Down-regulation of BK channel expression in the pilocarpine model of temporal lobe epilepsy

Brain Research

Volumn 1200, Issue , 2008, Pages 116-131

  Pacheco Otalora, Luis F ^a   Hernandez, Eder F ^a   Arshadmansab, Massoud F ^a   Francisco, Sebastian ^a   Willis, Michael ^c   Ermolinsky, Boris ^a   Zarei, Masoud ^a,b   Knaus, Hans Guenther ^c   Garrido Sanabria, Emilio R ^a,b  

^a UNIVERSITY OF TEXAS AT BROWNSVILLE   (United States)

^b The Center for Biomedical Studies   (United States)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Epilepsy; Granule cell; Mossy fiber; Pilocarpine; Presynaptic

Indexed keywords

GLUTAMIC ACID; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; PILOCARPINE;

ALPHA CHAIN; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CHANNEL GATING; CHANNELOPATHY; CHRONIC DISEASE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CORRELATION ANALYSIS; DOWN REGULATION; FUNCTIONAL ASSESSMENT; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOSSY FIBER; NERVE CELL EXCITABILITY; NERVE ENDING; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; RECURRENT DISEASE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TEMPORAL LOBE EPILEPSY; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

ANIMALS; CELL MEMBRANE; CEREBRAL CORTEX; CHRONIC DISEASE; CONVULSANTS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; EPILEPSY, TEMPORAL LOBE; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC PREDISPOSITION TO DISEASE; HIPPOCAMPUS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MEMBRANE POTENTIALS; MOSSY FIBERS, HIPPOCAMPAL; MUSCARINIC AGONISTS; NEURONS; PILOCARPINE; POTASSIUM; RATS; RNA, MESSENGER; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

RATTUS;

EID: 40849084918     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.01.017     Document Type: Article

References (95)

