Modification of ionotropic glutamate receptor-mediated processes in the rat hippocampus following repeated, brief seizures

Neuroscience

Volumn 159, Issue 1, 2009, Pages 358-368

  Borbely S ^a   Dobo E ^b   Czege D ^a   Molnar E ^c   Bakos, M ^b   Szucs, B ^b   Vincze, A ^b   Vilagi I ^a   Mihaly A ^b  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b UNIVERSITY OF SZEGED   (Hungary)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

4 aminopyridine; brain slice; Co2+ uptake; electrophysiology; glutamate antagonists; histoblot; subunit composition

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 4 AMINOPYRIDINE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; CALCIUM; COBALT; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; IONOTROPIC RECEPTOR; KA 2 POTEIN; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; BRAIN; BRAIN NERVE CELL; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; CONVULSION; DENSITOMETRY; DENTATE GYRUS; ELECTROPHYSIOLOGY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; INJECTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; RATING SCALE; RECORDING; TONIC CLONIC SEIZURE; WISTAR RAT;

2-AMINO-5-PHOSPHONOVALERATE; 4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; BENZODIAZEPINES; BIOPHYSICS; CALCIUM; COBALT; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; NEURONS; PROTEIN SUBUNITS; RATS; RATS, WISTAR; RECEPTORS, GLUTAMATE; SEIZURES; SYNAPTIC TRANSMISSION;

EID: 60649084927     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.12.027     Document Type: Article

References (60)

