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Cytoprotective Role of Ca2+- Activated K+ Channels in the Cardiac Inner Mitochondrial Membrane
Wenhong Xu,1Yongge Liu,2Sheng Wang,2Todd McDonald,3Jennifer E. Van Eyk,3Agnieszka Sidor,1Brian O'Rourke1*
Ion channels on the mitochondrial inner membrane
influence cell function in specific ways that can be detrimental or
beneficialto cell survival. At least one type of potassium
(K+) channel, the mitochondrial adenosine
triphosphate-sensitiveK+ channel
(mitoKATP), is an important effector of protection againstnecrotic and apoptotic cell injury after ischemia. Here anotherchannel
with properties similar to the surface membrane calcium-activatedK+ channel was found on the mitochondrial inner membrane
(mitoKCa)of guinea pig ventricular cells.
MitoKCa significantly contributedto mitochondrial
K+ uptake of the myocyte, and an opener of
mitoKCa protected heartsagainst infarction.
1 Institute of Molecular Cardiobiology, The
Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
2 Maryland Research Laboratories, Otsuka Maryland
Research Institute, Rockville, MD 20850, USA.
3 Department of Physiology, Queen's University,
Kingston, Ontario, K7L 3N6 Canada.
*
To whom correspondence should be addressed. E-mail:
bor{at}jhmi.edu.
6-[4-(1-Cyclohexyl-1H-tetrazol-5-yl)butoxy]-3,4-dihydro-2-(1H)quinolinone (Cilostazol), a Phosphodiesterase Type 3 Inhibitor, Reduces Infarct Size via Activation of Mitochondrial Ca2+-Activated K+ Channels in Rabbit Hearts.
M. Fukasawa, H. Nishida, T. Sato, M. Miyazaki, and H. Nakaya (2008)
J. Pharmacol. Exp. Ther.
326, 100-104
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Mechanisms Underlying Acute Protection From Cardiac Ischemia-Reperfusion Injury.
Activation of Mitochondrial Large-Conductance Calcium-Activated K+ Channels via Protein Kinase A Mediates Desflurane-Induced Preconditioning.
A. Redel, M. Lange, V. Jazbutyte, C. Lotz, T. M. Smul, N. Roewer, and F. Kehl (2008)
Anesth. Analg.
106, 384-391
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Infarct size limitation by adrenomedullin: protein kinase A but not PI3-kinase is linked to mitochondrial KCa channels.
H. Nishida, T. Sato, M. Miyazaki, and H. Nakaya (2008)
Cardiovasc Res
77, 398-405
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Mol. Pharmacol.
72, 1033-1044
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Reverse electron flow-induced ROS production is attenuated by activation of mitochondrial Ca2+-sensitive K+ channels.
A. Heinen, M. Aldakkak, D. F. Stowe, S. S. Rhodes, M. L. Riess, S. G. Varadarajan, and A. K. S. Camara (2007)
Am J Physiol Heart Circ Physiol
293, H1400-H1407
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Dynamic changes in nitric oxide and mitochondrial oxidative stress with site-dependent differential tissue response during anoxic preconditioning in rat heart.
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Am J Physiol Heart Circ Physiol
293, H1457-H1465
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Protein kinase C isoform-dependent modulation of ATP-sensitive K+ channels in mitochondrial inner membrane.
Isoflurane preconditioning uncouples mitochondria and protects against hypoxia-reoxygenation.
M. Ljubkovic, Y. Mio, J. Marinovic, A. Stadnicka, D. C. Warltier, Z. J. Bosnjak, and M. Bienengraeber (2007)
Am J Physiol Cell Physiol
292, C1583-C1590
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Pharmacological and physiological stimuli do not promote Ca2+-sensitive K+ channel activity in isolated heart mitochondria.
D. V. Cancherini, B. B. Queliconi, and A. J. Kowaltowski (2007)
Cardiovasc Res
73, 720-728
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Mitochondrial Ca2+-induced K+ influx increases respiration and enhances ROS production while maintaining membrane potential.
A. Heinen, A. K. S. Camara, M. Aldakkak, S. S. Rhodes, M. L. Riess, and D. F. Stowe (2007)
Am J Physiol Cell Physiol
292, C148-C156
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Regulation of mitochondrial matrix volume.
A. Kaasik, D. Safiulina, A. Zharkovsky, and V. Veksler (2007)
Am J Physiol Cell Physiol
292, C157-C163
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Calcium-dependent Spontaneously Reversible Remodeling of Brain Mitochondria.
N. Shalbuyeva, T. Brustovetsky, A. Bolshakov, and N. Brustovetsky (2006)
J. Biol. Chem.
281, 37547-37558
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Targeted expression of Kir6.2 in mitochondria confers protection against hypoxic stress.
