120 (1.314).
72. Balannik V, Menniti FS, Paternain AV, Lerma J, Stern-Bach Y. Molecular mechanism of AMPA receptor noncompetitive antagonism. Neuron 2005;48:279-88.
73. Qneibi MS, Micale N, Grasso S, Niu L. Mechanism of inhibition of GluA2 AMPA receptor channel opening by 2, 3-benzodiazepine derivatives: functional consequences of replacing a 7, 8-methylenedioxy with a 7, 8-ethylenedioxy moiety. Biochemistry 2012;51:1787-95.
74. Ohno K, Tsutsumi R, Matsumoto N et al. Functional characterization of YM928, a novel noncompetitive α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor antagonist. J Pharmacol Exp Ther 2003;306:66-72.
75. Yamashita H, Ohno K, Amada Y et al. Effect of YM928, a novel AMPA receptor antagonist, on seizures in EL mice and kainate-induced seizures in rats. Naunyn Schmiedebergs Arch Pharmacol 2004;370:99-105.
76. Abrahám G, Sólyom S, Csuzdi E et al. New non competitive AMPA antagonists. Bioorg Med Chem 2000;8:2127-43.
77. Menniti FS, Chenard BL, Collins MB et al. Characterization of the binding site for a novel class of noncompetitive α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor antagonists. Mol Pharmacol 2000;58:1310-7.
78. Welch WM, Ewing FE, Huang J et al. Atropisomeric quinazolin-4-one derivatives are potent noncompetitive α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor antagonists. Bioorg Med Chem Lett 2001;11:177-81.
79. French JA, Krauss GL, Biton V et al. Adjunctive perampanel for refractory partial-onset seizures: randomized phase III study 304. Neurology 2012;79:589-96.
80. French JA, Krauss GL, Steinhoff BJ et al. Evaluation of adjunctive perampanel in patients with refractory partial-onset seizures: results of randomized global phase III study 305. Epilepsia 2013;54:117-25.
81. Krauss GL, Serratosa JM, Villanueva V et al. Randomized phase III study 306: adjunctive perampanel for refractory partial-onset seizures. Neurology 2012;78:1408-15.
82. Rogawski MA, Hanada T. Preclinical pharmacology of perampanel, a selective noncompetitive AMPA receptor antagonist. Acta Neurol Scand 2013;127(Suppl. 197):19-24.
83. Rogawski MA, Donevan SD. AMPA receptors in epilepsy and as targets for antiepileptic drugs. In: AV Delgado-Escueta, WA Wilson, RW Olsen, RJ Porter, eds. Jasper's basic mechanisms of the epilepsies. Philadelphia, PA: Lippincott Williams & Wilkins, 1999;947-63.