1. Ayala G.X., and Tapia R. Late N-methyl-d-aspartate receptor blockade rescues hippocampal neurons from excitotoxic stress and death after 4-aminopyridine-induced epilepsy. Eur J Neurosci 22 (2005) 3067-3076
2. Berg M., Bruhn T., Johansen F.F., and Diemer N.H. Kainic acid-induced seizures and brain damage in the rat: different effects of NMDA and AMPA receptor agonists. Pharmacol Toxicol 73 (1993) 262-268
3. Bleakman D., Ballyk B.A., Schoepp D.D., Palmer A.J., Bath C.P., Sharpe E.F., Woolley M.L., Bufton H.R., Kamboj R.K., Tarnawa I., and Lodge D. Activity of 2,3-benzodiazepines at native rat and recombinant human glutamate receptors in vitro: stereospecificity and selectivity profiles. Neuropharmacology 35 (1996) 1689-1702
4. Brewer L.D., Thibault O., Staton J., Thibault V., Rogers J.T., Garcia-Ramos G., Kraner S., Landfield P.W., and Porter N.M. Increased vulnerability of hippocampal neurons with age in culture: temporal association with increases in NMDA receptor current, NR2A subunit expression and recruitment of L-type calcium channels. Brain Res 1151 (2007) 20-31
5. Cavalheiro E., Naffah-Mazzacoratti M., Mello L., Leite J., Pitkanen A., Schwartzkroin P., and Moshe S. The pilocarpine model of seizures (2005), Academic Press 433-448
6. Cavalheiro E.A. The pilocarpine model of epilepsy. Ital J Neurol Sci 16 (1995) 33-37
7. Darstein M., Petralia R.S., Swanson G.T., Wenthold R.J., and Heinemann S.F. Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J Neurosci 23 (2003) 8013-8019
8. Dóczi J., Banczerowski-Pelyhe I., Barna B., and Vilagi I. Effect of a glutamate receptor antagonist (GYKI 52,466) on 4-aminopyridine-induced seizure activity developed in rat cortical slices. Brain Res Bull 49 (1999) 435-440
9. Fabene P.F., Weiczner R., Marzola P., Nicolato E., Calderan L., Andrioli A., Farkas E., Sule Z., Mihaly 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
10. Fragoso-Veloz J., Massieu L., Alvarado R., and Tapia R. Seizures and wet-dog shakes induced by 4-aminopyridine, and their potentiation by nifedipine. Eur J Pharmacol 178 (1990) 275-284
11. A receptor gene expression in adult rat hippocampus: an in situ hybridization study. J Neurosci 14 (1994) 2697-2707
12. Gashi E., Avallone J., Webster T., and Friedman L.K. Altered excitability and distribution of NMDA receptor subunit proteins in cortical layers of rat pups following multiple perinatal seizures. Brain Res 1145 (2007) 56-65
13. Geiger J.R., Melcher T., Koh D.S., Sakmann B., Seeburg P.H., Jonas P., and Monyer H. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15 (1995) 193-204
14. Gulyás-Kovács A., Doczi J., Tarnawa I., Detari L., Banczerowski-Pelyhe I., and Vilagi I. Comparison of spontaneous and evoked epileptiform activity in three in vitro epilepsy models. Brain Res 945 (2002) 174-180
15. Hassel B., and Dingledine R. Glutamate (2006), Academic Press 267-290
16. Hoffman S.N., Saline P.A., and Prince D.A. chronic neocortical epileptogenesis in vitro. J Neurophysiol 71 (1994) 1762-1773
17. Honavar M., Meldrum B., Graham D., and Lantos P. Epilepsy (2002), Arnold, London 899-941
18. Huettner J.E. Kainate receptors and synaptic transmission. Prog Neurobiol 70 (2003) 387-407
19. Isaac J.T., Ashby M., and McBain C.J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54 (2007) 859-871
20. Johansen T.H., Chaudhary A., and Verdoorn T.A. Interactions among GYKI-52466, cyclothiazide, and aniracetam at recombinant AMPA and kainate receptors. Mol Pharmacol 48 (1995) 946-955
21. Kopniczky Z., Dobo E., Borbely S., Vilagi I., Detari L., Krisztin-Peva B., Bagosi A., Molnar E., and Mihaly 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 (2005) 111-124
22. Kovacs A., Mihaly A., Komaromi A., Gyengesi E., Szente M., Weiczner R., Krisztin-Peva B., Szabo G., and Telegdy G. Seizure, neurotransmitter release, and gene expression are closely related in the striatum of 4-aminopyridine-treated rats. Epilepsy Res 55 (2003) 117-129
23. Kubova H., Vilagi I., Mikulecka A., and Mares P. Non-NMDA receptor antagonist GYKI 52,466 suppresses cortical afterdischarges in immature rats. Eur J Pharmacol 333 (1997) 17-26
24. Liu S., Lau L., Wei J., Zhu D., Zou S., Sun H.S., Fu Y., Liu F., and Lu Y. Expression of Ca(2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43 (2004) 43-55
25. Luhmann H.J., and Prince D.A. Control of NMDA receptor-mediated activity by GABAergic mechanisms in mature and developing rat neocortex. Brain Res Dev Brain Res 54 (1990) 287-290
26. Marinelli S., Gatta F., and Sagratella S. Effects of GYKI 52,466 and some 2,3-benzodiazepine derivatives on hippocampal in vitro basal neuronal excitability and 4-aminopyridine epileptic activity. Eur J Pharmacol 391 (2000) 75-80
27. Meldrum B.S., and Nilsson B. Cerebral blood flow and metabolic rate early and late in prolonged epileptic seizures induced in rats by bicuculline. Brain 99 (1976) 523-542
28. Mello L.E., Cavalheiro E.A., Tan A.M., Kupfer W.R., Pretorius J.K., Babb T.L., and Finch D.M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34 (1993) 985-995
29. Michaelis E.K. Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog Neurobiol 54 (1998) 369-415
30. Mihály A., Bencsik K., and Solymosi T. Naltrexone potentiates 4-aminopyridine seizures in the rat. J Neural Transm Gen Sect 79 (1990) 59-67
31. 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. Acta Physiol Hung 87 (2000) 43-52
