Circulation Research. 2001;88:802-809
Published online before print April 13, 2001, doi: 10.1161/hh0801.089342
Published online before print April 13, 2001, doi: 10.1161/hh0801.089342
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© 2001 American Heart Association, Inc.
Cellular Biology |
Diazoxide-Induced Cardioprotection Requires Signaling Through a Redox-Sensitive Mechanism
From the Laboratory of Signal Transduction (R.A.F., E.M.), National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, NC, and the Department of Pathology, Duke University Medical Center (C.S.), Durham, NC.
Correspondence to Elizabeth Murphy, PhD, NIEHS, National Institutes of Health, Laboratory of Signal Transduction, MD 2-03, 111 T.W. Alexander Dr, Research Triangle Park, NC 27709. E-mail murphy1{at}niehs.nih.gov
Abstract—Diazoxide, a selective opener of the mitochondrial ATP-sensitive potassium channel, has been shown to elicit tolerance to ischemia in cardiac myocytes and in perfused heart. However, the mechanism of this cardioprotection is poorly understood. Because reactive oxygen species (ROS) are recognized as important intracellular signaling molecules and have been implicated in ischemic preconditioning, we examined diazoxide-induced ROS production in adult cardiomyocytes. Cells treated with 50 µmol/L diazoxide showed a 173% increase in ROS production relative to baseline. 5-Hydroxydecanoate was found to attenuate the diazoxide-induced increase in ROS generation. The diazoxide-induced increase in ROS also was abrogated by the addition of either the antioxidant N-acetylcysteine (NAC) or N-mercaptopropionylglycine. We also examined the ability of NAC to block the protective effects of diazoxide in the perfused rat heart. After 20 minutes of global ischemia and 20 minutes of reflow, hearts perfused with 100 µmol/L diazoxide before ischemia showed significantly improved postischemic contractile function relative to untreated hearts (84% versus 29% of initial left ventricular developed pressure, respectively). Hearts treated with diazoxide in the presence of 4 mmol/L NAC recovered 53% of initial left ventricular developed pressure, whereas hearts treated with NAC alone recovered 46% of preischemic function. Using 31P NMR spectroscopy, we found that, similar to preconditioning, diazoxide significantly attenuated ischemia-induced intracellular acidification and enhanced post- ischemic recovery of phosphocreatine levels, both of which were blocked by cotreatment with NAC. These data suggest that the cardioprotective actions of diazoxide are mediated by generation of a pro-oxidant environment.
Key Words: reactive oxygen species • cardioprotection • intracellular pH • dichlorofluorescin diacetate
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G. Lebuffe, P. T. Schumacker, Z.-H. Shao, T. Anderson, H. Iwase, and T. L. Vanden Hoek ROS and NO trigger early preconditioning: relationship to mitochondrial KATP channel Am J Physiol Heart Circ Physiol, January 1, 2003; 284(1): H299 - H308. [Abstract] [Full Text] [PDF]
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K. H H Lim, S. A Javadov, M. Das, S. J Clarke, M-S. Suleiman, and A. P Halestrap The effects of ischaemic preconditioning, diazoxide and 5-hydroxydecanoate on rat heart mitochondrial volume and respiration J. Physiol., December 15, 2002; 545(3): 961 - 974. [Abstract] [Full Text] [PDF]
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 W. Xu, Y. Liu, S. Wang, T. McDonald, J. E. Van Eyk, A. Sidor, and B. O'Rourke Cytoprotective Role of Ca2+- Activated K+ Channels in the Cardiac Inner Mitochondrial Membrane Science, November 1, 2002; 298(5595): 1029 - 1033. [Abstract] [Full Text] [PDF]
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O. Oldenburg, M. V Cohen, D. M Yellon, and J. M Downey Mitochondrial KATP channels: role in cardioprotection Cardiovasc Res, August 15, 2002; 55(3): 429 - 437. [Abstract] [Full Text] [PDF]
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R. M Smith, S. Lecour, and M. N Sack Innate immunity and cardiac preconditioning: a putative intrinsic cardioprotective program Cardiovasc Res, August 15, 2002; 55(3): 474 - 482. [Abstract] [Full Text] [PDF]
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O. Oldenburg, Q. Qin, A. R Sharma, M. V Cohen, J. M Downey, and J. N Benoit Acetylcholine leads to free radical production dependent on KATP channels, Gi proteins, phosphatidylinositol 3-kinase and tyrosine kinase Cardiovasc Res, August 15, 2002; 55(3): 544 - 552. [Abstract] [Full Text] [PDF]
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R. M Smith, N. Suleman, J. McCarthy, and M. N Sack Classic ischemic but not pharmacologic preconditioning is abrogated following genetic ablation of the TNF{alpha} gene Cardiovasc Res, August 15, 2002; 55(3): 553 - 560. [Abstract] [Full Text] [PDF]
