Circulation Research. 2001;89:1177-1183
Published online before print November 8, 2001, doi: 10.1161/hh2401.101752
Published online before print November 8, 2001, doi: 10.1161/hh2401.101752
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© 2001 American Heart Association, Inc.
Cellular Biology |
Characteristics and Superoxide-Induced Activation of Reconstituted Myocardial Mitochondrial ATP-Sensitive Potassium Channels
From the Department of Pharmacology and Toxicology (D.X.Z., Y.-F.C., W.B.C., G.J.G., P.-L.L.) and the Department of Physiology (A.-P.Z.), Medical College of Wisconsin, Milwaukee, Wis.
Correspondence to Pin-Lan Li, MD, PhD, Department of Pharmacology and Toxicology, Medical College of Wisconsin, 8701 Watertown Plank Rd, Milwaukee, WI 53226. E-mail pli{at}mcw.edu
Mitochondrial ATP-sensitive potassium (mitoKATP) channels have been suggested as triggers and end effectors in myocardial ischemic preconditioning. However, the intracellular mechanism regulating mitoKATP channels remains unclear. In the present study, mitoKATP channels from bovine ventricular myocardium were reconstituted using planar lipid bilayers, and the effect of superoxide (O2-·) on the activity of these reconstituted channels was examined. After incorporation, a potassium-selective current was recorded. The mean conductance of this current was 56 pS at 150 mmol/L KCl, which was substantially inhibited by 1 mmol/L MgATP. 5-Hydroxydecanoate (5-HD, 10 to 100 µmol/L), a selective mitoKATP antagonist, reduced the open state probability (NPo) of these channels in a concentration-dependent manner, whereas diazoxide (10 µmol/L), a selective mitoKATP agonist, significantly increased channel activity. HMR-1098 (100 µmol/L), a selective sarcolemmal KATP antagonist, had no effect on the activity of reconstituted channels. Addition of xanthine/xanthine oxidase (100 µmol/L per 0.038 U/mL), an O2-·-generating system, resulted in a marked activation of mitoKATP channels; the NPo of the channels was increased from 0.60±0.10 to 1.94±0.02. This O2-·-induced channel activation was completely abolished by pretreatment with 5-HD (100 µmol/L) or a sulfhydryl alkylating compound, N-ethylmaleimide (2 mmol/L). It is concluded that myocardial mitoKATP channels can be reconstituted into lipid bilayers and that O2-· activates these channels. The effect of O2-· may be associated with its direct action on the sulfhydryl groups of the channel protein.
Key Words: ATP-sensitive K+ channel • mitochondria • superoxide • heart • channel reconstitution
This article has been cited by other articles:
 |
|
 |
|
  C. Maack, E. R. Dabew, M. Hohl, H.-J. Schafers, and M. Bohm Endogenous Activation of Mitochondrial KATP Channels Protects Human Failing Myocardium From Hydroxyl Radical-Induced Stunning Circ. Res., October 9, 2009; 105(8): 811 - 817. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Sedlic, D. Pravdic, M. Ljubkovic, J. Marinovic, A. Stadnicka, and Z. J. Bosnjak Differences in Production of Reactive Oxygen Species and Mitochondrial Uncoupling as Events in the Preconditioning Signaling Cascade Between Desflurane and Sevoflurane Anesth. Analg., August 1, 2009; 109(2): 405 - 411. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. C. Silva, M. A.B. Rosales, S. K. Biswas, J. B. Lopes de Faria, and J. M. Lopes de Faria Diabetic Retinal Neurodegeneration Is Associated With Mitochondrial Oxidative Stress and Is Improved by an Angiotensin Receptor Blocker in a Model Combining Hypertension and Diabetes Diabetes, June 1, 2009; 58(6): 1382 - 1390. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. D. Garciarena, C. I. Caldiz, M. V. Correa, G. R. Schinella, S. M. Mosca, G. E. Chiappe de Cingolani, H. E. Cingolani, and I. L. Ennis Na+/H+ exchanger-1 inhibitors decrease myocardial superoxide production via direct mitochondrial action J Appl Physiol, December 1, 2008; 105(6): 1706 - 1713. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Pasdois, B. Beauvoit, L. Tariosse, B. Vinassa, S. Bonoron-Adele, and P. D. Santos Effect of diazoxide on flavoprotein oxidation and reactive oxygen species generation during ischemia-reperfusion: a study on Langendorff-perfused rat hearts using optic fibers Am J Physiol Heart Circ Physiol, May 1, 2008; 294(5): H2088 - H2097. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. K. Doughan, D. G. Harrison, and S. I. Dikalov Molecular Mechanisms of Angiotensin II-Mediated Mitochondrial Dysfunction: Linking Mitochondrial Oxidative Damage and Vascular Endothelial Dysfunction Circ. Res., February 29, 2008; 102(4): 488 - 496. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. E. Pamenter, D. S.-H. Shin, M. Cooray, and L. T. Buck Mitochondrial ATP-sensitive K+ channels regulate NMDAR activity in the cortex of the anoxic western painted turtle J. Physiol., February 15, 2008; 586(4): 1043 - 1058. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Nishida, T. Sato, M. Miyazaki, and H. Nakaya Infarct size limitation by adrenomedullin: protein kinase A but not PI3-kinase is linked to mitochondrial KCa channels Cardiovasc Res, January 15, 2008; 77(2): 398 - 405. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-D. Jiao, V. Garg, B. Yang, and K. Hu Novel functional role of heat shock protein 90 in ATP-sensitive K+ channel-mediated hypoxic preconditioning Cardiovasc Res, January 1, 2008; 77(1): 126 - 133. