From the Section of Molecular and Cellular Cardiology, Department of
Medicine, Johns Hopkins University, Baltimore, Md. Yongge Liu is now at
Maryland Research Laboratories, Otsuka America Pharmaceutical Inc, Rockville,
Md.
Correspondence to Eduardo Marban, MD, PhD, Section of Molecular and Cellular Cardiology, Department of Medicine, Johns Hopkins University, Ross 844, 720 Rutland Ave, Baltimore, MD 21205. E-mail marban{at}welchlink.welch.jhu.edu
Background—Brief interruptions
of coronary blood flow paradoxically protect the heart from
subsequent prolonged ischemia. The basis of such
endogenous cardioprotection, known as "ischemic
preconditioning," remains uncertain. Pharmacological evidence has
implicated ATP-dependent potassium (KATP) channels in the
mechanism of preconditioning; however, the effects of sarcolemmal
KATP channels on excitability cannot account for the
protection.
Methods and Results—We simultaneously measured
flavoprotein fluorescence, an index of mitochondrial redox
state, and sarcolemmal KATP currents in intact rabbit
ventricular myocytes. Our results show that diazoxide, a
KATP channel opener, selectively activates
mitochondrial KATP channels. Diazoxide induced reversible
oxidation of flavoproteins with an EC50 of 27 µmol/L
but did not activate sarcolemmal KATP channels. The
subcellular site of diazoxide action is further localized to
mitochondria by confocal imaging of fluorescence arising from
flavoproteins and tetramethylrhodamine ethyl ester. In a cellular model
of simulated ischemia, inclusion of diazoxide decreased the
rate of cell death to about half of that in controls. Both the redox
changes and protection are inhibited by the KATP channel
blocker 5-hydroxydecanoic acid.
Conclusions—Our results demonstrate that diazoxide targets
mitochondrial but not sarcolemmal KATP channels and imply
that mitochondrial KATP channels may mediate the protection
from KATP channel openers.
© 1998 American Heart Association, Inc.
Basic Science Reports
Mitochondrial ATP-Dependent Potassium Channels
Novel Effectors of Cardioprotection?
Key Words: ischemia • potassium channels • mitochondria
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G. C Rodrigo, N. W Davies, and N. B Standen Diazoxide causes early activation of cardiac sarcolemmal KATP channels during metabolic inhibition by an indirect mechanism Cardiovasc Res, February 15, 2004; 61(3): 570 - 579. [Abstract] [Full Text] [PDF]
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 M. R. Duchen Roles of Mitochondria in Health and Disease Diabetes, February 1, 2004; 53(90001): S96 - 102. [Abstract] [Full Text]
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E. Murphy Primary and Secondary Signaling Pathways in Early Preconditioning That Converge on the Mitochondria to Produce Cardioprotection Circ. Res., January 9, 2004; 94(1): 7 - 16. [Abstract] [Full Text] [PDF]
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 T. Zhang, S. Miyamoto, and J. H. Brown Cardiomyocyte Calcium and Calcium/Calmodulin-dependent Protein Kinase II: Friends or Foes? Recent Prog. Horm. Res., January 1, 2004; 59(1): 141 - 168. [Abstract] [Full Text]
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M. A. Deja, K. S. Golba, M. Kolowca, K. Widenka, J. Biernat, and S. Wos Diazoxide provides protection to human myocardium in vitro that is concentration dependent Ann. Thorac. Surg., January 1, 2004; 77(1): 226 - 232. [Abstract] [Full Text] [PDF]
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T. Sato, T. Takizawa, T. Saito, S. Kobayashi, Y. Hara, and H. Nakaya Amiodarone Inhibits Sarcolemmal but Not Mitochondrial KATP Channels in Guinea Pig Ventricular Cells J. Pharmacol. Exp. Ther., December 1, 2003; 307(3): 955 - 960. [Abstract] [Full Text] [PDF]
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Y. Teshima, M. Akao, S. P. Jones, and E. Marban Cariporide (HOE642), a Selective Na+-H+ Exchange Inhibitor, Inhibits the Mitochondrial Death Pathway Circulation, November 4, 2003; 108(18): 2275 - 2281. [Abstract] [Full Text] [PDF]
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J. P. Headrick, B. Hack, and K. J. Ashton Acute adenosinergic cardioprotection in ischemic-reperfused hearts Am J Physiol Heart Circ Physiol, November 1, 2003; 285(5): H1797 - H1818. [Abstract] [Full Text] [PDF]
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W. de Ruijter, R. J.P. Musters, C. Boer, G. J. M. Stienen, W. S. Simonides, and J. J. de Lange The Cardioprotective Effect of Sevoflurane Depends on Protein Kinase C Activation, Opening of Mitochondrial K+ATP Channels, and the Production of Reactive Oxygen Species Anesth. Analg., November 1, 2003; 97(5): 1370 - 1376. [Abstract] [Full Text] [PDF]
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 D. M. YELLON and J. M. DOWNEY Preconditioning the Myocardium: From Cellular Physiology to Clinical Cardiology Physiol Rev, October 1, 2003; 83(4): 1113 - 1151. [Abstract] [Full Text] [PDF]
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Y. Nakae, S. Kohro, Q. H. Hogan, and Z. J. Bosnjak Intracellular Mechanism of Mitochondrial Adenosine Triphosphate-Sensitive Potassium Channel Activation with Isoflurane Anesth. Analg., October 1, 2003; 97(4): 1025 - 1032. [Abstract] [Full Text] [PDF]
