Role of KATP channels in protection against neuronal excitatory insults

Journal of Neurochemistry

Volumn 103, Issue 5, 2007, Pages 1721-1729

  Soundarapandian, Mangala M ^a   Zhong, Xiaofen ^a   Peng, Lisheng ^a   Wu, Di ^a   Lu, Youming ^a,b  

^a UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

Epilepsy; Excitotoxicity; Glutamate; Ischemia; KATP; Synaptic degeneration

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

BRAIN ISCHEMIA; CELL DEATH; CELL PROTECTION; ENZYME RELEASE; EPILEPSY; HUMAN; MITOCHONDRION; MOLECULAR DYNAMICS; MOLECULAR MODEL; NERVE CELL; NERVE DEGENERATION; NERVE ENDING; NEUROPROTECTION; NONHUMAN; PANCREAS ISLET BETA CELL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SYNAPTIC TRANSMISSION; UPREGULATION;

ANIMALS; GLUTAMIC ACID; ION CHANNEL GATING; MODELS, BIOLOGICAL; NERVE DEGENERATION; NEURONS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 36249010402     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04963.x     Document Type: Review

References (115)

1. Allen T. G. Brown D. A. (2004) Modulation of the excitability of cholinergic basal forebrain neurones by KATP channels. J. Physiol. 554, 353 370.
2. + channels. Science 247, 852 854.
3. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A. Nicotera P. (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961 973.
4. Antcliff J. F., Haider S., Proks P., Sansom M. S. Ashcroft F. M. (2005) Functional analysis of a structural model of the ATP-binding site of the KATP channel Kir6.2 subunit. EMBO J. 24, 229 239.
5. Ardehali H. (2005) Cytoprotective channels in mitochondria. J. Bioenerg. Biomembr. 37, 171 177.
6. Ardehali H. O'Rourke B. (2005) Mitochondrial K(ATP) channels in cell survival and death. J. Mol. Cell. Cardiol. 39, 7 16.
7. Arundine M. Tymianski M. (2003) Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34, 325 337.
8. Arundine M. Tymianski M. (2004) Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol. Life Sci. 61, 657 668.
9. + channels. Trends Neurosci. 21, 288 294.
10. Ashfield R., Gribble F. M., Ashcroft S. J. Ashcroft F. M. (1999) Identification of the high-affinity tolbutamide site on the SUR1 subunit of the K(ATP) channel. Diabetes 48, 1341 1347.
11. 2 underlies glutamate-dependent inhibition of striatal dopamine release. Proc. Natl Acad. Sci. USA 100, 11729 11734.
12. Ballanyi K. (2004) Protective role of neuronal KATP channels in brain hypoxia. J. Exp. Biol. 207, 3201 3212.
13. Bancila V., Nikonenko I., Dunant Y. Bloc A. (2004) Zinc inhibits glutamate release via activation of pre-synaptic K channels and reduces ischaemic damage in rat hippocampus. J. Neurochem. 90, 1243 1250.
14. 2 elevation, not ATP depletion. J. Neurosci. 25, 10029 10040.
15. Barnett D. W., Pressel D. M., Chern H. T., Scharp D. W. Misler S. (1994) cAMP-enhancing agents 'permit' stimulus-secretion coupling in canine pancreatic islet beta-cells. J. Membr. Biol. 138, 113 120.
16. Baukrowitz T., Schulte U., Oliver D., Herlitze S., Krauter T., Tucker S. J., Ruppersberg J. P. Fakler B. (1998) PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science 282, 1141 1144.
17. Ben-Ari Y. Cossart R. (2000) Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci. 23, 580 587.
18. Birnbaumer L., Campbell K. P., Catterall W. A. et al. (1994) The naming of voltage-gated calcium channels. Neuron 13, 505 506.
19. Bryan J. Aguilar-Bryan L. (1999) Sulfonylurea receptors: ABC transporters that regulate ATP-sensitive K(+) channels. Biochim. Biophys. Acta 1461, 285 303.
20. Camacho A. Massieu L. (2006) Role of glutamate transporters in the clearance and release of glutamate during ischemia and its relation to neuronal death. Arch. Med. Res. 37, 11 18.
