Neuroprotective role of ATP-sensitive potassium channels in cerebral ischemia

Acta Pharmacologica Sinica

Volumn 34, Issue 1, 2013, Pages 24-32

  Sun, Hong Shuo ^a   Feng, Zhong Ping ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

ATP sensitive potassium channel (KATP); Kir6.2; neuropathic pain; neuroprotection; nociception; stroke; SUR subunit

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2;

BRAIN CORTEX; BRAIN ISCHEMIA; CELL DAMAGE; CENTRAL NERVOUS SYSTEM; FOREBRAIN; HIPPOCAMPUS; HYPERPOLARIZATION; HYPOXIA; NERVE CELL; NEUROPATHIC PAIN; NEUROPROTECTION; NOCICEPTION; NONHUMAN; REVIEW; SEIZURE; SPINAL GANGLION; SUBSTANTIA NIGRA;

ANIMALS; BRAIN ISCHEMIA; CENTRAL NERVOUS SYSTEM; HUMANS; KATP CHANNELS; MOLECULAR TARGETED THERAPY;

EID: 84872072264     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2012.138     Document Type: Review

References (133)

1. Miller C. An overview of the potassium channel family. Genome Biol 2000;1:REVIEWS0004.
2. B. Hille. Potassium Channels and Chloride Channels in Ion channels of excitable membranes. 3ed. Sinauer Associates, Inc, Sunderkabd, Massachusetts USA, 2001. p 131-68.
3. Hodgkin AL, Huxley AF. Potassium leakage from an active nerve fibre. Nature 1946;158:376.
4. Hodgkin AL, Huxley AF. Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol 1952;116:449-72.
5. Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 2010;90:291-366.
6. Noma A. ATP-regulated K+ channels in cardiac muscle. Nature 1983;305:147-8.
7. Spruce AE, Standen NB, Stanfield PR. Voltage-dependent ATPsensitive potassium channels of skeletal muscle membrane. Nature 1985;316:736-8. (Pubitemid 16239351)
8. Standen NB, Quayle JM, Davies NW, Brayden JE, Huang Y, Nelson MT. Hyperpolarizing vasodilators activate ATP-sensitive K+ channels in arterial smooth muscle. Science 1989;245:177-80. (Pubitemid 19193933)
9. Ashford ML, Sturgess NC, Trout NJ, Gardner NJ, Hales CN. Adenosine 5'-triphosphate-sensitive ion channels in neonatal rat cultured central neurones. 1988;412:297-304.
10. Bernardi H, Fosset M, Lazdunski M. Characterization, purification, and affinity labeling of the brain [3H]glibenclamide-binding protein, a putative neuronal ATP-regulated K+ channel. Proc Natl Acad Sci U S A 1988;85:9816-20. (Pubitemid 19027216)
11. Amoroso S, Schmid-Antomarchi H, Fosset M, Lazdunski M. Glucose, sulfonylureas, and neurotransmitter release: role of ATP-sensitive K+ channels. Science 1990;247:852-4.
12. Bajgar R, Seetharaman S, Kowaltowski AJ, Garlid KD, Paucek P. Identification and properties of a novel intracellular (mitochondrial) ATP-sensitive potassium channel in brain. J Biol Chem 2001;276:33369-74.
13. Bernardi H, De W Jr, Epelbaum J, Mourre C, Amoroso S, Slama A, et al. ATP-modulated K+ channels sensitive to antidiabetic sulfonylureas are present in adenohypophysis and are involved in growth hormone release. Proc Natl Acad Sci U S A 1993;90:1340-4. (Pubitemid 23058167)
14. Inagaki N, Tsuura Y, Namba N, Masuda K, Gonoi T, Horie M, et al. Cloning and functional characterization of a novel ATP-sensitive potassium channel ubiquitously expressed in rat tissues, including pancreatic islets, pituitary, skeletal muscle, and heart. J Biol Chem 1995;270:5691-4.
