Blockade of AMPA-receptors attenuates 4-aminopyridine seizures, decreases the activation of inhibitory neurons but is ineffective against seizure-related astrocytic swelling

Epilepsy Research

Volumn 78, Issue 1, 2008, Pages 22-32

  Weiczner, Roland ^a   Krisztin Péva, Beáta ^a   Mihály, András ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

Author keywords

4 aminopyridine; Astrocytic swelling; c fos; GYKI 52466; Parvalbumin; Seizure

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 4 AMINOPYRIDINE; AMPA RECEPTOR; AMPA RECEPTOR ANTAGONIST; PARVALBUMIN; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL SWELLING; CONTROLLED STUDY; DRUG EFFECT; ELECTRON MICROSCOPY; GRAND MAL SEIZURE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; MALE; NONHUMAN; OLFACTORY CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

4-AMINOPYRIDINE; ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; BEHAVIOR, ANIMAL; BENZODIAZEPINES; BRAIN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; GENE EXPRESSION REGULATION; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MOTOR ACTIVITY; NEURAL INHIBITION; PARVALBUMINS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; RECEPTORS, AMPA; SEIZURES;

EID: 37349059328     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2007.10.004     Document Type: Article

References (83)

1. Alexander S.P.H., and Peters J.A. Receptor and ion channel nomenclature supplement. Trends Pharmacol. Sci. 11 (2000) 1-120
2. Amaral D.G. A golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182 (1978) 851-914
3. Arai A.C. GYKI 52466 has positive modulatory effects on AMPA receptors. Brain Res. 892 (2001) 396-400
4. Arias R.L., Tasse J.R.P., and Bowlby M.R. Neuroprotective interaction effects of NMDA and AMPA receptor antagonists in an in vitro model of cerebral ischemia. Brain Res. 816 (1999) 299-308
5. Barna B., Szász A., Világi I., and Szente M. Anticonvulsive effect of AMPA receptor antagonist GYKI 52466 on 4-aminopyridine-induced cortical ictal activity in rat. Brain Res. Bull. 51 3 (2000) 241-248
6. Bender A.S., Schousboe A., Reichelt W., and Norenberg M.D. Ionic mechanisms in glutamate-induced astrocyte swelling: role of K+ influx. J. Neurosci. Res. 52 3 (1998) 307-321
7. Berger S.G., Waser P.G., and Sin-Ren A.C. Distribution of the 4-aminopyridine derivative 3-methoxy-4-aminopyridine in mice. Neuropharmacology 28 2 (1989) 191-194
8. Berretta S., Parthasarathy H.B., and Graybiel A.M. Local release of GABAergic inhibition in the motor cortex induces immediate-early gene expression in indirect pathway neurons of the striatum. J. Neurosci. 17 12 (1997) 4752-4763
9. Block F., Schmitt W., and Schwarz M. Pretreatment but not post-treatment with GYKI 52466 reduces functional deficits and neuronal damage after global ischemia in rats. J. Neurosci. 139 (1996) 167-172
10. Block F., and Schwarz M. The depressant effect of GYKI 52466 on spinal reflex transmission in rats is mediated via non-NMDA and benzodiazepine receptors. Eur. J. Pharmacol. 256 2 (1994) 149-153
11. Bordey A., and Sontheimer H. Ion channel expression by astrocytes in situ: comparison of different CNS regions. Glia 30 1 (2000) 27-38
12. Borowicz K.K., Duda A.M., Kleinrok Z., and Czuczwar S.J. Interaction of GYKI 52466, a selective non-competitive antagonist of AMPA/kainate receptors, with conventional antiepileptic drugs in amygdala-kindled seizures in rats. Pol. J. Pharmacol. 53 2 (2001) 101-108