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. I. Caldiz, C. D. Garciarena, R. A. Dulce, L. P. Novaretto, A. M. Yeves, I. L. Ennis, H. E. Cingolani, G. Chiappe de Cingolani, and N. G. Perez Mitochondrial reactive oxygen species activate the slow force response to stretch in feline myocardium J. Physiol., November 1, 2007; 584(3): 895 - 905. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G.-X. Zhang, X.-M. Lu, S. Kimura, and A. Nishiyama Role of mitochondria in angiotensin II-induced reactive oxygen species and mitogen-activated protein kinase activation Cardiovasc Res, November 1, 2007; 76(2): 204 - 212. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. T. Jiang, Y. Nakae, M. Ljubkovic, W.-M. Kwok, D. F. Stowe, and Z. J. Bosnjak Isoflurane Activates Human Cardiac Mitochondrial Adenosine Triphosphate-Sensitive K+ Channels Reconstituted in Lipid Bilayers Anesth. Analg., October 1, 2007; 105(4): 926 - 932. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Ljubkovic, J. Marinovic, A. Fuchs, Z. J. Bosnjak, and M. Bienengraeber Targeted expression of Kir6.2 in mitochondria confers protection against hypoxic stress J. Physiol., November 15, 2006; 577(1): 17 - 29. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Ganitkevich, S. Reil, B. Schwethelm, T. Schroeter, and K. Benndorf Dynamic Responses of Single Cardiomyocytes to Graded Ischemia Studied by Oxygen Clamp in On-Chip Picochambers Circ. Res., July 21, 2006; 99(2): 165 - 171. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. T. Jiang, M. Ljubkovic, Y. Nakae, Y. Shi, W.-M. Kwok, D. F. Stowe, and Z. J. Bosnjak Characterization of human cardiac mitochondrial ATP-sensitive potassium channel and its regulation by phorbol ester in vitro Am J Physiol Heart Circ Physiol, May 1, 2006; 290(5): H1770 - H1776. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Daiber, M. Oelze, S. Sulyok, M. Coldewey, E. Schulz, N. Treiber, U. Hink, A. Mulsch, K. Scharffetter-Kochanek, and T. Munzel Heterozygous Deficiency of Manganese Superoxide Dismutase in Mice (Mn-SOD+/-): A Novel Approach to Assess the Role of Oxidative Stress for the Development of Nitrate Tolerance Mol. Pharmacol., September 1, 2005; 68(3): 579 - 588. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Juncos and J. L. Garvin Superoxide enhances Na-K-2Cl cotransporter activity in the thick ascending limb Am J Physiol Renal Physiol, May 1, 2005; 288(5): F982 - F987. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|
|
|
 |
|
 S. Kimura, G.-X. Zhang, A. Nishiyama, T. Shokoji, L. Yao, Y.-Y. Fan, M. Rahman, T. Suzuki, H. Maeta, and Y. Abe Role of NAD(P)H Oxidase- and Mitochondria-Derived Reactive Oxygen Species in Cardioprotection of Ischemic Reperfusion Injury by Angiotensin II Hypertension, May 1, 2005; 45(5): 860 - 866. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. P. Brandes Triggering Mitochondrial Radical Release: A New Function for NADPH Oxidases Hypertension, May 1, 2005; 45(5): 847 - 848. [Full Text] [PDF]
|
|
|
|
 |
|
 F. Er, G. Michels, N. Gassanov, F. Rivero, and U. C. Hoppe Testosterone Induces Cytoprotection by Activating ATP-Sensitive K+ Channels in the Cardiac Mitochondrial Inner Membrane Circulation, November 9, 2004; 110(19): 3100 - 3107. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. M. Ludwig, K. Tanaka, J. T. Eells, D. Weihrauch, P. S. Pagel, J. R. Kersten, and D. C. Warltier Preconditioning by Isoflurane Is Mediated by Reactive Oxygen Species Generated from Mitochondrial Electron Transport Chain Complex III Anesth. Analg., November 1, 2004; 99(5): 1308 - 1315. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. C. Santarelli, J. Chen, S. H. Heinemann, and T. Hoshi The {beta}1 Subunit Enhances Oxidative Regulation of Large-Conductance Calcium-activated K+ Channels J. Gen. Physiol., September 27, 2004; 124(4): 357 - 370. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Ardehali, Z. Chen, Y. Ko, R. Mejia-Alvarez, and E. Marban Multiprotein complex containing succinate dehydrogenase confers mitochondrial ATP-sensitive K+ channel activity PNAS, August 10, 2004; 101(32): 11880 - 11885. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. O'Rourke Evidence for Mitochondrial K+ Channels and Their Role in Cardioprotection Circ. Res., March 5, 2004; 94(4): 420 - 432. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|
|
|
|
|
J. N. Weiss, P. Korge, H. M. Honda, and P. Ping Role of the Mitochondrial Permeability Transition in Myocardial Disease Circ. Res., August 22, 2003; 93(4): 292 - 301. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|
|
|
|
|
M. M. da Silva, A. Sartori, E. Belisle, and A. J. Kowaltowski Ischemic preconditioning inhibits mitochondrial respiration, increases H2O2 release, and enhances K+ transport Am J Physiol Heart Circ Physiol, June 5, 2003; 285(1): H154 - H162. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|
|
|
|
|
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]
|
|
|
|
 |
|
 A. Munoz, M. Nakazaki, J. C. Goodman, R. Barrios, C. G. Onetti, J. Bryan, and L. Aguilar-Bryan Ischemic Preconditioning in the Hippocampus of a Knockout Mouse Lacking SUR1-Based KATP Channels Stroke, January 1, 2003; 34(1): 164 - 170. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|
|
|
|
|
P. A. Ortiz and J. L. Garvin Superoxide stimulates NaCl absorption by the thick ascending limb Am J Physiol Renal Physiol, November 1, 2002; 283(5): F957 - F962. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|