Published online before print November 7, 2002, doi: 10.1161/01.RES.0000046003.14031.98
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Submitted on July 2, 2002
Revised on October 25, 2002
Accepted on October 25, 2002
Peroxynitrite Inhibits Ca2+-Activated K+ Channel Activity in Smooth Muscle of Human Coronary Arterioles
Yanping Liu *;
From the Departments of Internal Medicine and Cardiovascular Center, Medical College of Wisconsin, and Zablocki VA Medical Center (Y.L., K.T., Q.C., H.L., D.G.), Milwaukee, Wis; and Cardiovascular Surgery Associates (L.K.), St Luke's Medical Center, Milwaukee, Wis.
* To whom correspondence should be addressed. E-mail: ypliu{at}mcw.edu.
We examined the hypothesis that ONOO-, a product of the interaction between superoxide (O2·-) and nitric oxide (NO), inhibits calcium-activated K+ (KCa) channel activity in vascular smooth muscle cells (VSMCs) of human coronary arterioles (HCAs), thereby reducing hyperpolarization-mediated vasodilation. HCAs were dissected from right atrial appendages. The interaction of ONOO- with microvessels was determined by immunohistochemistry using a nitrotyrosine antibody. Strong staining was observed in arteries exposed to authentic ONOO- or to sodium nitroprusside (SNP)+xanthine (XA)+xanthine oxidase (XO). Dilation to 10-8 mol/L bradykinin (BK) was abolished in vessels exposed to ONOO- (-2.5±8%; P<0.05) but not DC-ONOO- (65±8%). Reduced dilation to BK was also observed after application of XO and SNP. Dilation to NS1619 (KCa channel opener) was reduced in endothelial denuded arterioles treated with ONOO-. In isolated VSMCs, whole-cell peak K+ current density was reduced by ONOO- (control 65±15 pA/pF; ONOO- 42±9 pA/pF; P<0.05). Iberiotoxin had no further effect on whole-cell K+ current. In inside-out patches, ONOO- but not DC-ONOO- decreased open state probability (NPo) of KCa channel by 50±12%. O2·- generated by XA+XO had no effect on BK-induced dilation and NPo of KCa channels. These results suggest that ONOO-, but not O2·-, inhibits KCa channel activity in VSMCs possibly by a direct effect. This mechanism may contribute to impaired EDHF-mediated dilation in conditions such as ischemia/reperfusion where increased activity of NO synthase occurs in the presence of excess of O2·-.
Key words: K+ channels • peroxynitrite • coronary circulation • vascular smooth muscle
This article has been cited by other articles:
 |
|
 |
|
  S. Hou, S. H. Heinemann, and T. Hoshi Modulation of BKCa Channel Gating by Endogenous Signaling Molecules Physiology, February 1, 2009; 24(1): 26 - 35. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Bassil, Y. Li, and M. B. Anand-Srivastava Peroxynitrite inhibits the expression of Gi{alpha} protein and adenylyl cyclase signaling in vascular smooth muscle cells Am J Physiol Heart Circ Physiol, February 1, 2008; 294(2): H775 - H784. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Heintz, M. Damm, M. Brand, T. Koch, and A. Deussen Coronary flow regulation in mouse heart during hypercapnic acidosis: role of NO and its compensation during eNOS impairment Cardiovasc Res, January 1, 2008; 77(1): 188 - 196. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. H. Bubolz, Q. Wu, B. T. Larsen, D. D. Gutterman, and Y. Liu Ebselen reduces nitration and restores voltage-gated potassium channel function in small coronary arteries of diabetic rats Am J Physiol Heart Circ Physiol, October 1, 2007; 293(4): H2231 - H2237. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D.-L. Dong, Y. Zhang, D.-H. Lin, J. Chen, S. Patschan, M. S. Goligorsky, A. Nasjletti, B.-F. Yang, and W.-H. Wang Carbon Monoxide Stimulates the Ca2+ Activated Big Conductance K Channels in Cultured Human Endothelial Cells Hypertension, October 1, 2007; 50(4): 643 - 651. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Pacher, J. S. Beckman, and L. Liaudet Nitric Oxide and Peroxynitrite in Health and Disease Physiol Rev, January 1, 2007; 87(1): 315 - 424. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M.-E. Gendron, N. Thorin-Trescases, L. Villeneuve, and E. Thorin Aging associated with mild dyslipidemia reveals that COX-2 preserves dilation despite endothelial dysfunction Am J Physiol Heart Circ Physiol, January 1, 2007; 292(1): H451 - H458. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. E. Mullick, U. B. Zaid, C. N. Athanassious, S. R. Lentz, J. C. Rutledge, and J. D. Symons Hyperhomocysteinemia increases arterial permeability and stiffness in mice Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2006; 291(5): R1349 - R1354. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. Zhou, X.-L. Wang, K. G. Lamping, and H.-C. Lee Inhibition of Protein Kinase Cbeta Protects against Diabetes-Induced Impairment in Arachidonic Acid Dilation of Small Coronary Arteries J. Pharmacol. Exp. Ther., October 1, 2006; 319(1): 199 - 207. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. D. Rainbow, M. E. L. Hardy, N. B. Standen, and N. W. Davies Glucose reduces endothelin inhibition of voltage-gated potassium channels in rat arterial smooth muscle cells J. Physiol., September 15, 2006; 575(3): 833 - 844. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Lu, T. He, Z. S. Katusic, and H.-C. Lee Molecular Mechanisms Mediating Inhibition of Human Large Conductance Ca2+-Activated K+ Channels by High Glucose Circ. Res., September 15, 2006; 99(6): 607 - 616. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Yada, H. Shimokawa, O. Hiramatsu, Y. Haruna, Y. Morita, N. Kashihara, Y. Shinozaki, H. Mori, M. Goto, Y. Ogasawara, et al. Cardioprotective role of endogenous hydrogen peroxide during ischemia-reperfusion injury in canine coronary microcirculation in vivo Am J Physiol Heart Circ Physiol, September 1, 2006; 291(3): H1138 - H1146. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Zhang, T. Tazzeo, V. Chu, and L. J. Janssen Membrane potassium currents in human radial artery and their regulation by nitric oxide donor Cardiovasc Res, July 15, 2006; 71(2): 383 - 392. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. J. Maneen, R. Hannah, L. Vitullo, N. DeLance, and M. J. Cipolla Peroxynitrite Diminishes Myogenic Activity and Is Associated With Decreased Vascular Smooth Muscle F-Actin in Rat Posterior Cerebral Arteries Stroke, March 1, 2006; 37(3): 894 - 899. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Liu, A. H. Bubolz, Y. Shi, P. J. Newman, D. K. Newman, and D. D. Gutterman Peroxynitrite reduces the endothelium-derived hyperpolarizing factor component of coronary flow-mediated dilation in PECAM-1-knockout mice Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2006; 290(1): R57 - R65. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Ohashi, F. Faraci, and D. Heistad Peroxynitrite hyperpolarizes smooth muscle and relaxes internal carotid artery in rabbit via ATP-sensitive K+ channels Am J Physiol Heart Circ Physiol, November 1, 2005; 289(5): H2244 - H2250. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. H. Bubolz, H. Li, Q. Wu, and Y. Liu Enhanced oxidative stress impairs cAMP-mediated dilation by reducing Kv channel function in small coronary arteries of diabetic rats Am J Physiol Heart Circ Physiol, November 1, 2005; 289(5): H1873 - H1880. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Xu, X. Bian, S. W. Watts, and A. Hlavacova Activation of Vascular BK Channel by Tempol in DOCA-Salt Hypertensive Rats Hypertension, November 1, 2005; 46(5): 1154 - 1162. [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]
|
|
|
|
 |
|
 G. Tang, L. Wu, and R. Wang The Effect of Hydroxylamine on KATP Channels in Vascular Smooth Muscle and Underlying Mechanisms Mol. Pharmacol., May 1, 2005; 67(5): 1723 - 1731. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. D. Gutterman, H. Miura, and Y. Liu Redox Modulation of Vascular Tone: Focus of Potassium Channel Mechanisms of Dilation Arterioscler Thromb Vasc Biol, April 1, 2005; 25(4): 671 - 678. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Wilcox and D. Gutterman Focus on oxidative stress in the cardiovascular and renal systems Am J Physiol Heart Circ Physiol, January 1, 2005; 288(1): H3 - H6. [Full Text] [PDF]
|
|
|
|
 |
|
 H. Li, D. D. Gutterman, N. J. Rusch, A. Bubolz, and Y. Liu Nitration and Functional Loss of Voltage-Gated K+ Channels in Rat Coronary Microvessels Exposed to High Glucose Diabetes, September 1, 2004; 53(9): 2436 - 2442. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. W. Miller, C. D. Tulbert, and D. W. Busija Rosuvastatin treatment reverses impaired coronary artery vasodilation in fructose-fed, insulin-resistant rats Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2004; 287(1): R157 - R160. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Sato, I. Sakuma, and D. D. Gutterman Mechanism of dilation to reactive oxygen species in human coronary arterioles Am J Physiol Heart Circ Physiol, December 1, 2003; 285(6): H2345 - H2354. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Beckman, A. B. Goldfine, M. B. Gordon, L. A. Garrett, J. F. Keaney Jr., and M. A. Creager Oral antioxidant therapy improves endothelial function in Type 1 but not Type 2 diabetes mellitus Am J Physiol Heart Circ Physiol, December 1, 2003; 285(6): H2392 - H2398. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Liu, H. Zhao, H. Li, B. Kalyanaraman, A. C. Nicolosi, and D. D. Gutterman Mitochondrial Sources of H2O2 Generation Play a Key Role in Flow-Mediated Dilation in Human Coronary Resistance Arteries Circ. Res., September 19, 2003; 93(6): 573 - 580. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Li, Q. Chai, D. D. Gutterman, and Y. Liu Elevated glucose impairs cAMP-mediated dilation by reducing Kv channel activity in rat small coronary smooth muscle cells Am J Physiol Heart Circ Physiol, August 7, 2003; 285(3): H1213 - H1219. [Abstract] [Full Text] [PDF]
|
|