13. Briellmann R.S., Wellard R.M., and Jackson G.D. Seizure-associated abnormalities in epilepsy: evidence from MR imaging. Epilepsia 46 5 (2005) 760-766
14. Brückner C., and Heinemann U. Effects of standard anticonvulsant drugs on different patterns of epileptiform discharges induced by 4-aminopyridine in combined entorhinal cortex-hippocampal slices. Brain Res. 859 (2000) 15-20
15. + channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J. Neurosci. 19 21 (1999) 9332-9345
16. Clifford D.B., Olney J.W., Benz A.M., Fuller T.A., and Zorumski C.F. Ketamine, phencyclidine, and MK-801 protect against kainic acid-induced seizure-related brain damage. Epilepsia 31 4 (1990) 382-390
17. Conti F., and Weinberg R.J. Shaping excitation at glutamatergic synapses. TINS 22 10 (1999) 451-458
18. DeFelipe J. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, Parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat. 14 (1997) 1-19
19. de Sarro G., Chimirri A., de Sarro A., Gitto R., Grasso S., Giusti P., and Chapman A.G. GYKI 52466 and related 2,3-benzodiazepines as anticonvulsant agents in DBA/2 mice. Eur. J. Pharm. 294 (1995) 411-422
20. de Sarro G., Rizzo M., Sinopoli V.A., Gitto R., de Sarro A., Zappala M., and Chimirri A. Relationship between anticonvulsant activity and plasma level of some 2,3-benzodiazepines in genetically epilepsy-prone rats. Pharm. Biochem. Behav. 61 (1998) 215-220
21. Donevan S.D., and Rogawski M.A. GYKI 52466, a 2,3-benzodiazepine, is a highly selective, noncompetitive antagonist of AMPA/kainate receptor responses. Neuron 10 (1993) 51-59
22. Donevan S.D., and Rogawski M.A. Allosteric regulation of α-amino-3-hydroxy-5-methyl-4-isoxazole-propionate receptors by thiocyanate and cyclothiazide at a common modulatory site distinct from that of 2,3-benzodiazepines. Neuroscience 87 (1998) 615-629
23. Dragunow M., Currie R.W., Faull R.L.M., Robertson H.A., and Jansen K. Immediate-early-genes, kindling and long-term potentiation. Neurosci. Behav. Rev. 24 (1989) 301-313
24. Fabene P.F., Weiczner R., Marzola P., Nicolato E., Calderan L., Andrioli A., Farkas E., Süle Z., Mihály A., and Sbarbati A. Structural and functional MRI following 4-aminopyridine-induced seizures: a comparative imaging and anatomical study. Neurobiol. Dis. 21 (2006) 80-89
25. Fujikawa D.G., Söderfeldt B., and Wasterlain C.G. Neuropathological changes during generalised seizures in newborn monkeys. Epilepsy Res. 12 3 (1992) 243-251
26. Gass P., Herdegen T., Bravos R., and Kiessling M. Induction of immediate early gene encoded proteins in the rat hippocampus after bicuculline-induced seizures: Differential expression of KROX-24, fos and jun proteins. Neuroscience 48 (1992) 315-324
27. Greenberg M.E., and Ziff E.B. Signal transduction in the postsynaptic neuron. Activity-dependent regulation of gene expression. In: Cowan W.M., Südhof T.C., and Stevens C.F. (Eds). Synapses (2001), The Johns Hopkins University Press, Baltimore 357-391
28. Gulyás-Kovács A., Dóczi J., Tarnawa I., Détári L., Banczerowski-Pelyhe I., and Világi I. Comparison of spontaneous and evoked epileptiform activity in three in vitro epilepsy models. Brain Res. 945 (2002) 174-180
29. Han B.C., Koh S.B., Lee E.Y., and Seong Y.H. Regional difference of glutamate-induced swelling in cultured rat brain astrocytes. Life Sci. 76 (2004) 573-583
