Oxidative Stress-Induced Afterdepolarizations and Protein Kinase C Signaling
Abstract
:1. Introduction
2. Results
2.1. H2O2-Induced Afterdepolarizations in Adult Rabbit Ventricular Myocytes
2.2. The Role of PKC Signaling in H2O2-Induced Afterdepolarizations
2.3. PKC Mediates ICa,L Enhancement in H2O2-Induced Afterdepolarizations
2.4. PKC Mediates INa,L Augmentation in H2O2-Induced Afterdepolarizations
2.5. Less Involvement of Ito in PKC Signaling in H2O2-Induced Afterdepolarizations
3. Discussion
4. Materials and Methods
4.1. Solutions and Drugs
4.2. Cell Isolation
4.3. Patch-Clamp Methods
4.4. Data Acquisition and Analysis
5. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Tsutsui, H.; Kinugawa, S.; Matsushima, S. Oxidative stress and heart failure. Am. J. Physiol. Heart Circ. Physiol. 2011, 301, H2181–H2190. [Google Scholar] [CrossRef] [PubMed]
- Slezak, J.; Tribulova, N.; Pristacova, J.; Uhrik, B.; Thomas, T.; Khaper, N.; Kaul, N.; Singal, P.K. Hydrogen peroxide changes in ischemic and reperfused heart. Cytochemistry and biochemical and X-ray microanalysis. Am. J. Pathol. 1995, 147, 772–781. [Google Scholar] [PubMed]
- Xie, L.H.; Chen, F.; Karagueuzian, H.S.; Weiss, J.N. Oxidative-stress-induced afterdepolarizations and calmodulin kinase II signaling. Circ. Res. 2009, 104, 79–86. [Google Scholar] [CrossRef] [PubMed]
- Hudasek, K.; Brown, S.T.; Fearon, I.M. H2O2 regulates recombinant Ca2+ channel α1C subunits but does not mediate their sensitivity to acute hypoxia. Biochem. Biophys. Res. Commun. 2004, 318, 135–141. [Google Scholar] [CrossRef] [PubMed]
- Sag, C.M.; Wagner, S.; Maier, L.S. Role of oxidants on calcium and sodium movement in healthy and diseased cardiac myocytes. Free Radic. Biol. Med. 2013, 63, 338–349. [Google Scholar] [CrossRef] [PubMed]
- Berube, J.; Caouette, D.; Daleau, P. Hydrogen peroxide modifies the kinetics of HERG channel expressed in a mammalian cell line. J. Pharmacol. Exp. Ther. 2001, 297, 96–102. [Google Scholar] [PubMed]
- Zhao, Z.; Xie, Y.; Wen, H.; Xiao, D.; Allen, C.; Fefelova, N.; Dun, W.; Boyden, P.A.; Qu, Z.; Xie, L.H. Role of the transient outward potassium current in the genesis of early afterdepolarizations in cardiac cells. Cardiovasc. Res. 2012, 95, 308–316. [Google Scholar] [CrossRef] [PubMed]
- Ward, C.A.; Giles, W.R. Ionic mechanism of the effects of hydrogen peroxide in rat ventricular myocytes. J. Physiol. 1997, 500, 631–642. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Shryock, J.C.; Wagner, S.; Maier, L.S.; Belardinelli, L. Blocking late sodium current reduces hydrogen peroxide-induced arrhythmogenic activity and contractile dysfunction. J. Pharmacol. Exp. Ther. 2006, 318, 214–222. [Google Scholar] [CrossRef] [PubMed]
- Palaniyandi, S.S.; Sun, L.; Ferreira, J.C.; Mochly-Rosen, D. Protein kinase C in heart failure: A therapeutic target? Cardiovasc. Res. 2009, 82, 229–239. [Google Scholar] [CrossRef] [PubMed]
- Boyle, A.J.; Kelly, D.J.; Zhang, Y.; Cox, A.J.; Gow, R.M.; Way, K.; Itescu, S.; Krum, H.; Gilbert, R.E. Inhibition of protein kinase C reduces left ventricular fibrosis and dysfunction following myocardial infarction. J. Mol. Cell. Cardiol. 2005, 39, 213–221. [Google Scholar] [CrossRef] [PubMed]
- Braz, J.C.; Gregory, K.; Pathak, A.; Zhao, W.; Sahin, B.; Klevitsky, R.; Kimball, T.F.; Lorenz, J.N.; Nairn, A.C.; Liggett, S.B.; et al. PKC-α regulates cardiac contractility and propensity toward heart failure. Nat. Med. 2004, 10, 248–254. [Google Scholar] [CrossRef] [PubMed]
- Belin, R.J.; Sumandea, M.P.; Allen, E.J.; Schoenfelt, K.; Wang, H.; Solaro, R.J.; de Tombe, P.P. Augmented protein kinase Cα-induced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circ. Res. 2007, 101, 195–204. [Google Scholar] [CrossRef] [PubMed]