15. Hunter M, Giebisch G. Calcium-activated K-channels of Amphiuma early distal tubule: inhibition by ATP. Pflugers Arch 1988;412:331-3.
16. Ashcroft FM, Harrison DE, Ashcroft SJ. Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature 1984;312:446-8. (Pubitemid 15217837)
17. Cook DL, Hales CN. Intracellular ATP directly blocks K+ channels in pancreatic B-cells. Nature 1984;311:271-3. (Pubitemid 14071146)
18. Rorsman P, Trube G. Glucose dependent K+-channels in pancreatic beta-cells are regulated by intracellular ATP. Pflugers Arch 1985;405:305-9. (Pubitemid 16202499)
19. Kakei M, Kelly RP, Ashcroft SJ, Ashcroft FM. The ATP-sensitivity of K+ channels in rat pancreatic B-cells is modulated by ADP. FEBS Lett 1986;208:63-6. (Pubitemid 17191268)
20. Seino S. ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies. Annu Rev Physiol 1999;61:337-62. (Pubitemid 29143174)
21. Seino S. Miki T. Physiological and pathophysiological roles of ATPsensitive K+ channels. Prog. Biophys. Mol Biol 2003;81:133-76. (Pubitemid 36141258)
22. Besancon E, Guo S, Lok J, Tymianski M, Lo EH. Beyond NMDA and AMPA glutamate receptors: emerging mechanisms for ionic imbalance and cell death in stroke. Trends Pharmacol. Sci 2008;29:268-75.
23. Tymianski M. Emerging mechanisms of disrupted cellular signaling in brain ischemia. Nat Neurosci 2011;14:1369-73.
24. Isomoto S, Kurachi Y. Function, regulation, pharmacology, and molecular structure of ATP-sensitive K+ channels in the cardiovascular system. J Cardiovasc Electrophysiol 1997;8:1431-46. (Pubitemid 28013656)
25. Huopio H, Shyng SL, Otonkoski T, Nichols CG. KATP channels and insulin secretion disorders. Am J Physiol Endocrinol Metab 2002;283:E207-16. (Pubitemid 34827434)
26. Sun XL, Hu G. ATP-sensitive potassium channels: a promising target for protecting neurovascular unit function in stroke. Clin Exp Pharmacol Physiol 2010;37:243-52.
27. Babenko AP, Guilar-Bryan L, Bryan J. A view of sur/KIR6. X, KATP channels. Annu Rev Physiol 1998;60:667-87.
28. Baukrowitz T, Schulte U, Oliver D, Herlitze S, Krauter T, Tucker SJ, et al. PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science 1998;282:1141-4. (Pubitemid 28516246)
29. Miki T, Nagashima K, Seino S. The structure and function of the ATPsensitive K+ channel in insulin-secreting pancreatic beta-cells. J Mol Endocrinol 1999;22:113-23. (Pubitemid 29193099)
30. Inagaki N, Gonoi T, Clement JP, Namba N, Inazawa J, Gonzalez G, et al. Reconstitution of IKATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 1995;270:1166-70.
31. Inoue I, Nagase H, Kishi K, Higuti T. ATP-sensitive K+ channel in the mitochondrial inner membrane. Nature 1991;352:244-7. (Pubitemid 21912326)
32. Garlid KD. Opening mitochondrial KATP in the heart - what happens, and what does not happen. Basic Res Cardiol 2000;95:275-9. (Pubitemid 30657585)
33. Aguilar-Bryan L, Nichols CG, Wechsler SW, Clement JP, Boyd AE III, Gonzalez G, et al. Cloning of the beta cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 1995;268:423-6.
