Redox modification of ryanodine receptors by mitochondria-derived reactive oxygen species contributes to aberrant Ca2+ handling in ageing rabbit hearts

Journal of Physiology

Volumn 591, Issue 23, 2013, Pages 5895-5911

  Cooper, Leroy L ^a   Li, Weiyan ^a   Lu, Yichun ^a   Centracchio, Jason ^a   Terentyeva, Radmila ^a   Koren, Gideon ^a   Terentyev, Dmitry ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; FLUORESCENT DYE; REACTIVE OXYGEN METABOLITE; RYANODINE RECEPTOR;

ABERRANT CALCIUM HANDLING; AGING; ANIMAL CELL; ARTICLE; BETA ADRENERGIC STIMULATION; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL ISOLATION; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE PERMEABILITY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; FEMALE; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION REDUCTION STATE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RABBIT; SARCOPLASMIC RETICULUM; SENSITIVITY ANALYSIS;

AGING; ANIMALS; CALCIUM; FEMALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; OXIDATION-REDUCTION; RABBITS; REACTIVE OXYGEN SPECIES; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84888433466     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.260521     Document Type: Article

References (63)

1. Belevych A, Kubalova Z, Terentyev D, Hamlin RL, Carnes CA & Györke S (2007). Enhanced ryanodine receptor-mediated calcium leak determines reduced sarcoplasmic reticulum calcium content in chronic canine heart failure. Biophys J 93, 4083-4092.
2. Belevych AE, Sansom SE, Terentyeva R, Ho HT, Nishijima Y, Martin MM, Jindal HK, Rochira JA, Kunitomo Y, Abdellatif M, Carnes CA, Elton TS, Györke S & Terentyev D (2011a). MicroRNA-1 and -133 increase arrhythmogenesis in heart failure by dissociating phosphatase activity from RyR2 complex. PloS One 6, e28324.
3. 2+ signaling refractoriness underlies cellular arrhythmogenesis in a postinfarction model of sudden cardiac death. Circ Res 110, 569-577.
4. Belevych AE, Terentyev D, Terentyeva R, Nishijima Y, Sridhar A, Hamlin RL, Carnes CA & Györke S (2011b). The relationship between arrhythmogenesis and impaired contractility in heart failure: role of altered ryanodine receptor function. Cardiovasc Res 90, 493-502.
5. Belevych AE, Terentyev D, Viatchenko-Karpinski S, Terentyeva R, Sridhar A, Nishijima Y, Wilson LD, Cardounel AJ, Laurita KR, Carnes CA, Billman GE & Györke S (2009). Redox modification of ryanodine receptors underlies calcium alternans in a canine model of sudden cardiac death. Cardiovasc Res 84, 387-395.
6. Bers DM, Pogwizd SM & Schlotthauer K (2002). Upregulated Na/Ca exchange is involved in both contractile dysfunction and arrhythmogenesis in heart failure. Basic Res Cardiol 97 (Suppl. 1), I36-42.
7. 2+ waves during β-adrenergic receptor stimulation in rabbit cardiomyocytes. J Physiol 590, 3291-3304.
8. Brown DA, Aon MA, Frasier CR, Sloan RC, Maloney AH, Anderson EJ & O'Rourke B (2010). Cardiac arrhythmias induced by glutathione oxidation can be inhibited by preventing mitochondrial depolarization. J Mol Cell Cardiol 48, 673-679.
9. Brown DA & O'Rourke B (2010). Cardiac mitochondria and arrhythmias. Cardiovasc Res 88, 241-249.
10. Brunner M, Peng X, Liu GX, Ren XQ, Ziv O, Choi BR, Mathur R, Hajjiri M, Odening KE, Steinberg E, Folco EJ, Pringa E, Centracchio J, Macharzina RR, Donahay T, Schofield L, Rana N, Kirk M, Mitchell GF, Poppas A, Zehender M & Koren G (2008). Mechanisms of cardiac arrhythmias and sudden death in transgenic rabbits with long QT syndrome. J Clin Invest 118, 2246-2259.
11. Cerbai E, Guerra L, Varani K, Barbieri M, Borea PA & Mugelli A (1995). Beta-adrenoceptor subtypes in young and old rat ventricular myocytes: a combined patch-clamp and binding study. Br J Pharmacol 116, 1835-1842.
