Stimulation of NOX2 in isolated hearts reversibly sensitizes RyR2 channels to activation by cytoplasmic calcium

Journal of Molecular and Cellular Cardiology

Volumn 68, Issue , 2014, Pages 38-46

  Donoso, Paulina ^a   Finkelstein, José Pablo ^a   Montecinos, Luis ^a   Said, Matilde ^a   Sánchez, Gina ^b   Vittone, Leticia ^a   Bull, Ricardo ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSIDAD NACIONAL DE LA PLATA   (Argentina)

Author keywords

Ca2+ induced Ca2+ release; Ischemia reperfusion; Preconditioning; Redox signaling; Single channel

Indexed keywords

CA(2+)-INDUCED CA(2+) RELEASE; ISCHEMIA/REPERFUSION; PRECONDITIONING; REDOX SIGNALING; SINGLE CHANNEL;

ANIMALS; CALCIUM SIGNALING; HEART VENTRICLES; ION CHANNEL GATING; KINETICS; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM;

EID: 84894232511     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.12.028     Document Type: Article

References (40)

1. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
2. Voss A.A., Lango J., Ernst-Russell M., Morin D., Pessah I.N. Identification of hyperreactive cysteines within ryanodine receptor type 1 by mass spectrometry. J Biol Chem 2004, 279:34514-34520.
3. Aracena-Parks P., Goonasekera S.A., Gilman C.P., Dirksen R.T., Hidalgo C., Hamilton S.L. Identification of cysteines involved in S-nitrosylation, S-glutathionylation, and oxidation to disulfides in ryanodine receptor type 1. J Biol Chem 2006, 281:40354-40368.
4. Donoso P., Sanchez G., Bull R., Hidalgo C. Modulation of cardiac ryanodine receptor activity by ROS and RNS. Front Biosci 2011, 16:553-567.
5. 2+ release in muscle and neurons. Biol Res 2004, 37:539-552.
6. Zima A.V., Blatter L.A. Redox regulation of cardiac calcium channels and transporters. Cardiovasc Res 2006, 71:310-321.
7. Tian C., Shao C.H., Moore C.J., Kutty S., Walseth T., DeSouza C., et al. Gain of function of cardiac ryanodine receptor in a rat model of type 1 diabetes. Cardiovasc Res 2011, 91:300-309.
8. Turan B., Vassort G. Ryanodine receptor: a new therapeutic target to control diabetic cardiomyopathy. Antioxid Redox Signal 2011, 15:1847-1861.
9. Yano M., Okuda S., Oda T., Tokuhisa T., Tateishi H., Mochizuki M., et al. Correction of defective interdomain interaction within ryanodine receptor by antioxidant is a new therapeutic strategy against heart failure. Circulation 2005, 112:3633-3643.
10. Gonzalez D.R., Treuer A.V., Castellanos J., Dulce R.A., Hare J.M. Impaired S-nitrosylation of the ryanodine receptor caused by xanthine oxidase activity contributes to calcium leak in heart failure. J Biol Chem 2010, 285:28938-28945.
11. 2+ leak in chronic heart failure. Circ Res 2008, 103:1466-1472.
12. Belevych A.E., Terentyev D., Viatchenko-Karpinski S., Terentyeva R., Sridhar A., Nishijima Y., et al. Redox modification of ryanodine receptors underlies calcium alternans in a canine model of sudden cardiac death. Cardiovasc Res 2009, 84:387-395.
13. Sanchez G., Escobar M., Pedrozo Z., Macho P., Domenech R., Hartel S., et al. Exercise and tachycardia increase NADPH oxidase and ryanodine receptor-2 activity: possible role in cardioprotection. Cardiovasc Res 2008, 77:380-386.
14. Sanchez G., Pedrozo Z., Domenech R.J., Hidalgo C., Donoso P. Tachycardia increases NADPH oxidase activity and RyR2 S-glutathionylation in ventricular muscle. J Mol Cell Cardiol 2005, 39:982-991.
15. Prosser B.L., Ward C.W., Lederer W.J. X-ROS signaling: rapid mechano-chemo transduction in heart. Science 2011, 333:1440-1445.
16. Prosser B.L., Ward C.W., Lederer W.J. X-ROS signalling is enhanced and graded by cyclic cardiomyocyte stretch. Cardiovasc Res 2013, 98:307-314.
