Circulation Research. 2004;94:420-432
doi: 10.1161/01.RES.0000117583.66950.43
doi: 10.1161/01.RES.0000117583.66950.43
© 2004 American Heart Association, Inc.
Reviews |
Evidence for Mitochondrial K+ Channels and Their Role in Cardioprotection
From the Institute of Molecular Cardiobiology, Johns Hopkins University, Baltimore, Md.
Correspondence to Brian O’Rourke, PhD, Johns Hopkins University, Institute of Molecular Cardiobiology, 720 Rutland Ave, 844 Ross Bldg, Baltimore, MD 21205-2195. E-mail bor{at}jhmi.edu
This Review is part of a thematic series on Mitochondrial Dysfunction in Ischemia, which includes the following articles:
Role of the Mitochondrial Permeability Transition in Myocardial Disease
Primary and Secondary Signaling Pathways in Early Preconditioning That Converge on the Mitochondria to Produce Cardioprotection
Evidence for Mitochondrial K+ Channels and Their Role in Cardioprotection
Mitochondrial Death Pathways
Roberto Bolli Editor
Twenty years after the discovery of sarcolemmal ATP-sensitive K+ channels and 12 years after the discovery of mitochondrial KATP (mitoKATP) channels, progress has been remarkable, but many questions remain. In the case of the former, detailed structural information is available, and it is well accepted that the channel couples bioenergetics to cellular electrical excitability; however, in the heart, a clear physiological or pathophysiological role has yet to be defined. For mitoKATP, structural information is lacking, but there is abundant evidence linking the opening of the channel to protection against ischemia-reperfusion injury or apoptosis. This review updates recent progress in understanding the physiological role of mitoKATP and highlights outstanding questions and controversies, with the intent of stimulating additional investigation on this topic.
Key Words: ischemia • reperfusion • mitochondria • ATP-sensitive potassium channels • calcium-activated potassium channels
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|
|
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 D. Ai, W. Pang, N. Li, M. Xu, P. D. Jones, J. Yang, Y. Zhang, N. Chiamvimonvat, J. Y.-J. Shyy, B. D. Hammock, et al. Soluble epoxide hydrolase plays an essential role in angiotensin II-induced cardiac hypertrophy PNAS, January 13, 2009; 106(2): 564 - 569. [Abstract] [Full Text] [PDF]
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|
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|
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|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
 |
|
 E. Murphy and C. Steenbergen Mechanisms Underlying Acute Protection From Cardiac Ischemia-Reperfusion Injury Physiol Rev, April 1, 2008; 88(2): 581 - 609. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
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|
|
|
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|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
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|
|
|
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|
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|
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|
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|
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|
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|
|
|
|
|
|
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|
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|
|
 |
|
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|
|
|
|
 |
|
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|
|
|
|
|
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|
|
|
|
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|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
 K Boengler, R Schulz, and G Heusch Connexin 43 signalling and cardioprotection Heart, December 1, 2006; 92(12): 1724 - 1727. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
 S. Roth, J. C. Dreixler, A. R. Shaikh, K. H. Lee, and V. Bindokas Mitochondrial Potassium ATP Channels and Retinal Ischemic Preconditioning Invest. Ophthalmol. Vis. Sci., May 1, 2006; 47(5): 2114 - 2124. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
|
|
R. J. Diaz and G. J. Wilson Studying ischemic preconditioning in isolated cardiomyocyte models Cardiovasc Res, May 1, 2006; 70(2): 286 - 296. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
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|
|
|
|
|
