Network excitability in a model of chronic temporal lobe epilepsy critically depends on SK channel-mediated AHP currents

Neurobiology of Disease

Volumn 45, Issue 1, 2012, Pages 337-347

  Schulz, Robert ^a   Kirschstein, Timo ^a   Brehme, Hannes ^a   Porath, Katrin ^a   Mikkat, Ulrike ^a   Köhling, Rüdiger ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

After hyperpolarizing potential; Ca 2+ activated K + channel; Patch clamp; Status epilepticus; UCL1684

Indexed keywords

MAGNESIUM ION; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE EXACERBATION; DOWN REGULATION; EPILEPTOGENESIS; HIPPOCAMPAL CA1 REGION; MALE; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; QUANTITATIVE ANALYSIS; RAT; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TEMPORAL LOBE EPILEPSY; TISSUE SECTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; MALE; NERVE NET; NEURONS; PILOCARPINE; RATS; RATS, WISTAR; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS;

EID: 81955162907     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.08.019     Document Type: Article

References (74)

1. Aika Y., Ren J.Q., Kosaka K., Kosaka T. Quantitative analysis of GABA-like-immunoreactive and parvalbumin-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the disector. Exp. Brain Res. 1994, 99:267-276.
2. + channel multiprotein complexes. J. Neurosci. 2007, 27:2369-2376.
3. 2+ currents in epilepsy. Epilepsy Res. 1998, 32:321-332.
4. Becker A.J., Pitsch J., Sochivko D., Opitz T., Staniek M., Chen C.C., Campbell K.P., Schoch S., Yaari Y., Beck H. Transcriptional upregulation of Cav3.2 mediates epileptogenesis in the pilocarpine model of epilepsy. J. Neurosci. 2008, 28:13341-13353.
5. Behr J., Gloveli T., Heinemann U. Kindling induces a transient suppression of afterhyperpolarization in rat subicular neurons. Brain Res. 2000, 867:259-264.
6. Bernard C., Anderson A., Becker A., Poolos N.P., Beck H., Johnston D. Acquired dendritic channelopathy in temporal lobe epilepsy. Science 2004, 305:532-535.
7. + channels and regulates channel gating. Neuron 2004, 43:847-858.
8. + channels as targets of CNS drug development. Curr. Drug Targets CNS Neurol. Disord. 2004, 3:161-167.
9. + channels of small conductance in cultured rat skeletal muscle. Nature 1986, 323:718-720.
10. Bloodgood B.L., Sabatini B.L. Ca(2+) signaling in dendritic spines. Curr. Opin. Neurobiol. 2007, 17:345-351.
11. + channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J. Neurosci. 2004, 24:5301-5306.
12. Bond C.T., Maylie J., Adelman J.P. SK channels in excitability, pacemaking and synaptic integration. Curr. Opin. Neurobiol. 2005, 15:305-311.
13. Bowden S.E., Fletcher S., Loane D.J., Marrion N.V. Somatic colocalization of rat SK1 and D class (Ca(v)1.2) L-type calcium channels in rat CA1 hippocampal pyramidal neurons. J. Neurosci. 2001, 21:RC175-
14. Cai X., Liang C.W., Muralidharan S., Kao J.P., Tang C.M., Thompson S.M. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 2004, 44:351-364.
15. Campos R.J., Galanakis D., Piergentili A., Bhandari K., Ganellin C.R., Dunn P.M., Jenkinson D.H. Synthesis, molecular modeling, and pharmacological testing of bis-quinolinium cyclophanes: potent, non-peptidic blockers of the apamin-sensitive Ca(2+)-activated K(+) channel. J. Med. Chem. 2000, 43:420-431.
16. Cohen I., Navarro V., Clemenceau S., Baulac M., Miles R. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 2002, 298:1418-1421.
17. DeLorenzo R.J. A molecular approach to the calcium signal in brain: relationship to synaptic modulation and seizure discharge. Adv. Neurol. 1986, 44:435-464.
18. DeLorenzo R.J., Sun D.A., Deshpande L.S. Erratum to "Cellular mechanisms underlying acquired epilepsy: the calcium hypothesis of the induction and maintenance of epilepsy." [Pharmacol. Ther. 105(3), 2005, pp. 229-266]. Pharmacol. Ther. 2006, 111:288-325.
19. Empson R.M., Jefferys J.G. Ca(2+) entry through L-type Ca(2+) channels helps terminate epileptiform activity by activation of a Ca(2+) dependent afterhyperpolarisation in hippocampal CA3. Neuroscience 2001, 102:297-306.