17. Marengo J.J., Bull R., Hidalgo C. Calcium dependence of ryanodine-sensitive calcium channels from brain cortex endoplasmic reticulum. FEBS Lett 1996, 383:59-62.
18. 2+ dependence of RyR channels from rat brain cortex. Am J Physiol Cell Physiol 2007, 293:C162-C171.
19. 2+ and redox modification of ryanodine receptor channels from rat brain cortex. J Neurosci 2008, 28:9463-9472.
20. Marengo J.J., Hidalgo C., Bull R. Sulfhydryl oxidation modifies the calcium dependence of ryanodine-sensitive calcium channels of excitable cells. Biophys J 1998, 74:1263-1277.
21. McManus T., Sadgrove M., Pringle A.K., Chad J.E., Sundstrom L.E. Intraischaemic hypothermia reduces free radical production and protects against ischaemic insults in cultured hippocampal slices. J Neurochem 2004, 91:327-336.
22. Blomgren K., Hagberg H. Free radicals, mitochondria, and hypoxia-ischemia in the developing brain. Free Radic Biol Med 2006, 40:388-397.
23. Zweier J.L., Talukder M.A. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 2006, 70:181-190.
24. Bull R., Marengo J.J., Finkelstein J.P., Behrens M.I., Alvarez O. SH oxidation coordinates subunits of rat brain ryanodine receptor channels activated by calcium and ATP. Am J Physiol Cell Physiol 2003, 285:C119-C128.
25. Sanchez G., Hidalgo C., Donoso P. Kinetic studies of calcium-induced calcium release in cardiac sarcoplasmic reticulum vesicles. Biophys J 2003, 84:2319-2330.
26. 2+) inhibition of calcium-induced calcium release in skeletal muscle triads. Biophys J 2000, 79:279-286.
27. van Oort R.J., McCauley M.D., Dixit S.S., Pereira L., Yang Y., Respress J.L., et al. Ryanodine receptor phosphorylation by calcium/calmodulin-dependent protein kinase II promotes life-threatening ventricular arrhythmias in mice with heart failure. Circulation 2010, 122:2669-2679.
28. 2+ activation of RyR1 channels. J Biol Chem 2003, 278:42927-42935.
29. Chen W., Gabel S., Steenbergen C., Murphy E. A redox-based mechanism for cardioprotection induced by ischemic preconditioning in perfused rat heart. Circ Res 1995, 77:424-429.
30. Vanden Hoek T.L., Becker L.B., Shao Z., Li C., Schumacker P.T. Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem 1998, 273:18092-18098.
31. Forbes R.A., Steenbergen C., Murphy E. Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res 2001, 88:802-809.
32. Dost T., Cohen M.V., Downey J.M. Redox signaling triggers protection during the reperfusion rather than the ischemic phase of preconditioning. Basic Res Cardiol 2008, 103:378-384.
33. Bell R.M., Cave A.C., Johar S., Hearse D.J., Shah A.M., Shattock M.J. Pivotal role of NOX-2-containing NADPH oxidase in early ischemic preconditioning. FASEB J 2005, 19:2037-2039.
34. 2+ flux measurements of the cardiac sarcoplasmic reticulum calcium channel. Biophys J 1986, 50:1009-1014.
35. 2+ release channel complex. J Biol Chem 1989, 264:1329-1335.
36. 2+ release is observed in native vesicles. J Membr Biol 1993, 135:49-59.
37. Holmberg S.R., Williams A.J. The cardiac sarcoplasmic reticulum calcium-release channel: modulation of ryanodine binding and single-channel activity. Biochim Biophys Acta 1990, 1022:187-193.
38. 2+ inactivation of canine reconstituted cardiac sarcoplasmic reticulum Ca(2+)-release channels. J Physiol 1995, 489(Pt 2):337-348.
39. 2+ inhibits the ryanodine receptor from cardiac muscle. J Membr Biol 1995, 147:7-22.
40. Rebrin I., Kamzalov S., Sohal R.S. Effects of age and caloric restriction on glutathione redox state in mice. Free Radic Biol Med 2003, 35:626-635.