- Bowling, N.; Walsh, R.A.; Song, G.; Estridge, T.; Sandusky, G.E.; Fouts, R.L.; Mintze, K.; Pickard, T.; Roden, R.; Bristow, M.R.; et al. Increased protein kinase C activity and expression of Ca2+-sensitive isoforms in the failing human heart. Circulation 1999, 99, 384–391. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, J.C.; Koyanagi, T.; Palaniyandi, S.S.; Fajardo, G.; Churchill, E.N.; Budas, G.; Disatnik, M.H.; Bernstein, D.; Brum, P.C.; Mochly-Rosen, D. Pharmacological inhibition of βIIPKC is cardioprotective in late-stage hypertrophy. J. Mol. Cell. Cardiol. 2011, 51, 980–987. [Google Scholar] [CrossRef] [PubMed]
- Aydin, O.; Becker, R.; Kraft, P.; Voss, F.; Koch, M.; Kelemen, K.; Katus, H.A.; Bauer, A. Effects of protein kinase C activation on cardiac repolarization and arrhythmogenesis in Langendorff-perfused rabbit hearts. Europace 2007, 9, 1094–1098. [Google Scholar] [CrossRef] [PubMed]
- Gopalakrishna, R.; Anderson, W.B. Ca2+- and phospholipid-independent activation of protein kinase C by selective oxidative modification of the regulatory domain. Proc. Natl. Acad. Sci. USA 1989, 86, 6758–6762. [Google Scholar] [CrossRef] [PubMed]
- Shasby, D.M.; Yorek, M.; Shasby, S.S. Exogenous oxidants initiate hydrolysis of endothelial cell inositol phospholipids. Blood 1988, 72, 491–499. [Google Scholar] [PubMed]
- Hou, J.W.; Li, W.; Guo, K.; Chen, X.M.; Chen, Y.H.; Li, C.Y.; Zhao, B.C.; Zhao, J.; Wang, H.; Wang, Y.P.; et al. Antiarrhythmic effects and potential mechanism of WenXin KeLi in cardiac Purkinje cells. Heart Rhythm 2016, 13, 973–982. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Wang, Y.P.; Gao, L.; Zhang, P.P.; Zhou, Q.; Xu, Q.F.; Zhou, Z.W.; Guo, K.; Chen, R.H.; Yang, H.T.; et al. Resveratrol protects rabbit ventricular myocytes against oxidative stress-induced arrhythmogenic activity and Ca2+ overload. Acta Pharmacol. Sin. 2013, 34, 1164–1173. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Yu, Y.; Hou, J.W.; Zhou, Z.W.; Guo, K.; Zhang, P.P.; Wang, Z.Q.; Yan, J.H.; Sun, J.; Zhou, Q.; et al. Larger rate dependence of late sodium current in cardiac Purkinje cells: A potential link to arrhythmogenesis. Heart Rhythm 2017, 14, 422–431. [Google Scholar] [CrossRef] [PubMed]
- Murphy, S.; Frishman, W.H. Protein kinase C in cardiac disease and as a potential therapeutic target. Cardiol. Rev. 2005, 13, 3–12. [Google Scholar] [PubMed]
- Puglisi, J.L.; Yuan, W.; Timofeyev, V.; Myers, R.E.; Chiamvimonvat, N.; Samarel, A.M.; Bers, D.M. Phorbol ester and endothelin-1 alter functional expression of Na+/Ca2+ exchange, K+, and Ca2+ currents in cultured neonatal rat myocytes. Am. J. Physiol. Heart Circ. Physiol. 2011, 300, H617–H626. [Google Scholar] [CrossRef] [PubMed]
- Morita, N.; Lee, J.H.; Xie, Y.; Sovari, A.; Qu, Z.; Weiss, J.N.; Karagueuzian, H.S. Suppression of re-entrant and multifocal ventricular fibrillation by the late sodium current blocker ranolazine. J. Am. Coll. Cardiol. 2011, 57, 366–375. [Google Scholar] [CrossRef] [PubMed]
- Dorn, G.W., 2nd; Force, T. Protein kinase cascades in the regulation of cardiac hypertrophy. J. Clin. Investig. 2005, 115, 527–537. [Google Scholar] [CrossRef] [PubMed]
- House, C.; Kemp, B.E. Protein kinase C contains a pseudosubstrate prototope in its regulatory domain. Science 1987, 238, 1726–1728. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Liu, G.; Zakharov, S.I.; Morrow, J.P.; Rybin, V.O.; Steinberg, S.F.; Marx, S.O. Ser1928 is a common site for Cav1.2 phosphorylation by protein kinase C isoforms. J. Biol. Chem. 2005, 280, 207–214. [Google Scholar] [CrossRef] [PubMed]