21. Cartier E. A., Conti L. R., Vandenberg C. A. Shyng S. L. (2001) Defective trafficking and function of KATP channels caused by a sulfonylurea receptor 1 mutation associated with persistent hyperinsulinemic hypoglycemia of infancy. Proc. Natl Acad. Sci. USA 98, 2882 2887.
22. Chen M., Dong Y. Simard J. M. (2003) Functional coupling between sulfonylurea receptor type 1 and a nonselective cation channel in reactive astrocytes from adult rat brain. J. Neurosci. 23, 8568 8577.
23. Choi D. W. (1987) Ionic dependence of glutamate neurotoxicity. J. Neurosci. 7, 369 379.
24. Choi D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623 634.
25. Choi D. W. (1992) Excitotoxic cell death. J. Neurobiol. 23, 1261 1276.
26. Collingridge G. L. Lester R. A. (1989) Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev. 41, 143 210.
27. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 16, 288 297.
28. Cuong D. V., Kim N., Joo H., Youm J. B., Chung J. Y., Lee Y., Park W. S., Kim E., Park Y. S. Han J. (2005) Subunit composition of ATP-sensitive potassium channels in mitochondria of rat hearts. Mitochondrion 5, 121 133.
29. + channels in rat hearts. Am. J. Physiol Heart Circ. Physiol. 290, H1808 H1817.
30. Frandsen A. Schousboe A. (1993) Excitatory amino acid-mediated cytotoxicity and calcium homeostasis in cultured neurons. J. Neurochem. 60, 1202 1211.
31. + channels in hypoxia-induced neuronal injuries. Clin. Exp. Pharmacol. Physiol. 27, 569 574.
32. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193 204.
33. Glaser B., Chiu K. C., Anker R., Nestorowicz A., Landau H., Ben-Bassat H., Shlomai Z., Kaiser N., Thornton P. S. Stanley C. A. (1994) Familial hyperinsulinism maps to chromosome 11p14-15.1, 30 cM centromeric to the insulin gene. Nat. Genet. 7, 185 188.
34. Gloyn A. L., Pearson E. R., Antcliff J. F. et al. (2004) Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes. N. Engl. J. Med. 350, 1938 1949.
35. Gloyn A. L., Reimann F., Girard C. et al. (2005) Relapsing diabetes can result from moderately activating mutations in KCNJ11. Hum. Mol. Genet. 14, 925 934.
36. Gogvadze V. Orrenius S. (2006) Mitochondrial regulation of apoptotic cell death. Chem. Biol. Interact. 163, 4 14.
37. 2+ influx in hippocampal CA1 neurons of gerbil. J. Neurosci. 17, 6179 6188.
38. + channels and myocardial preconditioning. Circ. Res. 84, 973 979.
39. Gunter T. E. Gunter K. K. (2001) Uptake of calcium by mitochondria: transport and possible function. IUBMB Life 52, 197 204.
40. Haider S., Antcliff J. F., Proks P., Sansom M. S. Ashcroft F. M. (2005) Focus on Kir6.2: a key component of the ATP-sensitive potassium channel. J. Mol. Cell. Cardiol. 38, 927 936.
41. Hara M. R. Snyder S. H. (2007) Cell signaling and neuronal death. Annu. Rev. Pharmacol. Toxicol. 47, 117 141.
42. Hernandez-Sanchez C., Basile A. S., Fedorova I., Arima H., Stannard B., Fernandez A. M., Ito Y. LeRoith D. (2001) Mice transgenically overexpressing sulfonylurea receptor 1 in forebrain resist seizure induction and excitotoxic neuron death. Proc. Natl Acad. Sci. USA 98, 3549 3554.
43. Hollmann M. Heinemann S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31 108.
44. 2+ overload in rat cardiac mitochondria. J. Physiol. 519, 347 360.
45. Holz G. G., Kang G., Harbeck M., Roe M. W. Chepurny O. G. (2006) Cell physiology of cAMP sensor Epac. J. Physiol. 577, 5 15.
46. Hussain K. Cosgrove K. E. (2005) From congenital hyperinsulinism to diabetes mellitus: the role of pancreatic beta-cell KATP channels. Pediatr. Diabetes 6, 103 113.
