Diazoxide preconditioning protects against neuronal cell death by attenuation of oxidative stress upon glutamate stimulation

Journal of Neuroscience Research

Volumn 76, Issue 5, 2004, Pages 697-704

  Nagy, Krisztina ^a,b   Kis, Bela ^a   Rajapakse, Nishadi C ^a   Bari, Ferenc ^a,b   Busija, David W ^a  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^b UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Diazoxide; Glutamate; mitoKATP channels; Neuron; Preconditioning

Indexed keywords

5 HYDROXYDECANOIC ACID; ADENOSINE TRIPHOSPHATE; DIAZOXIDE; GLUTAMIC ACID; M 40401; NICORANDIL; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; EMBRYO; FETUS; NERVE CELL; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CARRIER PROTEINS; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DIAZOXIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EMBRYO; FEMALE; GLUTAMIC ACID; MALE; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PEROXIDASES; PREGNANCY; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUPEROXIDES; TIME FACTORS;

EID: 2542483507     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20120     Document Type: Article

References (58)

1. Bajgar R, Seetharaman S, Kowaltowski AJ, Garlid KD, Paucek P. 2001. Identification and properties of a novel intracellular (mitochondrial) ATP-sensitive potassium channel in brain. J Biol Chem 276:33369-33374.
2. Bindokas VP, Jordan J, Lee CC, Miller PJ. 1996. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J Neurosci 16:1324-1336.
3. Blondeau N, Plamondon H, Richelme C, Heurteaux C, Lazdunski M. 2000. K(ATP) channel openers, adenosine agonists and epileptic preconditioning are stress signals inducing hippocampal neuroprotection. Neuroscience 100:465-474.
4. Bryk R, Griffin P, Nathan C. 2000. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211-215.
5. Caparrelli DJ, Cattaneo SM, 2nd, Bethea BT, Shake JG, Eberhart C, Blue ME, Marban E, Johnston MV, Baumgartner WA, Gott VL. 2002. Pharmacological preconditioning ameliorates neurological injury in a model of spinal cord ischemia. Ann Thorac Surg 74:838-844.
6. Carriedo SG, Sensi SL, Yin HZ, Weiss JH. 2000. AMPA exposures induce mitochondrial Ca(2+) overload and ROS generation in spinal motor neurons in vitro. J Neurosci 20:240-250.
7. Carroll R, Gant VA, Yellon DM. 2001. Mitochondrial K(ATP) channel opening protects a human atrial-derived cell line by a mechanism involving free radical generation. Cardiovasc Res 51:691-700.
8. Cuzzocrea S, Mazzon E, Dugo L, Caputi AP, Aston K, Riley DP, Salvemini D. 2001. Protective effects of a new stable, highly active SOD mimetic, M40401 in splanchnic artery occlusion and reperfusion. Br J Pharmacol 132:19-29.
9. Debska G, May R, Kicinska A, Szewczyk A, Elger CE, Kunz WS. 2001. Potassium channel openers depolarize hippocampal mitochondria. Brain Res 892:42-50.
10. D'Hahan N, Moreau C, Prost AL, Jacquet H, Alekseev AE, Terzic A, Vivaudou M. 1999. Pharmacological plasticity of cardiac ATP-sensitive potassium channels toward diazoxide revealed by ADP. Proc Natl Acad Sci USA 96:12162-12167.
11. Domoki F, Perciaccante JV, Veltkamp R, Bari F, Busija DW. 1999. Mitochondrial potassium channel opener diazoxide preserves neuronal-vascular function after cerebral ischemia in newborn pigs. Stroke 30:2713-2718.
12. Dzeja PP, Bast P, Ozcan C, Valverde A, Holmuhamedov EL, Van Wylen DG, Terzic A. 2003. Targeting nucleotide-requiring enzymes: implications for diazoxide-induced cardioprotection. Am J Physiol Heart Circ Physiol 284:1048-1056.
13. Forbes RA, Steenbergen C, Murphy E. 2001. Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res 88:802-809.
14. Garcia de Arriba S, Franke H, Pissarek M, Nieber K, Illes P. 1999. Neuroprotection by ATP-dependent potassium channels in rat neocortical brain slices during hypoxia. Neurosci Lett 273:13-16.
15. Garlid KD. 1996. Cation transport in mitochondria - the potassium cycle. Biochim Biophys Acta 1275:123-126.
16. Garlid KD, Dos Santos P, Xie ZJ, Costa AD, Paucek P. 2003. Mitochondrial potassium transport: the role of the mitochondrial ATP-sensitive K(+) channel in cardiac function and cardioprotection. Biochim Biophys Acta 1606:1-21.