30. Hantzschel A., and Andreas K. Efficacy of glutamate receptor antagonists in the management of functional disorders in cytotoxic brain oedema induced by hexachlorophene. Pharmacol. Toxicol. 82 2 (1998) 80-88
31. Herdegen T., and Waetzig V. AP-1 proteins in the adult brain: Facts and fiction about effectors of neuroprotection and neurodegeneration. Oncogene 20 (2001) 2424-2437
32. Herdegen T., and Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: Control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Rev. 28 (1998) 370-490
33. Hicks T.P., and Conti F. Amino acids as the source of considerable excitation in cerebral cortex. Can. J. Physiol. Pharmacol. 74 (1996) 341-361
34. Hoffmann G.E., and Lyo D. Anatomical markers of activity in neuroendocrine systems: are we all 'fos-ed out'?. J. Neuroendocr. 14 (2002) 259-268
35. Hong K.S., Cho Y.J., Lee S.K., Jeong S.W., Kim W.K., and Oh E.J. Diffusion changes suggesting predominant vasogenic oedema during partial status epilepticus. Seizure 13 5 (2004) 317-321
36. Hwa G.G.C., and Avoli M. The involvement of excitatory amino acids in neocortical epileptogenesis: NMDA and non-NMDA receptors. Exp. Brain Res. 186 (1991) 248-256
37. Jakus R., Gráf M., Andó R.D., Balogh B., Gacsályi I., Lévay G., Kántor S., and Bagdy G.E. Effect of two noncompetitive AMPA receptor antagonists GYKI 52466 and GYKI 53405 on vigilance, behavior and spike-wave discharges in a genetic rat model of absence epilepsy. Brain Res. 1008 2 (2004) 236-244
38. Kelso A.R.C., and Cock H.R. Advances in epilepsy. Brit. Med. Bull. 72 (2004) 135-148
39. Kimelberg H.K. Water homeostasis in the brain: basic concepts. Neuroscience 129 (2004) 851-860
40. Kleindienst A., Dunbar J.G., Glisson R., Okuno K., and Marmarou A. Effect of dimethyl sulfoxide on blood-brain barrier integrity following middle cerebral artery occlusion in the rat. Acta Neurochir. Suppl. 96 (2006) 258-262
41. Kopniczky Z., Dobó E., Borbély S., Világi I., Détári L., Krisztin-Péva B., Bagosi A., Molnár E., and Mihály A. Lateral entorhinal cortex lesions rearrange afferents, glutamate receptors, increase seizure latency and suppress seizure-induced c-fos expression in the hippocampus of adult rat. J. Neurochem. 95 1 (2005) 111-124
42. Kovács A., Mihály A., Komáromi A., Gyengési E., Szente M., Weiczner R., Krisztin-Péva B., Szabó Gy., and Telegdy Gy. Seizure, neurotransmitter release, and gene expression are closely related in the striatum of 4-aminopyridine-treated rats. Epil. Res. 55 (2003) 117-129
43. Kubová H., Világi I., Mikulecká A., and Mareš P. Non-NMDA receptor antagonist GYKI 52466 suppresses cortical afterdischarges in immature rats. Eur. J. Pharm. 333 (1997) 17-26
44. Labiner D.M., Butler L.S., Cao Z., Hosford D.A., Shin C., and McNamara J.O. Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing. J. Neurosci. 1 (1993) 744-751
45. Lado F.A., Laureta E.C., and Moshé S.L. Seizure-induced hippocampal damage in the mature and immature brain. Epil. Disord. 4 2 (2002) 83-97
46. Lees G.J., and Leong W. In vivo, the direct and seizure-induced neuronal cytotoxicity of kainate and AMPA is modified by the non-competitive antagonist, GYKI 52466. Brain Res. 890 (2001) 66-77
47. Lemeignan M., Millart H., Lamiable D., Molgo J., and Lechat P. Evaluation of 4-aminopyridine and 3,4-diaminopyridine penetrability into cerebrospinal fluid in anesthetized rats. Brain Res. 304 (1984) 166-169