1. Arabadzisz D., Antal K., Parpan F., Emri Z., and Fritschy J.M. Epileptogenesis and chronic seizures in a mouse model of temporal lobe epilepsy are associated with distinct EEG patterns and selective neurochemical alterations in the contralateral hippocampus. Exp. Neurol. 194 (2005) 76-90
2. Aronica E., and Gorter J.A. Gene expression profile in temporal lobe epilepsy. Neuroscientist 13 (2007) 100-108
3. Behrens R., Nolting A., Reimann F., Schwarz M., Waldschutz R., and Pongs O. hKCNMB3 and hKCNMB4, cloning and characterization of two members of the large-conductance calcium-activated potassium channel beta subunit family. FEBS Lett. 474 (2000) 99-106
4. Bernard C., Anderson A., Becker A., Poolos N.P., Beck H., and Johnston D. Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305 (2004) 532-535
5. Bernasconi N., Natsume J., and Bernasconi A. Progression in temporal lobe epilepsy: differential atrophy in mesial temporal structures. Neurology 65 (2005) 223-228
6. Borges K., Gearing M., McDermott D.L., Smith A.B., Almonte A.G., Wainer B.H., and Dingledine R. Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp. Neurol. 182 (2003) 21-34
7. Brenner R., Jegla T.J., Wickenden A., Liu Y., and Aldrich R.W. Cloning and functional characterization of novel large conductance calcium-activated potassium channel beta subunits, hKCNMB3 and hKCNMB4. J. Biol. Chem. 275 (2000) 6453-6461
8. Brenner R., Chen Q.H., Vilaythong A., Toney G.M., Noebels J.L., and Aldrich R.W. BK channel beta4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures. Nat. Neurosci. 8 (2005) 1752-1759
9. Cavalheiro E.A., Leite J.P., Bortolotto Z.A., Turski W.A., Ikonomidou C., and Turski L. Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia 32 (1991) 778-782
10. Cavalheiro E.A. The pilocarpine model of epilepsy. Ital. J. Neurol. Sci. 16 (1995) 33-37
11. Cavazos J.E., and Cross D.J. The role of synaptic reorganization in mesial temporal lobe epilepsy. Epilepsy Behav. 8 (2006) 483-493
12. Celesia G.G. Disorders of membrane channels or channelopathies. Clin. Neurophysiol. 112 (2001) 2-18
13. Chen L., Tian L., MacDonald S.H., McClafferty H., Hammond M.S., Huibant J.M., Ruth P., Knaus H.G., and Shipston M.J. Functionally diverse complement of large conductance calcium- and voltage-activated potassium channel (BK) alpha-subunits generated from a single site of splicing. J. Biol. Chem. 280 (2005) 33599-33609
14. Cheney J.A., Weisser J.D., Bareyre F.M., Laurer H.L., Saatman K.E., Raghupathi R., Gribkoff V., Starrett Jr. J.E., and McIntosh T.K. The maxi-K channel opener BMS-204352 attenuates regional cerebral edema and neurologic motor impairment after experimental brain injury. J. Cereb. Blood Flow Metab. 21 (2001) 396-403
15. Cooper E.C., Aldape K.D., Abosch A., Barbaro N.M., Berger M.S., Peacock W.S., Jan Y.N., and Jan L.Y. Colocalization and coassembly of two human brain M-type potassium channel subunits that are mutated in epilepsy. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4914-4919
16. Crino P.B., and Becker A.J. Gene profiling in temporal lobe epilepsy tissue and dysplastic lesions. Epilepsia 47 (2006) 1608-1616
17. Danzer S.C., and McNamara J.O. Localization of brain-derived neurotrophic factor to distinct terminals of mossy fiber axons implies regulation of both excitation and feedforward inhibition of CA3 pyramidal cells. J. Neurosci. 24 (2004) 11346-11355
18. Debanne D., Thompson S.M., and Gahwiler B.H. A brief period of epileptiform activity strengthens excitatory synapses in the rat hippocampus in vitro. Epilepsia 47 (2006) 247-256
19. Delorenzo R.J., Sun D.A., and Deshpande L.S. Cellular mechanisms underlying acquired epilepsy: the calcium hypothesis of the induction and maintainance of epilepsy. Pharmacol. Ther. 105 (2005) 229-266