34. Babenko AP, Bryan J. Sur domains that associate with and gate KATP pores define a novel gatekeeper. J Biol Chem 2003;278:41577-80. (Pubitemid 37310410)
35. Inagaki N, Gonoi T, Clement JP, Wang CZ, Aguilar-Bryan L, Bryan J, et al. A family of sulfonylurea receptors determines the pharmacological properties of ATP-sensitive K+ channels. Neuron 1996;16:1011-7. (Pubitemid 26171205)
36. Nichols CG. KATP channels as molecular sensors of cellular metabolism. Nature 2006;440:470-6.
37. Isomoto S, Kondo C, Yamada M, Matsumoto S, Higashiguchi O, Horio Y, et al. A novel sulfonylurea receptor forms with BIR (Kir6.2) a smooth muscle type ATP-sensitive K+ channel. J Biol Chem 1996;271:24321-4. (Pubitemid 26333158)
38. Ammala C, Moorhouse A, Gribble F, Ashfield R, Proks P, Smith PA, et al. Promiscuous coupling between the sulphonylurea receptor and inwardly rectifying potassium channels. Nature 1996;379:545-8. (Pubitemid 26049582)
39. Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992;8:67-113. (Pubitemid 23000992)
40. Nichols CG, Shyng SL, Nestorowicz A, Glaser B, Clement JP, Gonzalez G, et al. Adenosine diphosphate as an intracellular regulator of insulin secretion. Science 1996;272:1785-7. (Pubitemid 26256397)
41. Proks P, Capener CE, Jones P, Ashcroft FM. Mutations within the P-loop of Kir6.2 modulate the intraburst kinetics of the ATP-sensitive potassium channel. J Gen Physiol 2001;118:341-53. (Pubitemid 32979999)
42. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R. The open pore conformation of potassium channels. Nature 2002;417:523-6. (Pubitemid 34595913)
43. Enkvetchakul D, Nichols CG. Gating mechanism of KATP channels: function fits form. J Gen Physiol 2003;122:471-80. (Pubitemid 37420843)
44. Drain P, Li L, Wang J. KATP channel inhibition by ATP requires distinct functional domains of the cytoplasmic C terminus of the pore-forming subunit. Proc Natl Acad Sci U S A 1998;95:13953-8.
45. Drain P, Geng X, Li L. Concerted gating mechanism underlying KATP channel inhibition by ATP. Biophys J 2004;86:2101-12. (Pubitemid 38524400)
46. Babenko AP, Bryan J. SUR-dependent modulation of KATP channels by an N-terminal KIR6.2 peptide. Defining intersubunit gating interactions. J Biol Chem 2002;277:43997-4004. (Pubitemid 36157825)
47. Antcliff JF, Haider S, Proks P, Sansom MS, Ashcroft FM. Functional analysis of a structural model of the ATP-binding site of the KATP channel Kir6.2 subunit. EMBO J 2005;24:229-39. (Pubitemid 40216128)
48. Dong K, Tang LQ, MacGregor GG, Leng Q, Hebert SC. Novel nucleotidebinding sites in ATP-sensitive potassium channels formed at gating interfaces. EMBO J 2005;24:1318-29. (Pubitemid 40593053)
49. Yamada M, Kurachi Y. The nucleotide-binding domains of sulfonylurea receptor 2A and 2B play different functional roles in nicorandilinduced activation of ATP-sensitive K+ channels. Mol Pharmacol 2004;65:1198-207. (Pubitemid 38543490)
50. Campbell JD, Proks P, Lippiat JD, Sansom MS, Ashcroft FM. Identification of a functionally important negatively charged residue within the second catalytic site of the SUR1 nucleotide-binding domains. Diabetes 2004;53:S123-7. (Pubitemid 39564533)
51. Masia R, Nichols CG. Functional clustering of mutations in the dimer interface of the nucleotide binding folds of the sulfonylurea receptor. J Biol Chem 2008;283:30322-9.