48. Lu C., and Mattson M.P. Dimethyl sulfoxide suppresses NMDA- and AMPA-induced ion currents and calcium influx and protects against excitotoxic death in hippocampal neurons. Exp. Neurol. 170 1 (2001) 180-185
49. A-mediated toxicity of hippocampal neurons in vitro. J. Neurochem. 74 6 (2000) 2445-2453
50. McBain C.J., Freund T.F., and Mody I. Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity. TINS 22 5 (1999) 228-235
51. MacDonald, R.L., McLean, M.J., Skerritt, J.H., 1985. Anticonvulsant drug mechanisms of action. In: Neurobiology of antiepileptic drugs. Feder. Proc. 44 (10), 2634-2639.
52. Mihály A., Bencsik K., and Solymosi T. Naltrexone potentiates 4-aminopyridine seizures in the rat. J. Neural. Transm. (GenSect) 79 (1990) 59-67
53. Mihály A., Shihab-Eldeen A., Owunwanne A., Gopinath S., Ayesha A., and Mathew M. Acute 4-aminopyridine seizures increase the regional cerebral blood flow in the thalamus and neocortex, but not in the entire allocortex of the mouse brain. Act. Phys. Hung. 87 (2000) 43-52
54. Mihály A., Borbély S., Világi I., Détári L., Weiczner R., Zádor Zs., Krisztin-Péva B., Bagosi A., Kopniczky Zs., and Zádor E. Neocortical c-fos mRNA transcription in repeated, brief, acute seizures: is c-fos a coincidence detector?. Int. J. Mol. Med. 15 (2005) 481-486
55. Moga D., Hof P.R., Vissavajjhala P., Moran T.M., and Morrison J.H. Parvalbumin-containing interneurons in rat hippocampus have an AMPA receptor profile suggestive of vulnerability to excitotoxicity. J. Chem. Neuroanat. 23 4 (2002) 249-253
56. Molnár E., Baude A., Richmond S.A., Patel P.B., Somogyi P., and McIlhinney R.A.J. Biochemical and immunocytochemical characterization of antipeptide antibodies to a cloned GluR1 glutamate receptor subunit: cellular and subcellular distribution in the rat forebrain. Neuroscience 53 (1993) 307-326
57. Morgan J.I., and Curran T. Proto-oncogene transcription factors and epilepsy. TIPS 12 (1991) 343-349
58. Olsson T., Broberg M., Pope K.J., Wallace A., Mackenzie L., Blomstrand F., Nilsson M., and Willoughby J.O. Cell swelling, seizures and spreading depression: an impedance study. Neuroscience 140 2 (2006) 505-515
59. Papadopoulos M.C., and Verkman A.S. Aquaporin-4 and brain edema. Pediatr. Nephrol. 22 (2007) 778-784.0
60. Paternain A.V., Morales M., and Lerma J. Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14 (1995) 185-189
61. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1998), Academic Press, San Diego
62. Peña F., and Tapia R. Relationships among seizures, extracellular amino acid changes, and neurodegeneration induced by 4-aminopyridine in rat hippocampus. A microdialysis and electro-encephalographic study. J. Neurochem. 72 (1999) 2006-2014
63. Peña F., and Tapia R. Seizures and neurodegeneration induced by 4-aminopyridine in rat hippocampus in vivo: role of glutamate- and GABA-mediated neurotransmission and of ion channels. Neuroscience 101 (2000) 547-561
64. Perrault P., and Avoli M. Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices. J. Neurophysiol. 65 (1991) 771-779
65. Retchkiman I., Fischer B., Platt D., and Wagner A.P. Seizure induced c-fos mRNA in the rat brain: comparison between young and aging animals. Neurobiol. Aging 17 1 (1996) 41-44
66. Rocha L., Ondarza R., and Kaufman D.L. Antisense oligonucleotides to c-fos reduce postictal seizure susceptibility following fully kindled seizures in rats. Neurosci. Lett. 268 (1999) 143-146