20. Du W., Bautista J.F., Yang H., Diez-Sampedro A., You S.A., Wang L., Kotagal P., Luders H.O., Shi J., Cui J., Richerson G.B., and Wang Q.K. Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nat. Genet. 37 (2005) 733-738
21. Dyhrfjeld-Johnsen J., and Soltesz I. Dendritic h channelopathy in epileptogenesis. Neuron 44 (2004) 402-403
22. Epsztein J., Represa A., Jorquera I., Ben-Ari Y., and Crepel V. Recurrent mossy fibers establish aberrant kainate receptor-operated synapses on granule cells from epileptic rats. J. Neurosci. 25 (2005) 8229-8239
23. Feng L., Molnar P., and Nadler J.V. Short-term frequency-dependent plasticity at recurrent mossy fiber synapses of the epileptic brain. J. Neurosci. 23 (2003) 5381-5390
24. Gabriel S., Njunting M., Pomper J.K., Merschhemke M., Sanabria E.R., Eilers A., Kivi A., Zeller M., Meencke H.J., Cavalheiro E.A., Heinemann U., and Lehmann T.N. Stimulus and potassium-induced epileptiform activity in the human dentate gyrus from patients with and without hippocampal sclerosis. J. Neurosci. 24 (2004) 10416-10430
25. Ghatta S., Nimmagadda D., Xu X., and O'Rourke S.T. Large-conductance, calcium-activated potassium channels: structural and functional implications. Pharmacol. Ther. 110 (2006) 103-116
26. Gonzales R.B., DeLeon Galvan C.J., Rangel Y.M., and Claiborne B.J. Distribution of thorny excrescences on CA3 pyramidal neurons in the rat hippocampus. J. Comp. Neurol. 430 (2001) 357-368
27. Gorter J.A., van Vliet E.A., Aronica E., Breit T., Rauwerda H., Lopes da Silva F.H., and Wadman W.J. Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy. J. Neurosci. 26 (2006) 11083-11110
28. Gribkoff V.K., Starrett Jr. J.E., and Dworetzky S.I. Maxi-K potassium channels: form, function, and modulation of a class of endogenous regulators of intracellular calcium. Neuroscientist 7 (2001) 166-177
29. Gribkoff V.K., Starrett Jr. J.E., Dworetzky S.I., Hewawasam P., Boissard C.G., Cook D.A., Frantz S.W., Heman K., Hibbard J.R., Huston K., Johnson G., Krishnan B.S., Kinney G.G., Lombardo L.A., Meanwell N.A., Molinoff P.B., Myers R.A., Moon S.L., Ortiz A., Pajor L., Pieschl R.L., Post-Munson D.J., Signor L.J., Srinivas N., Taber M.T., Thalody G., Trojnacki J.T., Wiener H., Yeleswaram K., and Yeola S.W. Targeting acute ischemic stroke with a calcium-sensitive opener of maxi-K potassium channels. Nat. Med. 7 (2001) 471-477
30. Gutierrez R., and Heinemann U. Co-existence of GABA and Glu in the hippocampal granule cells: implications for epilepsy. Curr. Top. Med. Chem. 6 (2006) 975-978
31. Ha T.S., Heo M.S., and Park C.S. Functional effects of auxiliary beta4-subunit on rat large-conductance Ca(2+)-activated K(+) channel. Biophys. J. 86 (2004) 2871-2882
32. Heinemann U., Beck H., Dreier J.P., Ficker E., Stabel J., and Zhang C.L. The dentate gyrus as a regulated gate for the propagation of epileptiform activity. Epilepsy Res., Suppl. 7 (1992) 273-280
33. Henze D.A., Wittner L., and Buzsaki G. Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat. Neurosci. 5 (2002) 790-795
34. Hewawasam P., Ding M., Chen N., King D., Knipe J., Pajor L., Ortiz A., Gribkoff V.K., and Starrett J. Synthesis of water-soluble prodrugs of BMS-191011: a maxi-K channel opener targeted for post-stroke neuroprotection. Bioorg. Med. Chem. Lett. 13 (2003) 1695-1698
35. Hirose S. A new paradigm of channelopathy in epilepsy syndromes: intracellular trafficking abnormality of channel molecules. Epilepsy Res. 70 Suppl. 1 (2006) S206-S217
36. Holmes G.L., Sarkisian M., Ben-Ari Y., and Chevassus-Au-Louis N. Mossy fiber sprouting after recurrent seizures during early development in rats. J. Comp. Neurol. 404 (1999) 537-553
37. Hotson J.R., and Prince D.A. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J. Neurophysiol. 43 (1980) 409-419