52. Vergani P, Lockless SW, Nairn AC, Gadsby DC. CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature 2005;433:876-80. (Pubitemid 40314897)
53. Sharma N, Crane A, Gonzalez G, Bryan J, Aguilar-Bryan L. Familial hyperinsulinism and pancreatic beta-cell ATP-sensitive potassium channels. Kidney Int 2000;57:803-8. (Pubitemid 30434769)
54. Otonkoski T, Ammala C, Huopio H, Cote GJ, Chapman J, Cosgrove K, et al. A point mutation inactivating the sulfonylurea receptor causes the severe form of persistent hyperinsulinemic hypoglycemia of infancy in Finland. Diabetes 1999;48:408-15. (Pubitemid 29061118)
55. Misler S, Giebisch G. ATP-sensitive potassium channels in physiology, pathophysiology, and pharmacology. Curr Opin Nephrol Hypertens 1992;1:21-33.
56. Ashfield R, Gribble FM, Ashcroft SJ, Ashcroft FM. Identification of the high-affinity tolbutamide site on the SUR1 subunit of the KATP channel. Diabetes 1999;48:1341-7. (Pubitemid 29241036)
57. Mikhailov MV, Mikhailova EA, Ashcroft SJ. Molecular structure of the glibenclamide binding site of the beta-cell KATP channel. FEBS Lett 2001;499:154-60. (Pubitemid 32539340)
58. Gribble FM, Tucker SJ, Ashcroft FM. The interaction of nucleotides with the tolbutamide block of cloned ATP-sensitive K+ channel currents expressed in Xenopus oocytes: a reinterpretation. J Physiol 1997;504:35-45. (Pubitemid 27464270)
59. Ashcroft FM, Gribble FM. New windows on the mechanism of action of KATP channel openers. Trends Pharmacol Sci 2000;21:439-45.
60. Terzic A, Jahangir A, Kurachi Y. Cardiac ATP-sensitive K+ channels: regulation by intracellular nucleotides and K+ channel-opening drugs. Am J Physiol 1995;269:C525-45.
61. Moreau C, Jacquet H, Prost AL, D'hahan N, Vivaudou M. The molecular basis of the specificity of action of KATP channel openers. EMBO J 2000;19:6644-51. (Pubitemid 32011657)
62. Moreau C, Gally F, Jacquet-Bouix H, Vivaudou M. The size of a single residue of the sulfonylurea receptor dictates the effectiveness of KATP channel openers. Mol Pharmacol 2005;67:1026-33. (Pubitemid 40410405)
63. Moreau C, Prost AL, Derand R, Vivaudou M. SUR, ABC proteins targeted by KATP channel openers. J Mol Cell Cardiol 2005;38:951-63. (Pubitemid 40725943)
64. Wang H, Zhang YL, Tang XC, Feng HS, Hu G. Targeting ischemic stroke with a novel opener of ATP-sensitive potassium channels in the brain. Mol Pharmacol 2004;66:1160-8. (Pubitemid 39411056)
65. Hu LF, Wang S, Shi XR, Yao HH, Sun YH, Ding JH, et al. G ATPsensitive potassium channel opener iptakalim protected against the cytotoxicity of MPP+ on SH-SY5Y cells by decreasing extracellular glutamate level. J Neurochem 2005;94:1570-9. (Pubitemid 41324639)
66. Costa AD. Iptakalim: a new or just another KCO? Cardiovasc Res 2009;83:417-8.
67. Shyng SL, Cukras CA, Harwood J, Nichols CG. Structural determinants of PIP (2) regulation of inward rectifier KATP channels. J Gen Physiol 2000;116:599-608.
