Neuronal Ca2+ - activated K+ channels limit brain infarction and promote survival

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Liao, Yiliu ^c   Kristiansen, Ase Marit ^b   Oksvold, Cecilie P ^b   Tuvnes, Frode A ^b   Gu, Ning ^b   Rundén Pran, Elise ^b   Ruth, Peter ^a   Sausbier, Matthias ^a   Storm, Johan F ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF OSLO   (Norway)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; N METHYL DEXTRO ASPARTIC ACID; CALCIUM; CALCIUM CHANNEL; N METHYLASPARTIC ACID; POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN INFARCTION; BRAIN INFARCTION SIZE; CONTROLLED STUDY; DISEASE SEVERITY; HIPPOCAMPAL CA1 REGION; IN VITRO STUDY; IN VIVO STUDY; LASER DOPPLER FLOWMETRY; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL CULTURE; NERVE POTENTIAL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PATCH CLAMP; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; WHOLE CELL; WILD TYPE; ANIMAL; BRAIN CIRCULATION; BRAIN CORTEX; C57BL MOUSE; CELL SURVIVAL; CHEMISTRY; HOMOZYGOTE; MALE; METABOLISM; MIDDLE CEREBRAL ARTERY; NERVE CELL; PATHOLOGY;

MUS;

ANIMALS; BRAIN INFARCTION; CALCIUM; CALCIUM CHANNELS; CELL SURVIVAL; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; HOMOZYGOTE; MALE; MICE; MICE, INBRED C57BL; MIDDLE CEREBRAL ARTERY; N-METHYLASPARTATE; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS;

EID: 78651255395     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015601     Document Type: Article

References (63)