38. Hu H., Shao L.R., Chavoshy S., Gu N., Trieb M., Behrens R., Laake P., Pongs O., Knaus H.G., Ottersen O.P., and Storm J.F. Presynaptic Ca2+-activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J. Neurosci. 21 (2001) 9585-9597
39. Hu S., Labuda M.Z., Pandolfo M., Goss G.G., McDermid H.E., and Ali D.W. Variants of the KCNMB3 regulatory subunit of maxi BK channels affect channel inactivation. Physiol. Genomics 15 (2003) 191-198
40. Jamali S., Bartolomei F., Robaglia-Schlupp A., Massacrier A., Peragut J.C., Regis J., Dufour H., Ravid R., Roll P., Pereira S., Royer B., Roeckel-Trevisiol N., Fontaine M., Guye M., Boucraut J., Chauvel P., Cau P., and Szepetowski P. Large-scale expression study of human mesial temporal lobe epilepsy: evidence for dysregulation of the neurotransmission and complement systems in the entorhinal cortex. Brain 129 (2006) 625-641
41. Jin W., Sugaya A., Tsuda T., Ohguchi H., and Sugaya E. Relationship between large conductance calcium-activated potassium channel and bursting activity. Brain Res. 860 (2000) 21-28
42. Jung S., Jones T.D., Lugo Jr. J.N., Sheerin A.H., Miller J.W., D'Ambrosio R., Anderson A.E., and Poolos N.P. Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy. J. Neurosci. 27 (2007) 13012-13021
43. Kaczorowski G.J., Knaus H.G., Leonard R.J., McManus O.B., and Garcia M.L. High-conductance calcium-activated potassium channels; structure, pharmacology, and function. J. Bioenerg. Biomembr. 28 (1996) 255-267
44. Kaneko T., and Fujiyama F. Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci. Res. 42 (2002) 243-250
45. Kaneko T., Fujiyama F., and Hioki H. Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J. Comp. Neurol. 444 (2002) 39-62
46. Knaus H.G., Schwarzer C., Koch R.O., Eberhart A., Kaczorowski G.J., Glossmann H., Wunder F., Pongs O., Garcia M.L., and Sperk G. Distribution of high-conductance Ca(2+)-activated K+ channels in rat brain: targeting to axons and nerve terminals. J. Neurosci. 16 (1996) 955-963
47. Kutlu G., Bilir E., Erdem A., Gomceli Y.B., Leventoglu A., Kurt G.S., Karatas A., and Serdaroglu A. Temporal lobe ictal behavioral patterns in hippocampal sclerosis and other structural abnormalities. Epilepsy Behav. 6 (2005) 353-359
48. Lawson K. Is there a role for potassium channel openers in neuronal ion channel disorders?. Expert Opin. Investig. Drugs 9 (2000) 2269-2280
49. Leite J.P., Garcia-Cairasco N., and Cavalheiro E.A. New insights from the use of pilocarpine and kainate models. Epilepsy Res. 50 (2002) 93-103
50. Lemos T., and Cavalheiro E.A. Suppression of pilocarpine-induced status epilepticus and the late development of epilepsy in rats. Exp. Brain Res. 102 (1995) 423-428
51. Lerche H., Jurkat-Rott K., and Lehmann-Horn F. Ion channels and epilepsy. Am. J. Med. Genet. 106 (2001) 146-159
52. Liu Z., Nagao T., Desjardins G.C., Gloor P., and Avoli M. Quantitative evaluation of neuronal loss in the dorsal hippocampus in rats with long-term pilocarpine seizures. Epilepsy Res. 17 (1994) 237-247
53. Liu Z., Yang Y., Silveira D.C., Sarkisian M.R., Tandon P., Huang L.T., Stafstrom C.E., and Holmes G.L. Consequences of recurrent seizures during early brain development. Neuroscience 92 (1999) 1443-1454
54. Lorenz S., Heils A., Kasper J.M., and Sander T. Allelic association of a truncation mutation of the KCNMB3 gene with idiopathic generalized epilepsy. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 144B (2006) 10-13
55. Lu R., Alioua A., Kumar Y., Eghbali M., Stefani E., and Toro L. MaxiK channel partners: physiological impact. J. Physiol. 570 (2006) 65-72
56. Lukasiuk K., Dabrowski M., Adach A., and Pitkanen A. Epileptogenesis-related genes revisited. Prog. Brain Res. 158 (2006) 223-241