M. Ljubkovic, J. Marinovic, A. Fuchs, Z. J. Bosnjak, and M. Bienengraeber (2006)
J. Physiol.
577, 17-29
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Role of Soluble Epoxide Hydrolase in Postischemic Recovery of Heart Contractile Function.
J. M. Seubert, C. J. Sinal, J. Graves, L. M. DeGraff, J. A. Bradbury, C. R. Lee, K. Goralski, M. A. Carey, A. Luria, J. W. Newman, et al. (2006)
Circ. Res.
99, 442-450
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Levosimendan protects against experimental endotoxemic acute renal failure.
R. A. Zager, A. C. Johnson, S. Lund, S. Y. Hanson, and C. K. Abrass (2006)
Am J Physiol Renal Physiol
290, F1453-F1462
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Three methionine residues located within the regulator of conductance for K+ (RCK) domains confer oxidative sensitivity to large-conductance Ca2+-activated K+ channels.
L. C. Santarelli, R. Wassef, S. H. Heinemann, and T. Hoshi (2006)
J. Physiol.
571, 329-348
|Abstract »|Full Text »|PDF »
Cardiac mitochondrial preconditioning by Big Ca2+-sensitive K+ channel opening requires superoxide radical generation.
D. F. Stowe, M. Aldakkak, A. K. S. Camara, M. L. Riess, A. Heinen, S. G. Varadarajan, and M.-T. Jiang (2006)
Am J Physiol Heart Circ Physiol
290, H434-H440
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Mitochondrial Ion Channels: Gatekeepers of Life and Death.
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S. Ohya, Y. Kuwata, K. Sakamoto, K. Muraki, and Y. Imaizumi (2005)
Am J Physiol Heart Circ Physiol
289, H1635-H1642
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W.-K. Lee, M. Spielmann, U. Bork, and F. Thevenod (2005)
Am J Physiol Cell Physiol
289, C656-C664
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A Novel Potassium Channel in Lymphocyte Mitochondria.
I. Szabo, J. Bock, A. Jekle, M. Soddemann, C. Adams, F. Lang, M. Zoratti, and E. Gulbins (2005)
J. Biol. Chem.
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Calcium-Activated Potassium Channel Triggers Cardioprotection of Ischemic Preconditioning.
C.-M. Cao, Q. Xia, Q. Gao, M. Chen, and T.-M. Wong (2005)
J. Pharmacol. Exp. Ther.
312, 644-650
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Mitochondrial Ca2+-Activated K+ Channels in Cardiac Myocytes: A Mechanism of the Cardioprotective Effect and Modulation by Protein Kinase A.
T. Sato, T. Saito, N. Saegusa, and H. Nakaya (2005)
Circulation
111, 198-203
|Abstract »|Full Text »|PDF »
Testosterone Induces Cytoprotection by Activating ATP-Sensitive K+ Channels in the Cardiac Mitochondrial Inner Membrane.
F. Er, G. Michels, N. Gassanov, F. Rivero, and U. C. Hoppe (2004)
Circulation
110, 3100-3107
|Abstract »|Full Text »|PDF »
Opening of Ca2+-activated K+ channels triggers early and delayed preconditioning against I/R injury independent of NOS in mice.
X. Wang, C. Yin, L. Xi, and R. C. Kukreja (2004)
Am J Physiol Heart Circ Physiol
287, H2070-H2077
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Spontaneous mitochondrial depolarizations are independent of SR Ca2+ release.
C. M. O'Reilly, K. E. Fogarty, R. M. Drummond, R. A. Tuft Jr., and J. V. Walsh (2004)
Am J Physiol Cell Physiol
286, C1139-C1151
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BK Channel News: Full Coverage on the Calcium Bowl.
E. G. Moczydlowski (2004)
J. Gen. Physiol.
123, 471-473
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Evidence for Mitochondrial K+ Channels and Their Role in Cardioprotection.
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A. P Halestrap, S. J Clarke, and S. A Javadov (2004)
Cardiovasc Res
61, 372-385
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Activation of K+ channels: an essential pathway in programmed cell death.
C. V. Remillard and J. X.-J. Yuan (2004)
Am J Physiol Lung Cell Mol Physiol
286, L49-L67
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Spontaneous Changes in Mitochondrial Membrane Potential in Single Isolated Brain Mitochondria.
O. Vergun, T. V. Votyakova, and I. J. Reynolds (2003)
Biophys. J.
85, 3358-3366
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Proteomic Analysis of the Mouse Liver Mitochondrial Inner Membrane.
S. Da Cruz, I. Xenarios, J. Langridge, F. Vilbois, P. A. Parone, and J.-C. Martinou (2003)
J. Biol. Chem.
278, 41566-41571
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Role of the Mitochondrial Permeability Transition in Myocardial Disease.
J. N. Weiss, P. Korge, H. M. Honda, and P. Ping (2003)
Circ. Res.
93, 292-301
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Mitochondrial plasticity in classical ischemic preconditioning--moving beyond the mitochondrial KATP channel.