1. Deshpande JK, Siesjo BK, Wieloch T (1987) Calcium accumulation and neuronal damage in the rat hippocampus following cerebral ischemia. J Cereb Blood Flow Metab 7: 89-95.
2. MacManus JP, Buchan AM, Hill IE, Rasquinha I, Preston E (1993) Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci Lett 164: 89-92.
3. Leist M, Jaattela M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2: 589-598.
4. Nishizawa Y (2001) Glutamate release and neuronal damage in ischemia. Life Sci 69: 369-381.
5. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65: 1-105.
6. Hardingham GE, Bading H (2003) The Yin and Yang of NMDA receptor signalling. Trends Neurosci 26: 81-89.
7. Michaelis EK (1998) Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog Neurobiol 54: 369-415.
8. Ojcius DM, Zychlinsky A, Zheng LM, Young JD (1991) Ionophore-induced apoptosis: role of DNA fragmentation and calcium fluxes. Exp Cell Res 197: 43-49.
9. Wieloch T (2001) Mitochondrial involvement in acute neurodegeneration. IUBMB Life 52: 247-254.
10. Orrenius S, Zhivotovsky B, Nicotera P (2003) Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4: 552-565.
11. Storm JF (1987) Intracellular injection of a Ca2+ chelator inhibits spike repolarization in hippocampal neurons. Brain Res 435: 387-392.
12. Storm JF (1990) Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83: 161-187.
13. Robitaille R, Charlton MP (1992) Presynaptic calcium signals and transmitter release are modulated by calcium-activated potassium channels. J Neurosci 12: 297-305.
14. Gribkoff VK, Lum-Ragan JT, Boissard CG, Post-Munson DJ, Meanwell NA, et al. (1996) Effects of channel modulators on cloned large-conductance calciumactivated potassium channels. Mol Pharmacol 50: 206-217.
15. Knaus HG, Schwarzer C, Koch RO, Eberhart A, Kaczorowski GJ, et al. (1996) Distribution of high-conductance Ca(2+)-activated K+ channels in rat brain: targeting to axons and nerve terminals. J Neurosci 16: 955-963.
16. Shao LR, Halvorsrud R, Borg-Graham L, Storm JF (1999) 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): 135-146.
17. Hu H, Shao LR, Chavoshy S, Gu N, Trieb M, et al. (2001) Presynaptic Ca2+- activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J Neurosci 21: 9585-9597.
18. Gribkoff VK, Starrett JE, Jr., Dworetzky SI, Hewawasam P, Boissard CG, et al. (2001) Targeting acute ischemic stroke with a calcium-sensitive opener of maxi- K potassium channels. Nat Med 7: 471-477.
19. Schroder RL, Jespersen T, Christophersen P, Strobaek D, Jensen BS, et al. (2001) KCNQ4 channel activation by BMS-204352 and retigabine. Neuropharmacology 40: 888-898.
20. Schroder RL, Strobaek D, Olesen SP, Christophersen P (2003) Voltageindependent KCNQ4 currents induced by (+/-)BMS-204352. Pflugers Arch 446: 607-616.
21. Dupuis DS, Schroder RL, Jespersen T, Christensen JK, Christophersen P, et al. (2002) Activation of KCNQ5 channels stably expressed in HEK293 cells by BMS-204352. Eur J Pharmacol 437: 129-137.
22. Runden-Pran E, Haug FM, Storm JF, Ottersen OP (2002) BK channel activity determines the extent of cell degeneration after oxygen and glucose deprivation: a study in organotypical hippocampal slice cultures. Neuroscience 112: 277-288.
23. Meera P, Wallner M, Toro L (2000) A neuronal beta subunit (KCNMB4) makes the large conductance, voltage- and Ca2+-activated K+ channel resistant to charybdotoxin and iberiotoxin. Proc Natl Acad Sci U S A 97: 5562-5567.
24. Lancaster B, Nicoll RA (1987) Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J Physiol 389: 187-203.
25. Hille B (2001) Ion Channels of Excitable Membranes. Sunderland, MA, USA: Sinauer Associates, Inc.
26. Gu N, Vervaeke K, Storm JF (2007) BK potassium channels facilitate highfrequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. J Physiol 580: 859-882.
27. Sausbier M, Hu H, Arntz C, Feil S, Kamm S, et al. (2004) Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-activated K+ channel deficiency. Proc Natl Acad Sci U S A 101: 9474-9478.
28. Du W, Bautista JF, Yang H, ez-Sampedro A, You SA, et al. (2005) Calciumsensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nat Genet 37: 733-738.
29. ez-Sampedro A, Silverman WR, Bautista JF, Richerson GB (2006) Mechanism of increased open probability by a mutation of the BK channel. J Neurophysiol 96: 1507-1516.
30. Gu N, Liao Y, Sausbier M, Kristiansen Å, Runden-Pran E, Ottersen OP, et al. (2006) Knock-out of BK channels in mice is accompanied by increased brain infarction after transient focal cerebral ischemia in vivo and enhanced neuronal death following oxygen and glucose deprivation in vitro. Soc Neurosci Abstracts 87.17.
31. Liao Y, Kristiansen AM, Oksvold CP, Tuvnes FA, Gu N, et al. (2009) Neuronal Ca2+-activated K+ channels limit brain infarction and promote survival. Soc Neurosci Abstracts 521.19.