57. MacDonald S.H., Ruth P., Knaus H.G., and Shipston M.J. Increased large conductance calcium-activated potassium (BK) channel expression accompanied by STREX variant downregulation in the developing mouse CNS. BMC Dev. Biol. 6 (2006) 37
58. Majores M., Eils J., Wiestler O.D., and Becker A.J. Molecular profiling of temporal lobe epilepsy: comparison of data from human tissue samples and animal models. Epilepsy Res. 60 (2004) 173-178
59. Martin E.D., Araque A., and Buno W. Synaptic regulation of the slow Ca2+-activated K+ current in hippocampal CA1 pyramidal neurons: implication in epileptogenesis. J. Neurophysiol. 86 (2001) 2878-2886
60. Masukawa L.M., O'Connor W.M., Lynott J., Burdette L.J., Uruno K., McGonigle P., and O'Connor M.J. Longitudinal variation in cell density and mossy fiber reorganization in the dentate gyrus from temporal lobe epileptic patients. Brain Res. 678 (1995) 65-75
61. 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
62. Mello L.E., Kohman C.M., Tan A.M., Cavalheiro E.A., and Finch D.M. Lack of Fos-like immunoreactivity after spontaneous seizures or reinduction of status epilepticus by pilocarpine in rats. Neurosci. Lett. 208 (1996) 133-137
63. Misonou H., Menegola M., Buchwalder L., Park E.W., Meredith A., Rhodes K.J., Aldrich R.W., and Trimmer J.S. Immunolocalization of the Ca2+-activated K+ channel Slo1 in axons and nerve terminals of mammalian brain and cultured neurons. J. Comp. Neurol. 496 (2006) 289-302
64. Muller Y.L., Reitstetter R., and Yool A.J. Regulation of Ca2+-dependent K+ channel expression in rat cerebellum during postnatal development. J. Neurosci. 18 (1998) 16-25
65. Nadler J.V. The recurrent mossy fiber pathway of the epileptic brain. Neurochem. Res. 28 (2003) 1649-1658
66. Naffah-Mazzacoratti M.G., Funke M.G., Sanabria E.R., and Cavalheiro E.A. Growth-associated phosphoprotein expression is increased in the supragranular regions of the dentate gyrus following pilocarpine-induced seizures in rats. Neuroscience 91 (1999) 485-492
67. Noebels J.L. Sodium channel gene expression and epilepsy. Novartis Found. Symp. 241 (2002) 109-120 (discussion 120-3, 226-32)
68. O'Malley D., Shanley L.J., and Harvey J. Insulin inhibits rat hippocampal neurones via activation of ATP-sensitive K+ and large conductance Ca2+-activated K+ channels. Neuropharmacology 44 (2003) 855-863
69. Oscarson M., Zanger U.M., Rifki O.F., Klein K., Eichelbaum M., and Meyer U.A. Transcriptional profiling of genes induced in the livers of patients treated with carbamazepine. Clin. Pharmacol. Ther. 80 (2006) 440-456
70. Pacheco Otalora L.F., Couoh J., Shigamoto R., Zarei M.M., and Garrido Sanabria E.R. Abnormal mGluR2/3 expression in the perforant path termination zones and mossy fibers of chronically epileptic rats. Brain Res. 1098 (2006) 170-185
71. Pal S., Sun D., Limbrick D., Rafiq A., and DeLorenzo R.J. Epileptogenesis induces long-term alterations in intracellular calcium release and sequestration mechanisms in the hippocampal neuronal culture model of epilepsy. Cell Calcium 30 (2001) 285-296
72. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (2004), Elsevier, New York Vol.
73. Pisani A., Bonsi P., Martella G., De Persis C., Costa C., Pisani F., Bernardi G., and Calabresi P. Intracellular calcium increase in epileptiform activity: modulation by levetiracetam and lamotrigine. Epilepsia 45 (2004) 719-728
74. Poolos N.P. The h-channel: a potential channelopathy in epilepsy?. Epilepsy Behav. 7 (2005) 51-56
75. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32 (1972) 281-294
76. Raza M., Pal S., Rafiq A., and DeLorenzo R.J. Long-term alteration of calcium homeostatic mechanisms in the pilocarpine model of temporal lobe epilepsy. Brain Res. 903 (2001) 1-12
77. Remy S., Urban B.W., Elger C.E., and Beck H. Anticonvulsant pharmacology of voltage-gated Na+ channels in hippocampal neurons of control and chronically epileptic rats. Eur. J. Neurosci. 17 (2003) 2648-2658
