Reactive oxygen species contribute to the development of arrhythmogenic Ca2+ waves during β-adrenergic receptor stimulation in rabbit cardiomyocytes

Journal of Physiology

Volumn 590, Issue 14, 2012, Pages 3291-3304

  Bovo, Elisa ^a   Lipsius, Stephen L ^a   Zima, Aleksey V ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ADRENERGIC RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; ISOPRENALINE; REACTIVE OXYGEN METABOLITE; ROTENONE; RYANODINE RECEPTOR; THIOL; TIRON;

ANIMAL CELL; ARTICLE; BETA ADRENERGIC STIMULATION; CALCIUM CURRENT; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DIASTOLE; HEART MUSCLE CELL; INOTROPISM; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RABBIT; SARCOPLASMIC RETICULUM; SYSTOLE;

ADRENERGIC BETA-AGONISTS; ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; CALCIUM SIGNALING; CARDIOTONIC AGENTS; CYTOSOL; HEART VENTRICLES; ISOPROTERENOL; MITOCHONDRIA; MYOCYTES, CARDIAC; OXIDATION-REDUCTION; PHOSPHORYLATION; RABBITS; REACTIVE OXYGEN SPECIES; RECEPTORS, ADRENERGIC, BETA; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM;

EID: 84864126936     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.230748     Document Type: Article

References (53)