12. Chaudhary KR, El-Sikhry H & Seubert JM (2011). Mitochondria and the aging heart. J Geriatr Cardiol 8, 159-167.
13. Cooper LL, Odening KE, Hwang MS, Chaves L, Schofield L, Taylor CA, Gemignani AS, Mitchell GF, Forder JR, Choi BR & Koren G (2012). Electromechanical and structural alterations in the aging rabbit heart and aorta. Am J Physiol Heart Circ Physiol 302, H1625-H1635.
14. Dibb KM, Rueckschloss U, Eisner DA, Isenberg G & Trafford AW (2004). Mechanisms underlying enhanced cardiac excitation contraction coupling observed in the senescent sheep myocardium. J Mol Cell Cardiol 37, 1171-1181.
15. Donoso P, Sanchez G, Bull R & Hidalgo C (2011). Modulation of cardiac ryanodine receptor activity by ROS and RNS. Front Biosci (Landmark Ed) 16, 553-567.
16. 2+-release channels from sheep myocardium. Am J Physiol Cell Physiol 272, C1908-C1918.
17. 2+ exchanger in hypoxic reoxygenated guinea pig ventricular myocytes. Am J Physiol Heart Circ Physiol 286, H955-H963.
18. Eisner D, Bode E, Venetucci L & Trafford A (2013). Calcium flux balance in the heart. J Mol Cell Cardiol 58, 110-117.
19. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O'Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ & Anderson ME (2008). A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133, 462-474.
20. Giordano FJ (2005). Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115, 500-508.
21. Gonzalez DR, Beigi F, Treuer AV & Hare JM (2007). Deficient ryanodine receptor S-nitrosylation increases sarcoplasmic reticulum calcium leak and arrhythmogenesis in cardiomyocytes. Proc Natl Acad Sci U S A 104, 20612-20617.
22. Grivennikova VG, Kareyeva AV & Vinogradov AD (2010). What are the sources of hydrogen peroxide production by heart mitochondria Biochim Biophys Acta 1797, 939-944.
23. 2+/calmodulin-dependent protein kinase II phosphorylation of ryanodine receptor does affect calcium sparks in mouse ventricular myocytes. Circ Res 99, 398-406.
24. Györke S & Carnes C (2008). Dysregulated sarcoplasmic reticulum calcium release: Potential pharmacological target in cardiac disease. Pharmacol Ther 119, 340-354.
25. Haarmann CS, Fink RH & Dulhunty AF (1999). Oxidation and reduction of pig skeletal muscle ryanodine receptors. Biophys J 77, 3010-3022.
26. Harman D (1972). The biologic clock: the mitochondria J Am Geriatr Soc 20, 145-147.
27. Ho HT, Stevens SC, Terentyeva R, Carnes CA, Terentyev D & Györke S (2011). Arrhythmogenic adverse effects of cardiac glycosides are mediated by redox modification of ryanodine receptors. J Physiol 589, 4697-46708.
28. Howlett SE (2010). Age-associated changes in excitation-contraction coupling are more prominent in ventricular myocytes from male rats than in myocytes from female rats. Am J Physiol Heart Circ Physiol 298, H659-H670.
29. 2+ cycling in systolic and diastolic heart failure associated with aging. Heart Fail Rev 15, 431-445.
30. Johnson-Cadwell LI, Jekabsons MB, Wang A, Polster BM & Nicholls DG (2007). 'Mild Uncoupling' does not decrease mitochondrial superoxide levels in cultured cerebellar granule neurons but decreases spare respiratory capacity and increases toxicity to glutamate and oxidative stress. J Neurochem 101, 1619-1631.
31. Kannel WB, Cupples LA & Dagostino RB (1987). Sudden death risk in overt coronary heart disease - the Framingham Study. Am Heart J 113, 799-804.
32. 2+ release, and catecholaminergic polymorphic ventricular tachycardia. J Clin Invest 116, 2510-2520.
33. 2+ depletion in cardiac myocytes. Free Radic Biol Med 48, 1182-1187.
34. Lakatta EG (1993). Cardiovascular regulatory mechanisms in advanced age. Physiol Rev 73, 413-467.
35. Lakatta EG & Sollott SJ (2002). Perspectives on mammalian cardiovascular aging: humans to molecules. Comp Biochem Physiol A Mol Integr Physiol 132, 699-721.