68. Shyng SL, Barbieri A, Gumusboga A, Cukras C, Pike L, Davis JN, et al. Modulation of nucleotide sensitivity of ATP-sensitive potassium channels by phosphatidylinositol-4-phosphate 5-kinase. Proc Natl Acad Sci U S A 2000;97:937-41. (Pubitemid 30070413)
69. Quinn KV, Giblin JP, Tinker A. Multisite phosphorylation mechanism for protein kinase A activation of the smooth muscle ATP-sensitive K+ channel. Circ Res 2004;94:1359-66. (Pubitemid 38724482)
70. Shi Y, Wu Z, Cui N, Shi W, Yang Y, Zhang X, et al. PKA phosphorylation of SUR2B subunit underscores vascular KATP channel activation by beta-adrenergic receptors. Am J Physiol Regul Integr Comp Physiol 2007;293:R1205-14. (Pubitemid 47358942)
71. Van Wagoner DR. Mechanosensitive gating of atrial ATP-sensitive potassium channels. Circ Res 1993;72:973-83. (Pubitemid 23105503)
72. Kang Y, Leung YM, Manning-Fox JE, Xia F, Xie H, Sheu L, et al. Syntaxin-1A inhibits cardiac KATP channels by its actions on nucleotide binding folds 1 and 2 of sulfonylurea receptor 2A. J Biol Chem 2004;279:47125-31. (Pubitemid 39518369)
73. Pasyk EA, Kang Y, Huang X, Cui N, Sheu L, Gaisano HY. Syntaxin-1A binds the nucleotide-binding folds of sulphonylurea receptor 1 to regulate the KATP channel. J Biol Chem 2004;279:4234-40. (Pubitemid 38199010)
74. Chao C, Liang T, Kang Y, Lin X, Xie H, Feng ZP, et al. Syntaxin-1A inhibits KATP channels by interacting with specific conserved motifs within sulfonylurea receptor 2A. J Mol Cell Cardiol 2011;51:790-802.
75. Chang N, Liang T, Lin X, Kang Y, Xie H, Feng ZP, et al. Syntaxin-1A interacts with distinct domains within nucleotide-binding folds of sulfonylurea receptor 1 to inhibit beta-cell ATP-sensitive potassium channels. J Biol Chem 2011;286:23308-18.
76. Cui N, Kang Y, He Y, Leung YM, Xie H, Pasyk EA, et al. H3 domain of syntaxin 1A inhibits KATP channels by its actions on the sulfonylurea receptor 1 nucleotide-binding folds-1 and -2. J Biol Chem 2004;279:53259-65. (Pubitemid 40051829)
77. Chen PC, Bruederle CE, Gaisano HY, Shyng SL. Syntaxin 1A regulates surface expression of {beta}-cell ATP-sensitive potassium channels. Am J Physiol Cell Physiol 2011;300:C506-16.
78. Ng B, Kang Y, Elias CL, He Y, Xie H, Hansen JB, et al. The actions of a novel potent islet beta-cell specific ATP-sensitive K+ channel opener can be modulated by syntaxin-1A acting on sulfonylurea receptor 1. Diabetes 2007;56:2124-34. (Pubitemid 47195828)
79. Ng B, Kang Y, Xie H, Sun H, Gaisano HY. Syntaxin-1A inhibition of P-1075, cromakalim, and diazoxide actions on mouse cardiac ATPsensitive potassium channel. Cardiovasc Res 2008;80:365-74.
80. Bernardi H, Fosset M, Lazdunski M. ATP/ADP binding sites are present in the sulfonylurea binding protein associated with brain ATPsensitive K+ channels. Biochemistry 1992;31:6328-32.
81. Roper J, Ashcroft FM. Metabolic inhibition and low internal ATP activate KATP channels in rat dopaminergic substantia nigra neurones. Pflugers Arch 1995;430:44-54.