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H. H. Patel, A. K. Hsu, J. N. Peart, and G. J. Gross Sarcolemmal KATP Channel Triggers Opioid-Induced Delayed Cardioprotection in the Rat Circ. Res., August 9, 2002; 91(3): 186 - 188. [Abstract] [Full Text] [PDF]
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P. J Hanley, M. Mickel, M. Loffler, U. Brandt, and J. Daut KATP channel-independent targets of diazoxide and 5-hydroxydecanoate in the heart J. Physiol., August 1, 2002; 542(3): 735 - 741. [Abstract] [Full Text] [PDF]
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L. Samavati, M. M. Monick, S. Sanlioglu, G. R. Buettner, L. W. Oberley, and G. W. Hunninghake Mitochondrial KATP channel openers activate the ERK kinase by an oxidant-dependent mechanism Am J Physiol Cell Physiol, July 1, 2002; 283(1): C273 - C281. [Abstract] [Full Text] [PDF]
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P. Dos Santos, A. J. Kowaltowski, M. N. Laclau, S. Seetharaman, P. Paucek, S. Boudina, J.-B. Thambo, L. Tariosse, and K. D. Garlid Mechanisms by which opening the mitochondrial ATP- sensitive K+ channel protects the ischemic heart Am J Physiol Heart Circ Physiol, July 1, 2002; 283(1): H284 - H295. [Abstract] [Full Text] [PDF]
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Y. Ohnuma, T. Miura, T. Miki, M. Tanno, A. Kuno, A. Tsuchida, and K. Shimamoto Opening of mitochondrial KATP channel occurs downstream of PKC-epsilon activation in the mechanism of preconditioning Am J Physiol Heart Circ Physiol, July 1, 2002; 283(1): H440 - H447. [Abstract] [Full Text] [PDF]
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H. Y. Zhang, B. C. McPherson, H. Liu, T. S. Baman, P. Rock, and Z. Yao H2O2 opens mitochondrial KATP channels and inhibits GABA receptors via protein kinase C-epsilon in cardiomyocytes Am J Physiol Heart Circ Physiol, April 1, 2002; 282(4): H1395 - H1403. [Abstract] [Full Text] [PDF]
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B. Pouzet, J.-B. Lecharny, M. Dehoux, S. Paquin, M. Kitakaze, J. Mantz, and P. Menasche Is there a place for preconditioning during cardiac operations in humans? Ann. Thorac. Surg., March 1, 2002; 73(3): 843 - 848. [Abstract] [Full Text] [PDF]
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P. Korge, H. M. Honda, and J. N. Weiss Protection of cardiac mitochondria by diazoxide and protein kinase C: Implications for ischemic preconditioning PNAS, February 20, 2002; (2002) 52713199. [Abstract] [Full Text] [PDF]
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C. Ozcan, M. Bienengraeber, P. P. Dzeja, and A. Terzic Potassium channel openers protect cardiac mitochondria by attenuating oxidant stress at reoxygenation Am J Physiol Heart Circ Physiol, February 1, 2002; 282(2): H531 - H539. [Abstract] [Full Text] [PDF]
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R. Schulz, M. V Cohen, M. Behrends, J. M Downey, and G. Heusch Signal transduction of ischemic preconditioning Cardiovasc Res, November 1, 2001; 52(2): 181 - 198. [Full Text] [PDF]
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P. P. Dzeja, E. L. Holmuhamedov, C. Ozcan, D. Pucar, A. Jahangir, and A. Terzic Mitochondria: Gateway for Cytoprotection Circ. Res., October 26, 2001; 89(9): 744 - 746. [Full Text] [PDF]
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H. H. Patel and G. J. Gross Diazoxide induced cardioprotection: what comes first, KATP channels or reactive oxygen species? Cardiovasc Res, September 1, 2001; 51(4): 633 - 636. [Full Text] [PDF]
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Y. Yue, M. Krenz, M. V. Cohen, J. M. Downey, and S. D. Critz Menadione mimics the infarct-limiting effect of preconditioning in isolated rat hearts Am J Physiol Heart Circ Physiol, August 1, 2001; 281(2): H590 - H595. [Abstract] [Full Text] [PDF]
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Y. Liu and B. O'Rourke Opening of Mitochondrial KATP Channels Triggers Cardioprotection : Are Reactive Oxygen Species Involved? Circ. Res., April 27, 2001; 88(8): 750 - 752. [Full Text] [PDF]
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R. Bajgar, S. Seetharaman, A. J. Kowaltowski, K. D. Garlid, and P. Paucek Identification and Properties of a Novel Intracellular (Mitochondrial) ATP-sensitive Potassium Channel in Brain J. Biol. Chem., August 31, 2001; 276(36): 33369 - 33374. [Abstract] [Full Text] [PDF]
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D. Pucar, P. P. Dzeja, P. Bast, N. Juranic, S. Macura, and A. Terzic Cellular Energetics in the Preconditioned State. PROTECTIVE ROLE FOR PHOSPHOTRANSFER REACTIONS CAPTURED BY 18O-ASSISTED 31P NMR J. Biol. Chem., November 21, 2001; 276(48): 44812 - 44819. [Abstract] [Full Text] [PDF]
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