36. Lancel S, Qin F, Lennon SL, Zhang J, Tong X, Mazzini MJ, Kang YJ, Siwik DA, Cohen RA & Colucci WS (2010). Oxidative posttranslational modifications mediate decreased SERCA activity and myocyte dysfunction in Gαq-overexpressing mice. Circ Res 107, 228-232.
37. 2+ uptake into the sarcoplasmic reticulum. Circ Res 89, 614-622.
38. Miquel J, Economos AC, Fleming J & Johnson JE (1980). Mitochondrial role in cell aging. Exp Gerontol 15, 575-591.
39. 2+ leak via stabilization of ryanodine receptor in heart failure. J Am Coll Cardiol 49, 1722-1732.
40. Morita N, Sovari AA, Xie Y, Fishbein MC, Mandel WJ, Garfinkel A, Lin SF, Chen PS, Xie LH, Chen F, Qu Z, Weiss JN & Karagueuzian HS (2009). Increased susceptibility of aged hearts to ventricular fibrillation during oxidative stress. Am J Physiol Heart Circ Physiol 297, H1594-H1605.
41. 2+ signaling and EC-coupling. Biochim Biophys Acta 1833, 866-875.
42. O'Rourke B, Ramza BM & Marban E (1994). Oscillations of membrane current and excitability driven by metabolic oscillations in heart cells. Science 265, 962-966.
43. Pogwizd SM & Bers DM (2002). Na/Ca exchange in heart failure - Contractile dysfunction and arrhythmogenesis. Ann N Y Acad Sci 976, 454-465.
44. 2+ sequestration. Ann N Y Acad Sci 853, 341-344.
45. Rodriguez P, Bhogal MS & Colyer J (2003). Stoichiometric phosphorylation of cardiac ryanodine receptor on serine 2809 by calmodulin-dependent kinase II and protein kinase A. J Biol Chem 278, 38593-38600.
46. Sanchez G, Pedrozo Z, Domenech RJ, Hidalgo C & Donoso P (2005). Tachycardia increases NADPH oxidase activity and RyR2 S-glutathionylation in ventricular muscle. J Mol Cell Cardiol 39, 982-991.
47. Shabalina IG & Nedergaard J (2011). Mitochondrial ('mild') uncoupling and ROS production: physiologically relevant or not Biochem Soc Trans 39, 1305-1309.
48. 2+ reserve. Circ Res 93, 40-45.
49. Squier TC (2001). Oxidative stress and protein aggregation during biological aging. Exp Gerontol 36, 1539-1550.
50. 2 tension and S-nitrosoglutathione. Biochemistry 47, 13985-13990.
51. Szalai G, Csordas G, Hantash BM, Thomas AP & Hajnoczky G (2000). Calcium signal transmission between ryanodine receptors and mitochondria. J Biol Chem 275, 15305-15313.
52. 2+ leak in chronic heart failure. Circ Res 103, 1466-1472.
53. 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.
54. 2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor. Circ Res 94, e61-70.
55. Witcher DR, Kovacs RJ, Schulman H, Cefali DC & Jones LR (1991). Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J Biol Chem 266, 11144-11152.
56. Xiao BL, Zhong GF, Obayashi M, Yang DM, Chen KY, Walsh MP, Shimoni Y, Cheng HP, ter Keurs H & Chen SRW (2006). Ser-2030, but not Ser-2808, is the major phosphorylation site in cardiac ryanodine receptors responding to protein kinase A activation upon β-adrenergic stimulation in normal and failing hearts. Biochem J 396, 7-16.
57. Xiao RP, Spurgeon HA, O'Connor F & Lakatta EG (1994). Age-associated changes in β-adrenergic modulation on rat cardiac excitation-contraction coupling. J Clin Invest 94, 2051-2059.
58. 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.
59. 2+ release mechanism. J Biol Chem 272, 7069-7077.
60. Zeng Q, Zhou Q, Yao F, O'Rourke ST & Sun C (2008). Endothelin-1 regulates cardiac L-type calcium channels via NAD(P)H oxidase-derived superoxide. J Pharmacol Exp Ther 326, 732-738.
61. 2+ sparks by mitochondrial oscillations in isolated guinea pig cardiomyocytes under oxidative stress. J Mol Cell Cardiol 51, 632-639.
62. 2+ sparks and gating properties of ryanodine receptors in aging cardiomyocytes. Cell Calcium 37, 583-591.
63. Zima AV & Blatter LA (2006). Redox regulation of cardiac calcium channels and transporters. Cardiovasc Res 71, 310-321.