20. Faas G.C., Vreugdenhil M., Wadman W.J. Calcium currents in pyramidal CA1 neurons in vitro after kindling epileptogenesis in the hippocampus of the rat. Neuroscience 1996, 75:57-67.
21. Faber E.S., Sah P. Calcium-activated potassium channels: multiple contributions to neuronal function. Neuroscientist 2003, 9:181-194.
22. Fernandez de Sevilla D., Garduno J., Galvan E., Buno W. Calcium-activated afterhyperpolarizations regulate synchronization and timing of epileptiform bursts in hippocampal CA3 pyramidal neurons. J. Neurophysiol. 2006, 96:3028-3041.
23. Garduno J., Galvan E., Fernandez D.S., Buno W. 1-Ethyl-2-benzimidazolinone (EBIO) suppresses epileptiform activity in in vitro hippocampus. Neuropharmacology 2005, 49:376-388.
24. Gu N., Hu H., Vervaeke K., Storm J.F. SK (KCa2) channels do not control somatic excitability in CA1 pyramidal neurons but can be activated by dendritic excitatory synapses and regulate their impact. J. Neurophysiol. 2008, 100:2589-2604.
25. Gu N., Vervaeke K., Hu H., Storm J.F. Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J. Physiol. 2005, 566:689-715.
26. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 1997, 387:869-875.
27. Hotson J.R., Prince D.A. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J. Neurophysiol. 1980, 43:409-419.
28. Kamal A., Notenboom R.G., de Graan P.N., Ramakers G.M. Persistent changes in action potential broadening and the slow afterhyperpolarization in rat CA1 pyramidal cells after febrile seizures. Eur. J. Neurosci. 2006, 23:2230-2234.
29. Keen J.E., Khawaled R., Farrens D.L., Neelands T., Rivard A., Bond C.T., Janowsky A., Fakler B., Adelman J.P., Maylie J. Domains responsible for constitutive and Ca(2+)-dependent interactions between calmodulin and small conductance Ca(2+)-activated potassium channels. J. Neurosci. 1999, 19:8830-8838.
30. Kirschstein T., Schulz R., Mikkat S., Kohling R., Glocker M.O. Proteome analysis in hippocampal tissue of pilocarpine-treated chronically epileptic rats. Acta Physiol 2007, 189(Suppl. 653):116-
31. Kohler M., Hirschberg B., Bond C.T., Kinzie J.M., Marrion N.V., Maylie J., Adelman J.P. Small-conductance, calcium-activated potassium channels from mammalian brain. Science 1996, 273:1709-1714.
32. Kong W.J., Guo C.K., Zhang S., Zhang X.W., Wang Y.J., Li Z.W. Fast cholinergic efferent inhibition in guinea pig outer hair cells. Brain Res. 2006, 1102:103-108.
33. Lappin S.C., Dale T.J., Brown J.T., Trezise D.J., Davies C.H. Activation of SK channels inhibits epileptiform bursting in hippocampal CA3 neurons. Brain Res. 2005, 1065:37-46.
34. + channels and calmodulin: cell surface expression and gating. J. Biol. Chem. 2003, 278:25940-25946.
35. Lin M.T., Lujan R., Watanabe M., Adelman J.P., Maylie J. SK2 channel plasticity contributes to LTP at Schaffer collateral-CA1 synapses. Nat. Neurosci. 2008, 11:170-177.
36. Madison D.V., Nicoll R.A. Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J. Physiol. 1984, 354:319-331.
37. 2+ channels in hippocampal neurons. Nature 1998, 395:900-905.
38. + channels and calmodulin. J. Physiol. 2004, 554:255-261.
39. Mody I., Lambert J.D., Heinemann U. Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. J. Neurophysiol. 1987, 57:869-888.
40. + channels interacts with both SK1 and SK2 subunits in a heterologous expression system. J. Biol. Chem. 2004, 279:1003-1009.
41. + channel SK2. J. Neurochem. 2008, 106:2312-2321.
42. Nagao T., Avoli M., Gloor P. Interictal discharges in the hippocampus of rats with long-term pilocarpine seizures. Neurosci. Lett. 1994, 174:160-164.
43. 2+-mediated feedback loop in dendritic spines. Nat. Neurosci. 2005, 8:642-649.
44. Pacheco Otalora L.F., Hernandez E.F., Arshadmansab M.F., Francisco S., Willis M., Ermolinsky B., Zarei M., Knaus H.G., Garrido-Sanabria E.R. Down-regulation of BK channel expression in the pilocarpine model of temporal lobe epilepsy. Brain Res. 2008, 1200:116-131.