82. Stanford IM, Lacey MG. Electrophysiological investigation of adenosine trisphosphate-sensitive potassium channels in the rat substantia nigra pars reticulata. Neuroscience 1996;74:499-509. (Pubitemid 26274219)
83. Ohno-Shosaku T, Yamamoto C. Identification of an ATP-sensitive K+ channel in rat cultured cortical neurons. Pflugers Arch 1992;422:260-6. (Pubitemid 23002137)
84. Zawar C, Plant TD, Schirra C, Konnerth A, Neumcke B. Cell-type specific expression of ATP-sensitive potassium channels in the rat hippocampus. J Physiol 1999;514:327-41. (Pubitemid 29055963)
85. Ashford ML, Boden PR, Treherne JM. Tolbutamide excites rat glucoreceptive ventromedial hypothalamic neurones by indirect inhibition of ATP-K+ channels. Br J Pharmacol 1990;101:531-40. (Pubitemid 20357171)
86. Ashford ML, Boden PR, Treherne JM. Glucose-induced excitation of hypothalamic neurones is mediated by ATP-sensitive K+ channels. Pflugers Arch 1990;415:479-83. (Pubitemid 20040708)
87. Zhou M, Tanaka O, Suzuki M, Sekiguchi M, Takata K, Kawahara K, et al. Localization of pore-forming subunit of the ATP-sensitive K (+) - channel, Kir6.2, in rat brain neurons and glial cells. Brain Res Mol Brain Res 2002;101:23-32. (Pubitemid 34465557)
88. Fujimura N, Tanaka E, Yamamoto S, Shigemori M, Higashi H. Contri bution of ATP-sensitive potassium channels to hypoxic hyperpolarization in rat hippocampal CA1 neurons in vitro. J Neurophysiol 1997;77:378-85. (Pubitemid 27053791)
89. Trapp S, Ballanyi K. KATP channel mediation of anoxia-induced outward current in rat dorsal vagal neurons in vitro. J Physiol 1995;487:37-50.
90. Dunn-Meynell AA, Rawson NE, Levin BE. Distribution and phenotype of neurons containing the ATP-sensitive K+ channel in rat brain. Brain Res 1998;814:41-54. (Pubitemid 29023410)
91. Liss B, Roeper J. A role for neuronal KATP channels in metabolic control of the seizure gate. Trends Pharmacol Sci 2001;22:599-601.
92. Sun HS, Feng ZP, Miki T, Seino S, French RJ. Enhanced neuronal damage after ischemic insults in mice lacking Kir6.2-containing ATPsensitive K+ channels. J Neurophysiol 2006;95:2590-601.
93. Sun HS, Feng ZP, Barber PA, Buchan AM, French RJ. Kir6.2-containing ATP-sensitive potassium channels protect cortical neurons from ischemic/anoxic injury in vitro and in vivo. Neuroscience 2007;144:1509-15. (Pubitemid 46123797)
94. Miki T, Liss B, Minami K, Shiuchi T, Saraya A, Kashima Y, et al. ATPsensitive K+ channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat Neurosci 2001;4:507-12. (Pubitemid 32397188)
95. Yamada K, Ji JJ, Yuan H, Miki T, Sato S, Horimoto N, et al. Protective role of ATP-sensitive potassium channels in hypoxia-induced generalized seizure. Science 2001;292:1543-6. (Pubitemid 32493422)
96. Thomzig A, Laube G, Pruss H, Veh RW. Pore-forming subunits of KATP channels, Kir6.1 and Kir6.2, display prominent differences in regional and cellular distribution in the rat brain. J Comp Neurol 2005;484:313-30. (Pubitemid 40316259)
97. Mourre C, Ben AY, Bernardi H, Fosset M, Lazdunski M. Antidiabetic sulfonylureas: localization of binding sites in the brain and effects on the hyperpolarization induced by anoxia in hippocampal slices. Brain Res 1989;486:159-64. (Pubitemid 19102860)
98. Taborsky GJ Jr, Ahren B, Havel PJ. Autonomic mediation of glucagon secretion during hypoglycemia: implications for impaired alpha-cell responses in type 1 diabetes. Diabetes 1998;47:995-1005. (Pubitemid 28294539)
99. Karschin C, Ecke C, Ashcroft FM, Karschin A. Overlapping distribution of KATP channel-forming Kir6.2 subunit and the sulfonylurea receptor SUR1 in rodent brain. FEBS Lett 1997;401:59-64. (Pubitemid 27051258)
100. Pierrefiche O, Bischoff AM, Richter DW. ATP-sensitive K+ channels are functional in expiratory neurones of normoxic cats. J Physiol 1996;494:399-409. (Pubitemid 26318779)
101. Allen TG, Brown DA. Modulation of the excitability of cholinergic basal forebrain neurones by KATP channels. J Physiol 2004;554:353-70. (Pubitemid 38181349)
102. Tanner GR, Lutas A, Martinez-Francois JR, Yellen G. Single KATP channel opening in response to action potential firing in mouse dentate granule neurons. J Neurosci 2011;31:8689-96.