17. Garlid KD, Paucek P, Yarov-Yarovoy V, Murray HN, Darbenzio RB, D'Alonzo AJ, Lodge NJ, Smith MA, Grover GJ. 1997. Cardioprotective effect of diazoxide and its interaction with mitochondrial ATP-sensitive K+ channels. Possible mechanism of cardioprotection. Circ Res 81:1072-1082.
18. Hanley PJ, Gopalan KV, Lareau RA, Srivastava DK, von Meltzer M, Daut J. 2003. Beta-oxidation of 5-hydroxydecanoate, a putative blocker of mitochondrial ATP-sensitive potassium channels. J Physiol 547:387-393.
19. Hanley PJ, Mickel M, Loffler M, Brandt U, Daut J. 2002. K(ATP) channel-independent targets of diazoxide and 5-hydroxydecanoate in the heart. J Physiol 542:735-741.
20. Hattori F, Murayama N, Noshita T, Oikawa S. 2003. Mitochondrial peroxiredoxin-3 protects hippocampal neurons from excitotoxic injury in vivo. J Neurochem 86:860-868.
21. Horiguchi T, Kis B, Rajapakse N, Shimizu K, Busija DW. 2003. Opening of mitochondrial ATP-sensitive potassium channels is a trigger of 3-nitropropionic acid-induced tolerance to transient focal cerebral ischemia in rats. Stroke 34:1015-1020.
22. Kim-Han JS, Reichert SA, Quick KL, Dugan LL. 2001. BMCP1: a mitochondrial uncoupling protein in neurons which regulates mitochondrial function and oxidant production. J Neurochem 79:658-668.
23. Kis B, Nagy K, Snipes JA, Rajapakse NC, Horiguchi T, Grover GJ, Busija DW. 2004. The mitochondrial KATP channel opener BMS-191095 induces neuronal preconditioning. Neuroreport 15:345-349.
24. Kis B, Rajapakse NC, Snipes JA, Nagy K, Horiguchi T, Busija DW. 2003. Diazoxide induces delayed pre-conditioning in cultured rat cortical neurons. J Neurochem 87:969-980.
25. Kitagawa K, Matsumoto M, Tagaya M, Hata R, Ueda H, Niinobe M, Handa N, Fukunaga K, Kimura K, Mikoshiba K, et al. 1990. "Ischemic tolerance" phenomenon found in the brain. Brain Res 528:21-24.
26. Lacza Z, Snipes JA, Kis B, Szabo C, Grover G, Busija DW. 2003. Investigation of the subunit composition and the pharmacology of the mitochondrial ATP-dependent K(+) channel in the brain. Brain Res 994:27-36.
27. Lauritzen I, De Weille JK, Lazdunski M. 1997. The potassium channel opener (-)-cromakalim prevents glutamate-induced cell death in hippocampal neurons. J Neurochem 69:1570-1579.
28. Laybutt DR, Sharma A, Sgroi DC, Gaudet J, Bonner-Weir S, Weir GC. 2002. Genetic regulation of metabolic pathways in beta-cells disrupted by hyperglycemia. J Biol Chem 277:10912-10921.
29. Lim KH, Javadov SA, Das M, Clarke SJ, Suleiman MS, Halestrap AP. 2002. The effects of ischaemic preconditioning, diazoxide and 5-hydroxydecanoate on rat heart mitochondrial volume and respiration. J Physiol 545:961-974.
30. Liu D, Lu C, Wan K, Auyeung WW, Mattson MP. 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.
31. Marban E. 2002. The surprising role of vascular K(ATP) channels in vasospastic angina. J Clin Invest 110:153-154.
32. Mattson MP, Liu D. 2003. Mitochondrial potassium channels and uncoupling proteins in synaptic plasticity and neuronal cell death. Biochem Biophys Res Commun 304:539-549.
33. Mattson MP, Zhang Y, Bose S. 1993. Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp Neurol 121:1-13.
34. Murry CE, Jennings RB, Reimer KA. 1986. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124-1136.
35. Nakagaxva I, Nakase H, Aketa S, Kamada Y, Yamashita M, Sakaki T. 2002. ATP-dependent potassium channel mediates neuroprotection by chemical preconditioning with 3-nitropropionic acid in gerbil hippocampus. Neurosci Lett 320:33-36.
36. Ockaili RA, Bhargava P, Kukreja RC. 2001. Chemical preconditioning with 3-nitropropionic acid in hearts: role of mitochondrial K(ATP) channel. Am J Physiol Heart Circ Physiol 280:2406-2411.
37. Oldenburg O, Cohen MV, Yellon DM, Downey JM. 2002. Mitochondrial K(ATP) channels: role in cardioprotection. Cardiovasc Res 55:429-437.
38. Ovide-Bordeaux S, Ventura-Clapier R, Veksler V. 2000. Do modulators of the mitochondrial K(ATP) channel change the function of mitochondria in situ? J Biol Chem 275:37291-37295.