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D. J. Chambers Invited commentary Ann. Thorac. Surg., April 1, 2006; 81(4): 1416 - 1416. [Full Text] [PDF]
|
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|
|
|
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|
|
|
|
|
|
D. A. Brown, A. J. Chicco, K. N. Jew, M. S. Johnson, J. M. Lynch, P. A. Watson, and R. L. Moore Cardioprotection afforded by chronic exercise is mediated by the sarcolemmal, and not the mitochondrial, isoform of the KATP channel in the rat J. Physiol., December 15, 2005; 569(3): 913 - 924. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
 |
|
 B. O'Rourke, S. Cortassa, and M. A. Aon Mitochondrial Ion Channels: Gatekeepers of Life and Death Physiology, October 1, 2005; 20(5): 303 - 315. [Abstract] [Full Text] [PDF]
|
|
|
|
|
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R. M. Mentzer Jr Invited commentary Ann. Thorac. Surg., October 1, 2005; 80(4): 1416 - 1416. [Full Text] [PDF]
|
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|
|
|
|
T. Brustovetsky, N. Shalbuyeva, and N. Brustovetsky Lack of manifestations of diazoxide/5-hydroxydecanoate-sensitive KATP channel in rat brain nonsynaptosomal mitochondria J. Physiol., October 1, 2005; 568(1): 47 - 59. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
 |
|
 F. R. Heinzel, Y. Luo, X. Li, K. Boengler, A. Buechert, D. Garcia-Dorado, F. Di Lisa, R. Schulz, and G. Heusch Impairment of Diazoxide-Induced Formation of Reactive Oxygen Species and Loss of Cardioprotection in Connexin 43 Deficient Mice Circ. Res., September 16, 2005; 97(6): 583 - 586. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Q. Xi, S. Y. Cheranov, and J. H. Jaggar Mitochondria-Derived Reactive Oxygen Species Dilate Cerebral Arteries by Activating Ca2+ Sparks Circ. Res., August 19, 2005; 97(4): 354 - 362. [Abstract] [Full Text] [PDF]
|
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|
|
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K. Boengler, G. Dodoni, A. Rodriguez-Sinovas, A. Cabestrero, M. Ruiz-Meana, P. Gres, I. Konietzka, C. Lopez-Iglesias, D. Garcia-Dorado, F. Di Lisa, et al. Connexin 43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning Cardiovasc Res, August 1, 2005; 67(2): 234 - 244. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
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M. Juhaszova, C. Rabuel, D. B. Zorov, E. G. Lakatta, and S. J. Sollott Protection in the aged heart: preventing the heart-break of old age? Cardiovasc Res, May 1, 2005; 66(2): 233 - 244. [Abstract] [Full Text] [PDF]
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|
|
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A. Sarre, N. Lange, P. Kucera, and E. Raddatz mitoKATP channel activation in the postanoxic developing heart protects E-C coupling via NO-, ROS-, and PKC-dependent pathways Am J Physiol Heart Circ Physiol, April 1, 2005; 288(4): H1611 - H1619. [Abstract] [Full Text] [PDF]
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T. Gori, S. Sicuro, S. Dragoni, G. Donati, S. Forconi, and J. D. Parker Sildenafil Prevents Endothelial Dysfunction Induced by Ischemia and Reperfusion via Opening of Adenosine Triphosphate-Sensitive Potassium Channels: A Human In Vivo Study Circulation, February 15, 2005; 111(6): 742 - 746. [Abstract] [Full Text] [PDF]
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T. Sato, T. Saito, N. Saegusa, and H. Nakaya Mitochondrial Ca2+-Activated K+ Channels in Cardiac Myocytes: A Mechanism of the Cardioprotective Effect and Modulation by Protein Kinase A Circulation, January 18, 2005; 111(2): 198 - 203. [Abstract] [Full Text] [PDF]
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P. J. Hanley, S. Drose, U. Brandt, R. A. Lareau, A. L. Banerjee, D. K. Srivastava, L. J. Banaszak, J. J. Barycki, P. P. Van Veldhoven, and J. Daut 5-Hydroxydecanoate is metabolised in mitochondria and creates a rate-limiting bottleneck for {beta}-oxidation of fatty acids J. Physiol., January 15, 2005; 562(2): 307 - 318. [Abstract] [Full Text] [PDF]
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J. Seubert, B. Yang, J. A. Bradbury, J. Graves, L. M. Degraff, S. Gabel, R. Gooch, J. Foley, J. Newman, L. Mao, et al. Enhanced Postischemic Functional Recovery in CYP2J2 Transgenic Hearts Involves Mitochondrial ATP-Sensitive K+ Channels and p42/p44 MAPK Pathway Circ. Res., September 3, 2004; 95(5): 506 - 514. [Abstract] [Full Text] [PDF]
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