78. Richichi C., Brewster A.L., Bender R.A., Simeone T.A., Zha Q., Yin H.Z., Weiss J.H., and Baram T.Z. Mechanisms of seizure-induced 'transcriptional channelopathy' of hyperpolarization-activated cyclic nucleotide gated (HCN) channels. Neurobiol. Dis. 29 2 (2008) 297-305
79. Robitaille R., Garcia M.L., Kaczorowski G.J., and Charlton M.P. Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron 11 (1993) 645-655
80. Sailer C.A., Kaufmann W.A., Kogler M., Chen L., Sausbier U., Ottersen O.P., Ruth P., Shipston M.J., and Knaus H.G. Immunolocalization of BK channels in hippocampal pyramidal neurons. Eur. J. Neurosci. 24 (2006) 442-454
81. Salkoff L., Butler A., Ferreira G., Santi C., and Wei A. High-conductance potassium channels of the SLO family. Nat. Rev. Neurosci. 7 (2006) 921-931
82. Sausbier M., Hu H., Arntz C., Feil S., Kamm S., Adelsberger H., Sausbier U., Sailer C.A., Feil R., Hofmann F., Korth M., Shipston M.J., Knaus H.G., Wolfer D.P., Pedroarena C.M., Storm J.F., and Ruth P. Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-activated K+ channel deficiency. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 9474-9478
83. Selke K., Muller A., Kukley M., Schramm J., and Dietrich D. Firing pattern and calbindin-D28k content of human epileptic granule cells. Brain Res. 1120 (2006) 191-201
84. Shanley L.J., O'Malley D., Irving A.J., Ashford M.L., and Harvey J. Leptin inhibits epileptiform-like activity in rat hippocampal neurones via PI 3-kinase-driven activation of BK channels. J. Physiol. 545 (2002) 933-944
85. Shao L.R., Halvorsrud R., Borg-Graham L., and Storm J.F. The role of BK-type Ca2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J. Physiol. 521 Pt 1 (1999) 135-146
86. Shigemoto R., Kinoshita A., Wada E., Nomura S., Ohishi H., Takada M., Flor P.J., Neki A., Abe T., Nakanishi S., and Mizuno N. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci. 17 (1997) 7503-7522
87. Tang F.R., Chia S.C., Chen P.M., Gao H., Lee W.L., Yeo T.S., Burgunder J.M., Probst A., Sim M.K., and Ling E.A. Metabotropic glutamate receptor 2/3 in the hippocampus of patients with mesial temporal lobe epilepsy, and of rats and mice after pilocarpine-induced status epilepticus. Epilepsy Res. 59 (2004) 167-180
88. Taniura H., Sng J.C., and Yoneda Y. Histone modifications in status epilepticus induced by kainate. Histol. Histopathol. 21 (2006) 785-791
89. Tu B., Timofeeva O., Jiao Y., and Nadler J.V. Spontaneous release of neuropeptide Y tonically inhibits recurrent mossy fiber synaptic transmission in epileptic brain. J. Neurosci. 25 (2005) 1718-1729
90. Turski W.A., Cavalheiro E.A., Bortolotto Z.A., Mello L.M., Schwarz M., and Turski L. Seizures produced by pilocarpine in mice: a behavioral, electroencephalographic and morphological analysis. Brain Res. 321 (1984) 237-253
91. Vrudhula V.M., Dasgupta B., Boissard C.G., Gribkoff V.K., Santone K.S., Dalterio R.A., Lodge N.J., and Starrett Jr. J.E. Analogs of a potent maxi-K potassium channel opener with an improved inhibitory profile toward cytochrome P450 isozymes. Bioorg. Med. Chem. Lett. 15 (2005) 4286-4290
92. Wanner S.G., Koch R.O., Koschak A., Trieb M., Garcia M.L., Kaczorowski G.J., and Knaus H.G. High-conductance calcium-activated potassium channels in rat brain: pharmacology, distribution, and subunit composition. Biochemistry 38 (1999) 5392-5400
93. Wong R.K., and Traub R.D. Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J. Neurophysiol. 49 (1983) 442-458
94. Wu S.N. Large-conductance Ca2+-activated K+ channels: physiological role and pharmacology. Curr. Med. Chem. 10 (2003) 649-661
95. Yamashita M., Sugioka M., and Ogawa Y. Voltage- and Ca2+-activated potassium channels in Ca2+ store control Ca2+ release. FEBS J. 273 (2006) 3585-3597