45. + channels. J. Biol. Chem. 2001, 276:9762-9769.
46. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 1993, 11:1023-1035.
47. 2+-calmodulin in intact cells. J. Biol. Chem. 1999, 274:6827-6830.
48. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 1972, 32:281-294.
49. 2+-activated potassium channel, Sk2, through direct phosphorylation by cAMP-dependent protein kinase. J. Biol. Chem. 2006, 281:11769-11779.
50. + channels. J. Physiol. Paris 1984, 79:259-264.
51. + channels in rat brain. J. Neurosci. 2002, 22:9698-9707.
52. 2+-activated potassium channel subunits, SK1, SK2, and SK3 in mouse brain. Mol. Cell. Neurosci. 2004, 26:458-469.
53. 2+/calmodulin. Nature 2001, 410:1120-1124.
54. Schwindt P.C., Spain W.J., Foehring R.C., Stafstrom C.E., Chubb M.C., Crill W.E. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 1988, 59:424-449.
55. + conductance. Exp. Brain Res. 1991, 86:141-150.
56. + channels modulate synaptic plasticity and memory encoding. J. Neurosci. 2002, 22:10163-10171.
57. + current in hippocampal pyramidal neurons. Proc. Natl Acad. Sci. USA 1999, 96:4662-4667.
58. Stocker M., Pedarzani P. Differential distribution of three Ca(2+)-activated K(+) channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol. Cell. Neurosci. 2000, 15:476-493.
59. Storm J.F. Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J. Physiol. 1987, 385:733-759.
60. Storm J.F. An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J. Physiol. 1989, 409:171-190.
61. Storm J.F. Potassium currents in hippocampal pyramidal cells. Prog. Brain Res. 1990, 83:161-187.
62. Strassmaier T., Bond C.T., Sailer C.A., Knaus H.G., Maylie J., Adelman J.P. A novel isoform of SK2 assembles with other SK subunits in mouse brain. J. Biol. Chem. 2005, 280:21231-21236.
63. Strobaek D., Jorgensen T.D., Christophersen P., Ahring P.K., Olesen S.P. Pharmacological characterization of small-conductance Ca(2+)-activated K(+) channels stably expressed in HEK 293 cells. Br. J. Pharmacol. 2000, 129:991-999.
64. 2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J. Neurosci. 2002, 22:3645-3655.
65. Timm F. Histochemistry of heavy metals; the sulfide-silver procedure. Dtsch. Z. Gesamte Gerichtl. Med. 1958, 46:706-711.
66. Tomita H., Shakkottai V.G., Gutman G.A., Sun G., Bunney W.E., Cahalan M.D., Chandy K.G., Gargus J.J. Novel truncated isoform of SK3 potassium channel is a potent dominant-negative regulator of SK currents: implications in schizophrenia. Mol. Psychiatry 2003, 8(524-35):460.
67. Turski W.A., Cavalheiro E.A., Schwarz M., Czuczwar S.J., Kleinrok Z., Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav. Brain Res. 1983, 9:315-335.
68. Verma-Ahuja S., Evans M.S., Pencek T.L. Evidence for decreased calcium dependent potassium conductance in hippocampal CA3 neurons of genetically epilepsy-prone rats. Epilepsy Res. 1995, 22:137-144.
69. Waroux O., Massotte L., Alleva L., Graulich A., Thomas E., Liegeois J.F., Scuvee-Moreau J., Seutin V. SK channels control the firing pattern of midbrain dopaminergic neurons in vivo. Eur. J. Neurosci. 2005, 22:3111-3121.
70. Wolfart J., Neuhoff H., Franz O., Roeper J. Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J. Neurosci. 2001, 21:3443-3456.
71. Xia X.M., Fakler B., Rivard A., Wayman G., Johnson-Pais T., Keen J.E., Ishii T., Hirschberg B., Bond C.T., Lutsenko S., Maylie J., Adelman J.P. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 1998, 395:503-507.
72. Yechikhov S., Morenkov E., Chulanova T., Godukhin O., Shchipakina T. Involvement of cAMP- and Ca(2+)/calmodulin-dependent neuronal protein phosphorylation in mechanisms underlying genetic predisposition to audiogenic seizures in rats. Epilepsy Res. 2001, 46:15-25.
73. Yue C., Yaari Y. KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci. 2004, 24:4614-4624.
74. Yue C., Yaari Y. Axo-somatic and apical dendritic Kv7/M channels differentially regulate the intrinsic excitability of adult rat CA1 pyramidal cells. J. Neurophysiol. 2006, 95:3480-3495.