103. Haller M, Mironov SL, Karschin A, Richter DW. Dynamic activation of K (ATP) channels in rhythmically active neurons. J Physiol 2001;537:69-81. (Pubitemid 33076955)
104. Busija DW, Lacza Z, Rajapakse N, Shimizu K, Kis B, Bari F, et al. Targeting mitochondrial ATP-sensitive potassium channels - a novel approach to neuroprotection. Brain Res Rev 2004;46:282-94. (Pubitemid 39574329)
105. Zoga V, Kawano T, Liang MY, Bienengraeber M, Weihrauch D, McCallum B, et al. KATP channel subunits in rat dorsal root ganglia: alterations by painful axotomy. Mol Pain 2010;6:6.
106. Kawano T, Zoga V, Gemes G, McCallum JB, Wu HE, Pravdic D, et al. Suppressed Ca2+/CaM/CaMKII-dependent KATP channel activity in primary afferent neurons mediates hyperalgesia after axotomy. Proc Natl Acad Sci U S A 2009;106:8725-30.
107. Hernandez-Sanchez C, Basile AS, Fedorova I, Arima H, Stannard B, Fernandez AM, et al. Mice transgenically overexpressing sulfonylurea receptor 1 in forebrain resist seizure induction and excitotoxic neuron death. Proc Natl Acad Sci U S A 2001;98:3549-54. (Pubitemid 32220882)
108. Iadarola MJ, Gale K. Substantia nigra: site of anticonvulsant activity mediated by gamma-aminobutyric acid. Science 1982;218:1237-40. (Pubitemid 13224837)
109. Yamada K, Inagaki N. Neuroprotection by KATP channels. J Mol Cell Cardiol 2005;38:945-9.
110. Hicks GA, Hudson AL, Henderson G. Localization of high affinity [3H]glibenclamide binding sites within the substantia nigra zona reticulata of the rat brain. Neuroscience 1994;61:285-92. (Pubitemid 24219007)
111. Munoz A, Nakazaki M, Goodman JC, Barrios R, Onetti CG, Bryan J, et al. Ischemic preconditioning in the hippocampus of a knockout mouse lacking SUR1-based KATP channels. Stroke 2003;34:164-70. (Pubitemid 36070818)
112. Benarroch EE. Potassium channels: brief overview and implications in epilepsy. Neurology 2009;72:664-9.
113. Gloyn AL, Pearson ER, Antcliff JF, Proks P, Bruining GJ, Slingerland AS, et al. Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes. N Engl J Med 2004;350:1838-49. (Pubitemid 38917250)
114. Ashcroft FM. Adenosine 5'-triphosphate-sensitive potassium channels. Annu Rev Neurosci 1988;11:97-118. (Pubitemid 18081035)
115. Heurteaux C, Bertaina V, Widmann C, Lazdunski M. K+ channel openers prevent global ischemia-induced expression of c-fos, c-jun, heat shock protein, and amyloid beta-protein precursor genes and neuronal death in rat hippocampus. Proc Natl Acad Sci U S A 1993;90:9431-5. (Pubitemid 23315798)
116. Asemu G, Papousek F, Ostadal B, Kolar F. Adaptation to high altitude hypoxia protects the rat heart against ischemia-induced arrhythmias. Involvement of mitochondrial K (ATP) channel. J Mol Cell Cardiol 1999;31:1821-31. (Pubitemid 29458701)
117. Testai L, Rapposelli S, Calderone V. Cardiac ATP-sensitive potassium channels: a potential target for an anti-ischaemic pharmacological strategy. Cardiovasc Hematol Agents Med Chem 2007;5:79-90. (Pubitemid 46062424)
118. Kim KO, Choe G, Chung SH, Kim CS. Delayed pharmacological preconditioning effect of mitochondrial ATP-sensitive potassium channel opener on neurologic injury in a rabbit model of spinal cord ischemia. Acta Anaesthesiol Scand 2008;52:236-42.