- Qu, Y.; Rogers, J.C.; Tanada, T.N.; Catterall, W.A.; Scheuer, T. Phosphorylation of S1505 in the cardiac Na+ channel inactivation gate is required for modulation by protein kinase C. J. Gen. Physiol. 1996, 108, 375–379. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Luo, A.; Wu, L.; Wan, W.; Zhang, P.; Ren, Z.; Zhang, S.; Qian, C.; Shryock, J.C.; Belardinelli, L. Calmodulin kinase II and protein kinase C mediate the effect of increased intracellular calcium to augment late sodium current in rabbit ventricular myocytes. Am. J. Physiol. Cell. Physiol. 2012, 302, C1141–C1151. [Google Scholar] [CrossRef] [PubMed]
- Xing, D.; Chaudhary, A.K.; Miller, F.J., Jr.; Martins, J.B. Free radical scavenger specifically prevents ischemic focal ventricular tachycardia. Heart Rhythm 2009, 6, 530–536. [Google Scholar] [CrossRef] [PubMed]
- Cristofori, L.; Tavazzi, B.; Gambin, R.; Vagnozzi, R.; Vivenza, C.; Amorini, A.M.; di Pierro, D.; Fazzina, G.; Lazzarino, G. Early onset of lipid peroxidation after human traumatic brain injury: A fatal limitation for the free radical scavenger pharmacological therapy? J. Investig. Med. 2001, 49, 450–458. [Google Scholar] [CrossRef] [PubMed]
- PKC-DMES Study Group. Effect of ruboxistaurin in patients with diabetic macular edema: Thirty-month results of the randomized PKC-DMES clinical trial. Arch. Ophthalmol. 2007, 125, 318–324. [Google Scholar]
- PKC-DMES Study Group. The effect of ruboxistaurin on visual loss in patients with moderately severe to very severe nonproliferative diabetic retinopathy: Initial results of the Protein Kinase Cβ Inhibitor Diabetic Retinopathy Study (PKC-DRS) multicenter randomized clinical trial. Diabetes 2005, 54, 2188–2197. [Google Scholar]
- Herbst, R.S.; Oh, Y.; Wagle, A.; Lahn, M. Enzastaurin, a protein kinase Cβ-selective inhibitor, and its potential application as an anticancer agent in lung cancer. Clin. Cancer Res. 2007, 13, 4641–4646. [Google Scholar] [CrossRef] [PubMed]
- Bates, E.; Bode, C.; Costa, M.; Gibson, C.M.; Granger, C.; Green, C.; Grimes, K.; Harrington, R.; Huber, K.; Kleiman, N.; et al. Intracoronary KAI-9803 as an adjunct to primary percutaneous coronary intervention for acute ST-segment elevation myocardial infarction. Circulation 2008, 117, 886–896. [Google Scholar] [PubMed]
- Advani, R.; Peethambaram, P.; Lum, B.L.; Fisher, G.A.; Hartmann, L.; Long, H.J.; Halsey, J.; Holmlund, J.T.; Dorr, A.; Sikic, B.I. A Phase II trial of aprinocarsen, an antisense oligonucleotide inhibitor of protein kinase Cα, administered as a 21-day infusion to patients with advanced ovarian carcinoma. Cancer 2004, 100, 321–326. [Google Scholar] [CrossRef] [PubMed]
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Fei, Y.-D.; Li, W.; Hou, J.-W.; Guo, K.; Chen, X.-M.; Chen, Y.-H.; Wang, Q.; Xu, X.-L.; Wang, Y.-P.; Li, Y.-G. Oxidative Stress-Induced Afterdepolarizations and Protein Kinase C Signaling. Int. J. Mol. Sci. 2017, 18, 688. https://doi.org/10.3390/ijms18040688
Fei Y-D, Li W, Hou J-W, Guo K, Chen X-M, Chen Y-H, Wang Q, Xu X-L, Wang Y-P, Li Y-G. Oxidative Stress-Induced Afterdepolarizations and Protein Kinase C Signaling. International Journal of Molecular Sciences. 2017; 18(4):688. https://doi.org/10.3390/ijms18040688
Chicago/Turabian StyleFei, Yu-Dong, Wei Li, Jian-Wen Hou, Kai Guo, Xiao-Meng Chen, Yi-He Chen, Qian Wang, Xiao-Lei Xu, Yue-Peng Wang, and Yi-Gang Li. 2017. "Oxidative Stress-Induced Afterdepolarizations and Protein Kinase C Signaling" International Journal of Molecular Sciences 18, no. 4: 688. https://doi.org/10.3390/ijms18040688