39. Ozcan C, Bienengraeber M, Dzeja PP, Terzic A. 2002. Potassium channel openers protect cardiac mitochondria by attenuating oxidant stress at reoxygenation. Am J Physiol Heart Circ Physiol 282:531-539.
40. Pain T, Yang XM, Critz SD, Yue Y, Nakano A, Liu GS, Heusch G, Cohen MV, Downey JM. 2000. Opening of mitochondrial K(ATP) channels triggers the preconditioned state by generating free radicals. Circ Res 87:460-466.
41. Rajapakse N, Kis B, Horiguchi T, Snipes J, Busija D. 2003. Diazoxide pretreatment induces delayed preconditioning in astrocytes against oxygen glucose deprivation and hydrogen peroxide-induced toxicity. J Neurosci Res 73:206-214.
42. Rajapakse N, Shimizu K, Kis B, Snipes J, Lacza Z, Busija D. 2002. Activation of mitochondrial ATP-sensitive potassium channels prevents neuronal cell death after ischemia in neonatal rats. Neurosci Lett 327:208-212.
43. Ravati A, Ahlemeyer B, Becker A, Klumpp S, Krieglstein J. 2001. Preconditioning-induced neuroprotection is mediated by reactive oxygen species and activation of the transcription factor nuclear factor-kappaB. J Neurochem 78:909-919.
44. Ravati A, Ahlemeyer B, Becker A, Krieglstein J. 2000. Preconditioning-induced neuroprotection is mediated by reactive oxygen species. Brain Res 866:23-32.
45. Reshef A, Sperling O, Zoref-Shani E. 1998. Opening of ATP-sensitive potassium channels by cromakalim confers tolerance against chemical ischemia in rat neuronal cultures. Neurosci Lett 250:111-114.
46. Salvemini D, Wang ZQ, Zwejer JL, Samouilov A, Macarthur H, Misko TP, Currie MG, Cuzzocrea S, Sikorski JA, Riley DP. 1999. A nonpeptidyl mimic of superoxide dismutase with therapeutic activity in rats. Science 286:304-306.
47. Sato T, Sasaki N, O'Rourke B, Marban E. 2000. Nicorandil, a potent cardioprotective agent, acts by opening mitochondrial ATP-dependent potassium channels. J Am Coll Cardiol 35:514-518.
48. Schafer G, Portenhauser R, Trolp R. 1971. Inhibition of mitochondrial metabolism by the diabetogenic thiadiazine diazoxide. I. Action on succinate dehydrogenase and TCA-cycle oxidations. Biochem Pharmacol 20:1271-1280.
49. Schafer G, Wegener C, Portenhauser R, Bojanovski D. 1969. Diazoxide, an inhibitor of succinate oxidation. Biochem Pharmacol 18:2678-2681.
50. Shake JG, Peck EA, Marban E, Gott VL, Johnston MV, Troncoso JC, Redmond JM, Baumgartner WA. 2001. Pharmacologically induced preconditioning with diazoxide: a novel approach to brain protection. Ann Thorac Surg 72:1849-1854.
51. Shimizu K, Lacza Z, Rajapakse N, Horiguchi T, Snipes J, Busija DW. 2002. MitoK(ATP) opener, diazoxide, reduces neuronal damage after middle cerebral artery occlusion in the rat. Am J Physiol Heart Circ Physiol 283:1005-1011.
52. Shimizu K, Rajapakse N, Horiguchi T, Payne RM, Busija DW. 2003. Neuroprotection against hypoxia-ischemia in neonatal rat brain by novel superoxide dismutase mimetics. Neurosci Lett 346:41-44.
53. Skulachev VP. 1998. Uncoupling: new approaches to an old problem of bioenergetics. Biochim Biophys Acta 1363:100-124.
54. Tai KK, McCrossan ZA, Abbott GW. 2003. Activation of mitochondrial ATP-sensitive potassium channels increases cell viability against rotenone-induced cell death. J Neurochem 84:1193-1200.
55. Terzic A, Dzeja PP, Holmuhamedov EL. 2000. Mitochondrial K(ATP) channels: probing molecular identity and pharmacology. J Mol Cell Cardiol 32:1911-1915.
56. Teshima Y, Akao M, Li RA, Chong TH, Baumgartner WA, Johnston MV, Marban E. 2003. Mitochondrial ATP-sensitive potassium channel activation protects cerebellar granule neurons from apoptosis induced by oxidative stress. Stroke 34:1796-1802.
57. Wiegand F, Liao W, Busch C, Castell S, Knapp F, Lindauer U, Megow D, Meisel A, Redetzky A, Ruscher K, Trendelenburg G, Victorov I, Riepe M, Diener HC, Dirnagl U. 1999. Respiratory chain inhibition induces tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 19:1229-1237.
58. Yamauchi T, Kashii S, Yasuyoshi H, Zhang S, Honda Y, Akaike A. 2003. Mitochondrial ATP-sensitive potassium channel: a novel site for neuroprotection. Invest Ophthalmol Vis Sci 44:2750-2756.