32. Zhang Z, Chopp M, Zhang RL, Goussev A (1997) A Mouse Model of Embolic Focal Cerebral Ischemia. J Cereb Blood Flow Metab 17: 1081-1088.
33. Parmentier-Batteur S, Jin K, Mao XO, Xie L, Greenberg DA (2002) Increased severity of stroke in CB1 cannabinoid receptor knock-out mice. J Neurosci 22: 9771-9775.
34. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, et al. (1986) Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 17: 472-476.
35. Menzies SA, Hoff JT, Betz AL (1992) Middle cerebral artery occlusion in rats: a neurological and pathological evaluation of a reproducible model. Neurosurgery 31: 100-106.
36. Barber PA, Hoyte L, Colbourne F, Buchan AM (2004) Temperature-Regulated Model of Focal Ischemia in the Mouse: A Study With Histopathological and Behavioral Outcomes. Stroke 35: 1720-1725.
37. Schabitz WR, Hoffmann TT, Heiland S, Kollmar R, Bardutzky J, et al. (2001) Delayed neuroprotective effect of insulin-like growth factor-i after experimental transient focal cerebral ischemia monitored with mri. Stroke 32: 1226-1233.
38. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182.
39. Rytter A, Cronberg T, Asztely F, Nemali S, Wieloch T (2003) Mouse hippocampal organotypic tissue cultures exposed to in vitro "ischemia" show selective and delayed CA1 damage that is aggravated by glucose. J Cereb Blood Flow Metab 23: 23-33.
40. Hansen AJ (1985) Effect of anoxia on ion distribution in the brain. Physiol Rev 65: 101-148.
41. Laake JH, Haug FM, Wieloch T, Ottersen OP (1999) A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence. Brain Research Protocols 4: 173-184.
42. Traystman RJ (2003) Animal models of focal and global cerebral ischemia. ILAR J 44: 85-95.
43. Sausbier U, Sausbier M, Sailer CA, Arntz C, Knaus HG, et al. (2006) Ca2+ - activated K+ channels of the BK-type in the mouse brain. Histochem Cell Biol 125: 725-741.
44. Sausbier M, Arntz C, Bucurenciu I, Zhao H, Zhou XB, et al. (2005) Elevated blood pressure linked to primary hyperaldosteronism and impaired vasodilation in BK channel-deficient mice. Circulation 112: 60-68.
45. Laake JH, Haug FM, Wieloch T, Ottersen OP (1999) A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence. Brain Res Brain Res Protoc 4: 173-184.
46. Noraberg J, Kristensen BW, Zimmer J (1999) Markers for neuronal degeneration in organotypic slice cultures. Brain Res Brain Res Protoc 3: 278-290.
47. Salkoff L, Butler A, Ferreira G, Santi C, Wei A (2006) High-conductance potassium channels of the SLO family. Nat Rev Neurosci 7: 921-931.
48. Storm JF (1987) Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 385: 733-759.
49. Lawson K (1996) Is there a therapeutic future for "potassium channel openers'? Clin Sci (Lond) 91: 651-663.
50. Popescu G (2005) Mechanism-based targeting of NMDA receptor functions. Cell Mol Life Sci 62: 2100-2111.
51. Haddad JJ (2005) N-methyl-D-aspartate (NMDA) and the regulation of mitogenactivated protein kinase (MAPK) signaling pathways: a revolving neurochemical axis for therapeutic intervention? Prog Neurobiol 77: 252-282.
52. Robitaille R, Garcia ML, Kaczorowski GJ, Charlton MP (1993) Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron 11: 645-655.
53. Raffaelli G, Saviane C, Mohajerani MH, Pedarzani P, Cherubini E (2004) BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus. J Physiol 557: 147-157.
54. Gu N, Storm JF (2002) Regulation of glutamate release by presynaptic calciumactivated potassium channels (BK channels) is enhanced under hypoxic conditions in rat hippocampus (CA1). Society for Neuroscience Abstracts 340.15: 35.
55. Gu N, Storm JF (2007) Feed-back regulation of glutamate release by presynaptic BK potassium channels is enhanced under low oxygenation conditions in rat hippocampus (CA1). The Annual meeting of The Scandinavian Physiological Society Poster number 11.
56. Geiger JR, Jonas P (2000) Dynamic control of presynaptic Ca(2+) inflow by fastinactivating K(+) channels in hippocampal mossy fiber boutons. Neuron 28: 927-939.
57. Bielefeldt K, Rotter JL, Jackson MB (1992) Three potassium channels in rat posterior pituitary nerve terminals. J Physiol 458: 41-67.
58. Roeper J, Pongs O (1996) Presynaptic potassium channels. Curr Opin Neurobiol 6: 338-341.
59. Cowan AI, Martin RL (1992) Ionic basis of membrane potential changes induced by anoxia in rat dorsal vagal motoneurones. J Physiol 455: 89-109.
60. Rossi DJ, Oshima T, Attwell D (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403: 316-321.
61. Faber ES, Sah P (2003) Calcium-activated potassium channels: multiple contributions to neuronal function. Neuroscientist 9: 181-194.
62. Liu H, Moczydlowski E, Haddad GG (1999) O(2) deprivation inhibits Ca(2+)- activated K(+) channels via cytosolic factors in mice neocortical neurons. J Clin Invest 104: 577-588.
63. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22: 391-397.