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J. Zhang, A. H. L. From, K. Ugurbil, and R. J. Bache Myocardial oxygenation and high-energy phosphate levels during KATP channel blockade Am J Physiol Heart Circ Physiol, October 1, 2003; 285(4): H1420 - H1427. [Abstract] [Full Text] [PDF]
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W. K. Laskey and D. Beach Frequency and clinical significance of ischemic preconditioning during percutaneous coronary intervention J. Am. Coll. Cardiol., September 17, 2003; 42(6): 998 - 1003. [Abstract] [Full Text] [PDF]
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D. J. Duncker, P. D. Verdouw, M. Suzuki, T. Saito, T. Sato, M. Tamagawa, T. Miki, S. Seino, and H. Nakaya Cardioprotective Effect of Diazoxide Is Mediated by Activation of Sarcolemmal but not Mitochondrial ATP-Sensitive Potassium Channels in Mice * Response Circulation, August 12, 2003; 108 (6): e44 - e44. [Full Text] [PDF]
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Y. Teshima, M. Akao, S. P. Jones, and E. Marban Uncoupling Protein-2 Overexpression Inhibits Mitochondrial Death Pathway in Cardiomyocytes Circ. Res., August 8, 2003; 93(3): 192 - 200. [Abstract] [Full Text] [PDF]
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Z. Cao, L. Liu, and D. M. Van Winkle Activation of {delta}- and {kappa}-opioid receptors by opioid peptides protects cardiomyocytes via KATP channels Am J Physiol Heart Circ Physiol, August 7, 2003; 285(3): H1032 - H1039. [Abstract] [Full Text] [PDF]
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 Y. Teshima, M. Akao, R. A. Li, T. H. Chong, W. A. Baumgartner, M. V. Johnston, and E. Marban Mitochondrial ATP-Sensitive Potassium Channel Activation Protects Cerebellar Granule Neurons From Apoptosis Induced by Oxidative Stress Stroke, July 1, 2003; 34(7): 1796 - 1802. [Abstract] [Full Text] [PDF]
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J. Minners, C. J. McLeod, and M. N. Sack Mitochondrial plasticity in classical ischemic preconditioning--moving beyond the mitochondrial KATP channel Cardiovasc Res, July 1, 2003; 59(1): 1 - 6. [Abstract] [Full Text] [PDF]
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J. P Headrick, L. Willems, K. J Ashton, K. Holmgren, J. Peart, and G P. Matherne Ischaemic tolerance in aged mouse myocardium: the role of adenosine and effects of A1 adenosine receptor overexpression J. Physiol., June 15, 2003; 549(3): 823 - 833. [Abstract] [Full Text] [PDF]
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 E. o. Cosar and C. J. O'Connor Hibernation, Stunning, and Preconditioning: Historical Perspective, Current Concepts, Clinical Applications, and Future Implications Seminars in Cardiothoracic and Vascular Anesthesia, June 1, 2003; 7(2): 115 - 140. [Abstract] [PDF]
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M. Ichinose, H. Yonemochi, T. Sato, and T. Saikawa Diazoxide triggers cardioprotection against apoptosis induced by oxidative stress Am J Physiol Heart Circ Physiol, June 1, 2003; 284(6): H2235 - H2241. [Abstract] [Full Text] [PDF]
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J. Peart and J. P Headrick Adenosine-mediated early preconditioning in mouse: protective signaling and concentration dependent effects Cardiovasc Res, June 1, 2003; 58(3): 589 - 601. [Abstract] [Full Text] [PDF]
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 T. Steensrud, D. Nordhaug, O.P. Elvenes, C. Korvald, and D.G. Sorlie Superior myocardial protection with nicorandil cardioplegia Eur. J. Cardiothorac. Surg., May 1, 2003; 23(5): 670 - 677. [Abstract] [Full Text] [PDF]
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L. Wei, S. P. Yu, F. Gottron, B. J. Snider, G. J. Zipfel, and D. W. Choi Potassium Channel Blockers Attenuate Hypoxia- and Ischemia-Induced Neuronal Death In Vitro and In Vivo Stroke, May 1, 2003; 34(5): 1281 - 1286. [Abstract] [Full Text] [PDF]
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Y. Nakae, W.-M. Kwok, Z. J. Bosnjak, and M. T. Jiang Isoflurane activates rat mitochondrial ATP-sensitive K+ channels reconstituted in lipid bilayers Am J Physiol Heart Circ Physiol, May 1, 2003; 284(5): H1865 - H1871. [Abstract] [Full Text] [PDF]
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 S. B. Digerness, P. S. Brookes, S. P. Goldberg, C. R. Katholi, and W. L. Holman Modulation of mitochondrial adenosine triphosphate-sensitive potassium channels and sodium-hydrogen exchange provide additive protection from severe ischemia-reperfusion injury J. Thorac. Cardiovasc. Surg., April 1, 2003; 125(4): 863 - 871. [Abstract] [Full Text] [PDF]
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P. P. Dzeja, P. Bast, C. Ozcan, A. Valverde, E. L. Holmuhamedov, D. G. L. Van Wylen, and A. Terzic Targeting nucleotide-requiring enzymes: implications for diazoxide-induced cardioprotection Am J Physiol Heart Circ Physiol, April 1, 2003; 284(4): H1048 - H1056. [Abstract] [Full Text] [PDF]
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M. Das, J. E Parker, and A. P Halestrap Matrix volume measurements challenge the existence of diazoxide/glibencamide-sensitive KATP channels in rat mitochondria J. Physiol., March 15, 2003; 547(3): 893 - 902. [Abstract] [Full Text] [PDF]
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