1. Andersson DC, Fauconnier J, Yamada T, Lacampagne A, Zhang SJ, Katz A & Westerblad H (2011). Mitochondrial production of reactive oxygen species contributes to the β-adrenergic stimulation of mouse cardiomycytes. J Physiol 589, 1791-1801.
2. Aon MA, Cortassa S & O'Rourke B (2010). Redox-optimized ROS balance: a unifying hypothesis. Biochim Biophys Acta 1797, 865-877.
3. Belevych AE, Terentyev D, Terentyeva R, Nishijima Y, Sridhar A, Hamlin RL, Carnes CA & Gyorke S (2011). The relationship between arrhythmogenesis and impaired contractility in heart failure: role of altered ryanodine receptor function. Cardiovasc Res 90, 493-502.
4. Bers DM (2001). Excitation-Contraction Coupling and Cardiac Contractile Force. Kluwer Academic Publishers, Dordrecht .
5. 2+ in rabbit ventricular myocytes. J Physiol 589, 6039-6050.
6. Bovo E, Mazurek SR, Lipsius SL & Zima AV (2011b). β-Adrenergic receptor stimulation of ROS production generates spontaneous Ca waves in rabbit ventricular myocytes. Biophys J 100, 559a-560a. Ref Type: Abstract
7. 2+ reuptake in rat ventricular myocytes. Proc Natl Acad Sci U S A 85, 2009-2013.
8. i during excitation-contraction coupling in cardiac myocytes. Biophys J 67, 1942-1956.
9. Communal C, Singh K, Pimentel DR & Colucci WS (1998). Norepinephrine stimulates apoptosis in adult rat ventricular myocytes by activation of the β-adrenergic pathway. Circulation 98, 1329-1334.
10. Csordas G, Thomas AP & Hajnoczky G (2001). Calcium signal transmission between ryanodine receptors and mitochondria in cardiac muscle. Trends Cardiovasc Med 11, 269-275.
11. 2+-calmodulin-dependent protein kinase II. J Mol Cell Cardiol 49, 25-32.
12. Curran J, Hinton MJ, Rios E, Bers DM & Shannon TR (2007). β-Adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circ Res 100, 391-398.
13. 2+ release termination by ryanodine receptor sensitization and in heart failure. J Physiol 587, 5197-5209.
14. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
15. Dzimiri N (1999). Regulation of β-adrenoceptor signaling in cardiac function and disease. Pharmacol Rev 51, 465-501.
16. Ellison GM, Torella D, Karakikes I, Purushothaman S, Curcio A, Gasparri C et al . (2007). Acute β-adrenergic overload produces myocyte damage through calcium leakage from the ryanodine receptor 2 but spares cardiac stem cells. J Biol Chem 282, 11397-11409.
17. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV et al . (2008). A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133, 462-474.
18. 2+ release kinetics during β-adrenergic stimulation. J Mol Cell Cardiol 43, 281-291.
19. 2+ current trigger. J Physiol 556, 463-480.
20. Ho HT, Stevens SC, Terentyeva R, Carnes CA, Terentyev D & Gyorke S (2011). Arrhythmogenic adverse effects of cardiac glycosides are mediated by redox modification of ryanodine receptors. J Physiol 589, 4697-4708.
21. Huke S & Bers DM (2008). Ryanodine receptor phosphorylation at Serine 2030, 2808 and 2814 in rat cardiomyocytes. Biochem Biophys Res Commun 376, 80-85.
22. 2+ transient in rat myocytes during β-adrenergic stimulation. J Physiol 505, 385-402.
23. Katra RP, Oya T, Hoeker GS & Laurita KR (2007). Ryanodine receptor dysfunction and triggered activity in the heart. Am J Physiol Heart Circ Physiol 292, H2144-H2151.
24. + increases mitochondrial formation of reactive oxygen species in failing cardiac myocytes. Circulation 121, 1606-1613.
25. Kosower NS & Kosower EM (1987). Thiol labeling with bromobimanes. Methods Enzymol 143, 76-84.
26. Kourie JI (1998). Interaction of reactive oxygen species with ion transport mechanisms. Am J Physiol Cell Physiol 275, C1-C24.
27. Liu G, Abramson JJ, Zable AC & Pessah IN (1994). Direct evidence for the existence and functional role of hyperreactive sulfhydryls on the ryanodine receptor-triadin complex selectively labeled by the coumarin maleimide 7-diethylamino-3-(4′-maleimidylphenyl)-4-methylcoumarin. Mol Pharmacol 45, 189-200.
28. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N & Marks AR (2000). PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101, 365-376.
29. 2+ leak in mouse heart. Biochem Biophys Res Commun 390, 87-92.
30. Nagasaka S, Katoh H, Niu CF, Matsui S, Urushida T, Satoh H, Watanabe Y & Hayashi H (2007). Protein kinase A catalytic subunit alters cardiac mitochondrial redox state and membrane potential via the formation of reactive oxygen species. Circ J 71, 429-436.
31. Nam GB, Burashnikov A & Antzelevitch C (2005). Cellular mechanisms underlying the development of catecholaminergic ventricular tachycardia. Circulation 111, 2727-2733.
32. 2+ release in cardiomyocytes during β-adrenergic stimulation. J Physiol 588, 225-242.
33. Opie LH, Thandroyen FT, Muller C & Bricknell OL (1979). Adrenaline-induced 'oxygen-wastage' and enzyme release from working rat heart. Effects of calcium antagonism, β-blockade, nicotinic acid and coronary artery ligation. J Mol Cell Cardiol 11, 1073-1094.
34. Remondino A, Kwon SH, Communal C, Pimentel DR, Sawyer DB, Singh K & Colucci WS (2003). β-Adrenergic receptor-stimulated apoptosis in cardiac myocytes is mediated by reactive oxygen species/c-Jun NH2-terminal kinase-dependent activation of the mitochondrial pathway. Circ Res 92, 136-138.
35. Rockman HA, Koch WJ & Lefkowitz RJ (2002). Seven-transmembrane-spanning receptors and heart function. Nature 415, 206-212.
36. 2+ release causes myocyte depolarization. Underlying mechanism and threshold for triggered action potentials. Circ Res 87, 774-780.
37. Shannon TR, Ginsburg KS & Bers DM (2000). Reverse mode of the sarcoplasmic reticulum calcium pump and load-dependent cytosolic calcium decline in voltage-clamped cardiac ventricular myocytes. Biophys J 78, 322-333.
38. 2+ leak-load relationship. Circ Res 91, 594-600.
39. 2+ release during excitation-contraction coupling in cardiac myocytes. Circ Res 88, 794-801.
40. Srivastava S, Chandrasekar B, Gu Y, Luo J, Hamid T, Hill BG & Prabhu SD (2007). Downregulation of CuZn-superoxide dismutase contributes to β-adrenergic receptor-mediated oxidative stress in the heart. Cardiovasc Res 74, 445-455.
41. 2+ leak in chronic heart failure. Circ Res 103, 1466-1472.
42. Turrens JF (2003). Mitochondrial formation of reactive oxygen species. J Physiol 552, 335-344.
43. van Oort RJ, McCauley MD, Dixit SS, Pereira L, Yang Y, Respress JL et al . (2010). Ryanodine receptor phosphorylation by calcium/calmodulin-dependent protein kinase II promotes life-threatening ventricular arrhythmias in mice with heart failure. Circulation 122, 2669-2679.
44. Venetucci LA, Trafford AW & Eisner DA (2007). Increasing ryanodine receptor open probability alone does not produce arrhythmogenic calcium waves: threshold sarcoplasmic reticulum calcium content is required. Circ Res 100, 105-111.
45. 2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 94, e61-e70.
46. Wehrens XH, Lehnart SE, Reiken S, Vest JA, Wronska A & Marks AR (2006). Ryanodine receptor/calcium release channel PKA phosphorylation: a critical mediator of heart failure progression. Proc Natl Acad Sci U S A 103, 511-518.
47. Xu L, Eu JP, Meissner G & Stamler JS (1998). Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279, 234-237.
48. 2+ sparks by mitochondria-derived reactive oxygen species in cardiac myocytes. Cardiovasc Res 77, 432-441.
49. Yoshida A, Takahashi M, Imagawa T, Shigekawa M, Takisawa H & Nakamura T (1992). Phosphorylation of ryanodine receptors in rat myocytes during β-adrenergic stimulation. J Biochem 111, 186-190.
50. Zhang GX, Kimura S, Nishiyama A, Shokoji T, Rahman M, Yao L et al . (2005). Cardiac oxidative stress in acute and chronic isoproterenol-infused rats. Cardiovasc Res 65, 230-238.
51. Zima AV & Blatter LA (2006). Redox regulation of cardiac calcium channels and transporters. Cardiovasc Res 71, 310-321.
52. 2+ leak in normal and failing rabbit ventricular myocytes. J Physiol 588, 4743-4757.
53. 2+ diffusion. Circ Res 103, e105-e115.