47. Jonas P. Burnashev N. (1995) Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels. Neuron 15, 987 990.
48. Kane G. C., Liu X. K., Yamada S., Olson T. M. Terzic A. (2005) Cardiac KATP channels in health and disease. J. Mol. Cell. Cardiol. 38, 937 943.
49. Kang G., Chepurny O. G., Malester B., Rindler M. J., Rehmann H., Bos J. L., Schwede F., Coetzee W. A. Holz G. G. (2006) cAMP sensor Epac as a determinant of ATP-sensitive potassium channel activity in human pancreatic beta cells and rat INS-1 cells. J. Physiol. 573, 595 609.
50. Khodorov B. (2004) Glutamate-induced deregulation of calcium homeostasis and mitochondrial dysfunction in mammalian central neurones. Prog. Biophys. Mol. Biol. 86, 279 351.
51. 2+ is dependent on mitochondrial-generated reactive oxygen species. FEBS Lett. 378, 150 152.
52. Kowaltowski A. J., Netto L. E. Vercesi A. E. (1998) The thiol-specific antioxidant enzyme prevents mitochondrial permeability transition. Evidence for the participation of reactive oxygen species in this mechanism. J. Biol. Chem. 273, 12766 12769.
53. Lawson K. McKay N. G. (2006) Modulation of potassium channels as a therapeutic approach. Curr. Pharm. Des. 12, 459 470.
54. Lerma J. (2006) Kainate receptor physiology. Curr. Opin. Pharmacol. 6, 89 97.
55. Lindholm D., Eriksson O. Korhonen L. (2004) Mitochondrial proteins in neuronal degeneration. Biochem. Biophys. Res. Commun. 321, 753 758.
56. Liu D., Lu C., Wan R., Auyeung W. W. Mattson M. P. (2002) 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. 22, 431 443.
57. Liu S., Lau L., Wei J., Zhu D., Zou S., Sun H. S., Fu Y., Liu F. Lu Y. (2004) Expression of Ca(2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43, 43 55.
58. Matsumoto N., Komiyama S. Akaike N. (2002) Pre- and postsynaptic ATP-sensitive potassium channels during metabolic inhibition of rat hippocampal CA1 neurons. J. Physiol. 541, 511 520.
59. Matsuo M., Kimura Y. Ueda K. (2005) KATP channel interaction with adenine nucleotides. J. Mol. Cell. Cardiol. 38, 907 916.
60. Meldrum B. S. (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J. Nutr. 130, 1007S 1015S.
61. 2+. Biophys. J. 88, 2234 2249.
62. Miki T. Seino S. (2005) Roles of KATP channels as metabolic sensors in acute metabolic changes. J. Mol. Cell. Cardiol. 38, 917 925.
63. Miki T., Nagashima K., Tashiro F., Kotake K., Yoshitomi H., Tamamoto A., Gonoi T., Iwanaga T., Miyazaki J. Seino S. (1998) Defective insulin secretion and enhanced insulin action in KATP channel-deficient mice. Proc. Natl Acad. Sci. USA 95, 10402 10406.
64. + channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat. Neurosci. 4, 507 512.
65. + channels as metabolic sensors: studies of Kir6.x null mice. Diabetes 53 (Suppl. 3 S176 S180.
66. Moldrich R. X. Beart P. M. (2003) Emerging signalling and protein interactions mediated via metabotropic glutamate receptors. Curr. Drug Targets CNS Neurol. Disord. 2, 109 122.
67. Moldrich R. X., Chapman A. G., De S. G. Meldrum B. S. (2003) Glutamate metabotropic receptors as targets for drug therapy in epilepsy. Eur. J. Pharmacol. 476, 3 16.
68. Moreau C., Prost A. L., Derand R. Vivaudou M. (2005) SUR, ABC proteins targeted by KATP channel openers. J. Mol. Cell. Cardiol. 38, 951 963.
69. Mulle C., Sailer A., Perez-Otano I. et al. (1998) Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392, 601 605.
70. Murphy K. P. Greenfield S. A. (1992) Neuronal selectivity of ATP-sensitive potassium channels in guinea-pig substantia nigra revealed by responses to anoxia. J. Physiol. 453, 167 183.
71. Neagoe I. Schwappach B. (2005) Pas de deux in groups of four - the biogenesis of KATP channels. J. Mol. Cell. Cardiol. 38, 887 894.