119. Mayanagi K, Gaspar T, Katakam PV, Busija DW. Systemic administration of diazoxide induces delayed preconditioning against transient focal cerebral ischemia in rats. Brain Res 2007;1168:106-11. (Pubitemid 47321902)
120. Shimizu K, Lacza Z, Rajapakse N, Horiguchi T, Snipes J, Busija DW. MitoK (ATP) opener, diazoxide, reduces neuronal damage after middle cerebral artery occlusion in the rat. Am J Physiol Heart Circ Physiol 2002;283:H1005-11.
121. Mayanagi K, Gaspar T, Katakam PV, Kis B, Busija DW. The mitochondrial KATP channel opener BMS-191095 reduces neuronal damage after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 2007;27:348-55. (Pubitemid 46148461)
122. Liu D, Lu C, Wan R, Auyeung WW, Mattson MP. Activation of mitochondrial ATP-dependent potassium channels protects neurons against ischemia-induced death by a mechanism involving suppression of Bax translocation and cytochrome c release. J Cereb Blood Flow Metab 2002;22:431-43. (Pubitemid 34273599)
123. Liu D, Slevin JR, Lu C, Chan SL, Hansson M, Elmer E, et al. Involvement of mitochondrial K+ release and cellular efflux in ischemic and apoptotic neuronal death. J Neurochem 2003;86:966-79. (Pubitemid 36988808)
124. Bantel C, Maze M, Trapp S. Neuronal preconditioning by inhalational anesthetics: evidence for the role of plasmalemmal adenosine triphosphate-sensitive potassium channels. Anesthesiology 2009;110:986-95.
125. Gross GJ, Fryer RM. Sarcolemmal versus mitochondrial ATP-sensitive K+ channels and myocardial preconditioning. Circ Res 1999;84:973-9. (Pubitemid 29227676)
126. Blondeau N, Plamondon H, Richelme C, Heurteaux C, Lazdunski M. KATP channel openers, adenosine agonists and epileptic preconditioning are stress signals inducing hippocampal neuroprotection. Neuroscience 2000;100:465-74.
127. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 1999;79:1431-568. (Pubitemid 29473320)
128. Johansen FF. Interneurons in rat hippocampus after cerebral ischemia. Morphometric, functional, and therapeutic investigations. Acta Neurol Scand Suppl 1993;150:1-32.
129. Yamamoto S, Tanaka E, Higashi H. Mediation by intracellular calciumdependent signals of hypoxic hyperpolarization in rat hippocampal CA1 neurons in vitro. J Neurophysiol 1997;77:386-92. (Pubitemid 27053792)
130. Garcia De AS, Franke H, Pissarek M, Nieber K, Illes P. Neuroprotection by ATP-dependent potassium channels in rat neocortical brain slices during hypoxia. Neurosci Lett 1999;273:13-6. (Pubitemid 29415691)
131. Heron-Milhavet L, Xue-Jun. Y, Vannucci SJ, Wood TL, Willing LB, Stannard B, et al. Protection against hypoxic-ischemic injury in transgenic mice overexpressing Kir6.2 channel pore in forebrain. Mol Cell Neurosci 2004;25:585-93. (Pubitemid 38481469)
132. Simard JM, Chen M, Tarasov KV, Bhatta S, Ivanova S, Melnitchenko L, et al. Newly expressed SUR1-regulated NC (Ca-ATP) channel mediates cerebral edema after ischemic stroke. Nat Med 2006;12:433-40.
133. Ortega FJ, Gimeno-Bayon J, Espinosa-Parrilla JF, Carrasco JL, Batlle M, Pugliese M, et al. ATP-dependent potassium channel blockade strengthens microglial neuroprotection after hypoxia-ischemia in rats. Exp Neurol 2012;235:282-96.