32. Mihaly A., Szakacs R., Bohata C., Dobo E., and Krisztin-Peva B. Time-dependent distribution and neuronal localization of c-fos protein in the rat hippocampus following 4-aminopyridine seizures. Epilepsy Res 44 (2001) 97-108
33. Mihaly A., Szente M., Dobo E., and Por I. Early activation of inhibitory neurons in the thalamic reticular nucleus during focal neocortical seizures. Acta Histochem 100 (1998) 383-393
34. Mihály A., Szente M., Dubravcsik Z., Boda B., Kiraly E., Nagy T., and Domonkos A. Parvalbumin- and calbindin-containing neurons express c-fos protein in primary and secondary (mirror) epileptic foci of the rat neocortex. Brain Res 761 (1997) 135-145
35. Nadler J.V., Perry B.W., and Cotman C.W. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 271 (1978) 676-677
36. Nadler J.V., Perry B.W., and Cotman C.W. Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res 182 (1980) 1-9
37. Pellegrini-Giampietro D.E., Gorter J.A., Bennett M.V., and Zukin R.S. The GluR2 (GluR-B) hypothesis: Ca(2+)-permeable AMPA receptors in neurological disorders. Trends Neurosci 20 (1997) 464-470
38. Pena 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
39. Pickard L., Noel J., Henley J.M., Collingridge G.L., and Molnar E. Developmental changes in synaptic AMPA and NMDA receptor distribution and AMPA receptor subunit composition in living hippocampal neurons. J Neurosci 20 (2000) 7922-7931
40. Porter B.E., Cui X.N., and Brooks-Kayal A.R. Status epilepticus differentially alters AMPA and kainate receptor subunit expression in mature and immature dentate granule neurons. Eur J Neurosci 23 (2006) 2857-2863
41. Pruss R.M., Akeson R.L., Racke M.M., and Wilburn J.L. Agonist-activated cobalt uptake identifies divalent cation-permeable kainate receptors on neurons and glial cells. Neuron 7 (1991) 509-518
42. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizurez. Electroencephalogr Clin Neurophysiol 32 (1972) 281-294
43. Schotanus S.M., and Chergui K. NR2A-containing NMDA receptors depress glutamatergic synaptic transmission and evoked-dopamine release in the mouse striatum. J Neurochem 106 (2008) 1758-1765
44. Sheng M., Cummings J., Roldan L.A., Jan Y.N., and Jan L.Y. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368 (1994) 144-147
45. Silva A.V., Regondi M.C., Cipelletti B., Frassoni C., Cavalheiro E.A., and Spreafico R. Neocortical and hippocampal changes after multiple pilocarpine-induced status epilepticus in rats. Epilepsia 46 (2005) 636-642
46. Singh L., Oles R.J., Vass C.A., and Woodruff G.N. A slow intravenous infusion of N-methyl-DL-aspartate as a seizure model in the mouse. J Neurosci Methods 37 (1991) 227-232
47. Sloviter R.S., and Dempster D.W. "Epileptic" brain damage is replicated qualitatively in the rat hippocampus by central injection of glutamate or aspartate but not by GABA or acetylcholine. Brain Res Bull 15 (1985) 39-60
48. Szakács R., Weiczner R., Mihaly A., Krisztin-Peva B., Zador Z., and Zador E. Non-competitive NMDA receptor antagonists moderate seizure-induced c-fos expression in the rat cerebral cortex. Brain Res Bull 59 (2003) 485-493
49. Tarnawa I., Engberg I., Flatman J., Lubec G., and Rosenthal G. GYKI 52,466, an inhibitor of spinal reflexes is a potent quisqualate antagonist. ESCOM (1990), Science Press, Leiden 538-546
50. Tonnes J., Stierli B., Cerletti C., Behrmann J.T., Molnar E., and Streit P. Regional distribution and developmental changes of GluR1-flop protein revealed by monoclonal antibody in rat brain. J Neurochem 73 (1999) 2195-2205
51. Turski W.A., Cavalheiro E.A., Schwarz M., Czuczwar S.J., Kleinrok Z., and Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav Brain Res 9 (1983) 315-335
52. Versteeg D.H., Heemskerk F.M., Spierenburg H.A., de Graan P.N., and Schrama L.H. 4-Aminopyridine differentially affects the spontaneous release of radiolabelled transmitters from rat brain slices in vitro. Brain Res 686 (1995) 233-238
53. Világi I., Takacs J., Gulyas-Kovacs A., Banczerowski-Pelyhe I., and Tarnawa I. Protective effect of the antiepileptic drug candidate talampanel against AMPA-induced striatal neurotoxicity in neonatal rats. Brain Res Bull 59 (2002) 35-40
54. Vizi S., Bagosi A., Krisztin-Peva B., Gulya K., and Mihaly A. Repeated 4-aminopyridine seizures reduce parvalbumin content in the medial mammillary nucleus of the rat brain. Brain Res Mol Br Res 131 (2004) 110-118
55. Weiczner R., Krisztin-Peva B., and Mihaly A. Blockade of AMPA-receptors attenuates 4-aminopyridine seizures, decreases the activation of inhibitory neurons but is ineffective against seizure-related astrocytic swelling. Epilepsy Res 78 (2008) 22-32
56. Wheal H.V., Bernard C., Chad J.E., and Cannon R.C. Pro-epileptic changes in synaptic function can be accompanied by pro-epileptic changes in neuronal excitability. Trends Neurosci 21 (1998) 167-174
57. Wisden W., and Seeburg P.H. A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13 (1993) 3582-3598
58. Xu B., McIntyre D.C., Fahnestock M., and Racine R.J. Strain differences affect the induction of status epilepticus and seizure-induced morphological changes. Eur J Neurosci 20 (2004) 403-418
59. Yamada K.A., and Turetsky D.M. Allosteric interactions between cyclothiazide and AMPA/kainate receptor antagonists. Br J Pharmacol 117 (1996) 1663-1672
60. Yamaguchi S., Donevan S.D., and Rogawski M.A. Anticonvulsant activity of AMPA/kainate antagonists: comparison of GYKI 52,466 and NBOX in maximal electroshock and chemoconvulsant seizure models. Epilepsy Res 15 (1993) 179-184