72. Nestorowicz A., Glaser B., Wilson B. A., Shyng S. L., Nichols C. G., Stanley C. A., Thornton P. S. Permutt M. A. (1998) Genetic heterogeneity in familial hyperinsulinism. Hum. Mol. Genet. 7, 1119 1128.
73. Nicholls D. G. (2004) Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr. Mol. Med. 4, 149 177.
74. Nicholls D. Attwell D. (1990) The release and uptake of excitatory amino acids. Trends Pharmacol. Sci. 11, 462 468.
75. Nicholls D. G. Budd S. L. (2000) Mitochondria and neuronal survival. Physiol. Rev. 80, 315 360.
76. Nichols C. G. (2006) KATP channels as molecular sensors of cellular metabolism. Nature 440, 470 476.
77. Nicoletti F., Bruno V., Copani A., Casabona G. Knopfel T. (1996) Metabotropic glutamate receptors: a new target for the therapy of neurodegenerative disorders? Trends Neurosci. 19, 267 271.
78. Nieoullon A., Canolle B., Masmejean F., Guillet B., Pisano P. Lortet S. (2006) The neuronal excitatory amino acid transporter EAAC1/EAAT3: does it represent a major actor at the brain excitatory synapse? J. Neurochem. 98, 1007 1018.
79. Niswender C. M., Jones C. K. Conn P. J. (2005) New therapeutic frontiers for metabotropic glutamate receptors. Curr. Top. Med. Chem. 5, 847 857.
80. Oldenburg O., Cohen M. V. Downey J. M. (2003) Mitochondrial K(ATP) channels in preconditioning. J. Mol. Cell. Cardiol. 35, 569 575.
81. Ozaki N., Shibasaki T., Kashima Y. et al. (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat. Cell Biol. 2, 805 811.
82. Partridge C. J., Beech D. J. Sivaprasadarao A. (2001) Identification and pharmacological correction of a membrane trafficking defect associated with a mutation in the sulfonylurea receptor causing familial hyperinsulinism. J. Biol. Chem. 276, 35947 35952.
83. Pellegrini-Giampietro D. E., Zukin R. S., Bennett M. V., Cho S. Pulsinelli W. A. (1992) Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats. Proc. Natl Acad. Sci. USA 89, 10499 10503.
84. Peng P. L., Zhong X., Tu W., Soundarapandian M. M., Molner P., Zhu D., Lau L., Liu S., Liu F. Lu Y. (2006) ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 49, 719 733.
85. Perez-Otano I. Ehlers M. D. (2004) Learning from NMDA receptor trafficking: clues to the development and maturation of glutamatergic synapses. Neurosignals 13, 175 189.
86. Plamondon H., Blondeau N., Heurteaux C. Lazdunski M. (1999) Mutually protective actions of kainic acid epileptic preconditioning and sublethal global ischemia on hippocampal neuronal death: involvement of adenosine A1 receptors and K(ATP) channels. J. Cereb. Blood Flow Metab. 19, 1296 1308.
87. Sagen J. V., Raeder H., Hathout E. et al. (2004) Permanent neonatal diabetes due to mutations in KCNJ11 encoding Kir6.2: patient characteristics and initial response to sulfonylurea therapy. Diabetes 53, 2713 2718.
88. Schousboe A. Waagepetersen H. S. (2005) Role of astrocytes in glutamate homeostasis: implications for excitotoxicity. Neurotox. Res. 8, 221 225.
89. + channel with an ABC transporter. Neuron 26, 155 167.
90. Seharaseyon J., Ohler A., Sasaki N., Fraser H., Sato T., Johns D. C., O'Rourke B. Marban E. (2000) Molecular composition of mitochondrial ATP-sensitive potassium channels probed by viral Kir gene transfer. J. Mol. Cell. Cardiol. 32, 1923 1930.
91. Seino S. (1999) ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies. Annu. Rev. Physiol. 61, 337 362.
92. Seino S. Shibasaki T. (2005) PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol. Rev. 85, 1303 1342.
93. Sheng M. Kim M. J. (2002) Postsynaptic signaling and plasticity mechanisms. Science 298, 776 780.