67. Santos N.C., Figueira-Coelho J., Martins-Silva J., and Saldanha C. Multidisciplinary utilization of dimethyl sulfoxide: pharmacological, cellular, and molecular aspects. Biochem. Pharmacol. 65 7 (2003) 1035-1041
68. Schmoll H., Badan I., Fischer B., and Wagner A.P. Dynamics of gene expression for immediate early- and late genes after seizure activity in aged rats. Arch. Ger. Ger. 32 (2001) 199-218
69. Schwaller B., Tetko I.V., Tandon P., Silveira D.C., Vreugdenhil M., Henzi T., Potier M.C., Celio M.R., and Villa A.E.P. Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures. Mol. Cell. Neurosci. 25 (2004) 650-663
70. Sloper J.J., and Powell T.P.S. An experimental electron microscope study of afferent connections to the primate motor and somatic sensory cortices. Phil. Trans. R. Soc. Lond. B 285 (1978) 199-226
71. Staiger J.F., Zilles K., and Freund T. Distribution of GABAergic elements postsynaptic to ventroposteromedial thalamic projections in layer IV of rat barrel cortex. Eur. J. Neurosci. 8 (1996) 2273-2285
72. Syková E. Glia and volume transmission during physiological and pathological states. J. Neur. Transm. 112 1 (2005) 137-147
73. Szabados T., Gigler G., Gacsályi I., Gyertyán I., and Lévay Gy. Comparison of anticonvulsive and acute neuroprotective activity of three 2,3-benzodiazepine compounds, GYKI 52466, GYKI 53405, GYKI 53655. Brain Res. Bull. 55 3 (2001) 387-391
74. Szakács R., Weiczner R., Mihály A., Krisztin-Péva B., Zádor Zs., and Zádor E. Non-competitive NMDA receptor antagonists moderate seizure-induced c-fos expression in the rat cerebral cortex. Brain Res. Bull. 59 (2003) 485-493
75. Székely J.I., Kedves R., Máté I., Török K., and Tarnawa I. Apparent antinociceptive and anti-inflammatory effects of GYKI 52466. Eur. J. Pharm. 336 (1997) 143-154
76. Tarnawa I., Farkas S., Berzsenyi P., Pataki A., and Andrási F. Electrophysiological studies with a 2,3-benzodiazepine muscle relaxant: GYKI 52466. Eur. J. Pharmacol. 167 2 (1989) 193-199
77. Tarnawa I., Molnár P., Gaál L., and Andrási F. Inhibition of hippocampal field potentials by GYKI 52466 in vitro and in vivo. Acta Physiol. Hung. 79 2 (1992) 163-169
78. Tian G.F., Azmi H., Takano T., Xu Q., Peng W., Lin J., Oberheim N., Lou N., Wang X., Zielke H.R., Kang J., and Nedergaard M. An astrocytic basis of epilepsy. Nat. Med. 11 9 (2005) 973-981
79. Trout J.J., Lu C.Y., Goldstone A.D., and Sahgal S. Polyamines and NMDA receptors modulate pericapillary astrocyte swelling following cerebral cryo-injury in the rat. J. Neurocytol. 24 5 (1995) 341-346
80. Tsvyetlynska N.A., Hill R.H., and Grillner S. Role of AMPA receptor desensitization and the side effects of a DMSO vehicle on reticulospinal EPSPs and locomotor activity. J. Neurophysiol. 94 6 (2005) 3951-3960
81. van Gelder N.M., Siatitsas I., Menini C., and Gloor P. Feline generalized penicillin epilepsy: changes of glutamic acid and taurine parallel the progressive increase in excitability of the cortex. Epilepsia 24 2 (1983) 200-213
82. Versteeg D.H.G., Heemskerk F.M.J., Spieremburg H.A., Degraan P.N.E., and Schrama L.H. 4-Aminopyridine differentially affects the spontaneous release of radiolabelled transmitters from rat hippocampal slices. Brain Res. 686 (1995) 233-238
83. Yang L., and Benardo L.S. Laminar properties of 4-aminopyridine-induced synchronous network activities in rat neocortex. Neuroscience 111 2 (2002) 303-313