94. 2+ channel in insulin granule exocytosis. J. Biol. Chem. 279, 7956 7961.
95. 2+ signals in insulin granule exocytosis. Diabetes 53 (Suppl. 3 S59 S62.
96. Shimizu K., Lacza Z., Rajapakse N., Horiguchi T., Snipes J. Busija D. W. (2002) MitoK(ATP) opener, diazoxide, reduces neuronal damage after middle cerebral artery occlusion in the rat. Am. J. Physiol Heart Circ. Physiol. 283, H1005 H1011.
97. Shyng S. L. Nichols C. G. (1998) Membrane phospholipid control of nucleotide sensitivity of KATP channels. Science 282, 1138 1141.
98. Shyng S. L., Ferrigni T., Shepard J. B., Nestorowicz A., Glaser B., Permutt M. A. Nichols C. G. (1998) Functional analyses of novel mutations in the sulfonylurea receptor 1 associated with persistent hyperinsulinemic hypoglycemia of infancy. Diabetes 47, 1145 1151.
99. Soundarapandian M. M., Tu W. H., Peng P. L., Zervos A. S. Lu Y. (2005) AMPA receptor subunit GluR2 gates injurious signals in ischemic stroke. Mol. Neurobiol. 32, 145 155.
100. Soundarapandian M. M., Wu D., Zhong X., Petralia R. S., Peng L., Tu W. Lu Y. (2007) Expression of functional Kir6.1 channels regulates glutamate release at CA3 synapses in generation of epileptic form of seizures. J. Neurochem. Epub ahead of print: doi:.
101. Starkov A. A., Chinopoulos C. Fiskum G. (2004) Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36, 257 264.
102. Steiner A. L., Ferrendelli J. A. Kipnis D. M. (1972) Radioimmunoassay for cyclic nucleotides. 3. Effect of ischemia, changes during development and regional distribution of adenosine 3′,5′-monophosphate and guanosine 3′,5′-monophosphate in mouse brain. J. Biol. Chem. 247, 1121 1124.
103. Steinlein O. K. Noebels J. L. (2000) Ion channels and epilepsy in man and mouse. Curr. Opin. Genet. Dev. 10, 286 291.
104. Sucher N. J., Awobuluyi M., Choi Y. B. Lipton S. A. (1996) NMDA receptors: from genes to channels. Trends Pharmacol. Sci. 17, 348 355.
105. + channels. J. Neurophysiol. 95, 2590 2601.
106. Taschenberger G., Mougey A., Shen S., Lester L. B., LaFranchi S. Shyng S. L. (2002) Identification of a familial hyperinsulinism-causing mutation in the sulfonylurea receptor 1 that prevents normal trafficking and function of KATP channels. J. Biol. Chem. 277, 17139 17146.
107. Wang L., Cherednichenko G., Hernandez L., Halow J., Camacho S. A., Figueredo V. Schaefer S. (2001) Preconditioning limits mitochondrial Ca(2+) during ischemia in rat hearts: role of K(ATP) channels. Am. J. Physiol Heart Circ. Physiol. 280, H2321 H2328.
108. Wang Q., Yu S., Simonyi A., Sun G. Y. Sun A. Y. (2005) Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol. Neurobiol. 31, 3 16.
109. Watkins J. C. Jane D. E. (2006) The glutamate story. Br. J. Pharmacol. 147 (Suppl. 1 S100 S108.
110. White R. J. Reynolds I. J. (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 16, 5688 5697.
111. Won S. J., Kim D. Y. Gwag B. J. (2002) Cellular and molecular pathways of ischemic neuronal death. J. Biochem. Mol. Biol. 35, 67 86.
112. Yamada K. Inagaki N. (2005) Neuroprotection by KATP channels. J. Mol. Cell. Cardiol. 38, 945 949.
113. Yamada K., Ji J. J., Yuan H., Miki T., Sato S., Horimoto N., Shimizu T., Seino S. Inagaki N. (2001) Protective role of ATP-sensitive potassium channels in hypoxia-induced generalized seizure. Science 292, 1543 1546.
114. + channels: implication for dimerization of nucleotide-binding domains to induce channel opening. Mol. Pharmacol. 66, 807 816.
115. Yi J. H. Hazell A. S. (2006) Excitotoxic mechanisms and the role of astrocytic glutamate transporters in traumatic brain injury. Neurochem. Int. 48, 394 403.