Role of oxidants on calcium and sodium movement in healthy and diseased cardiac myocytes

Free Radical Biology and Medicine

Volumn 63, Issue , 2013, Pages 338-349

  Sag, Can M ^a,b   Wagner, Stefan ^b   Maier, Lars S ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Ca handling; Calcium; CaMKII; Coupling; Exciation contraction; Late Na current; ROS; Sodium; SR Ca leak

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; OXIDOREDUCTASE; PROTEIN KINASE; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RYANODINE RECEPTOR 2; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM; SODIUM CALCIUM EXCHANGE PROTEIN;

CALCIUM TRANSPORT; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; ENZYME ACTIVATION; EXCITATION CONTRACTION COUPLING; HEART ARRHYTHMIA; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SCAVENGING SYSTEM; SIGNAL TRANSDUCTION; SODIUM TRANSPORT;

EID: 84879478027     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.05.035     Document Type: Review

References (170)

1. Bers, D. M.; Despa, S.; Bossuyt, J. Regulation of Ca2+ and Na+ in normal and failing cardiac myocytes. Ann. N. Y. Acad. Sci. 1080: 165-177; 2006. (Pubitemid 44955421)
2. Lehnart, S. E.; Maier, L. S.; Hasenfuss, G. Abnormalities of calcium metabolism and myocardial contractility depression in the failing heart. Heart Fail. Rev 14: 213-224; 2009.
3. Maier, L. S.; Zhang, T.; Chen, L.; DeSantiago, J.; Brown, J. H.; Bers, D. M. Transgenic CaMKIIdeltaC overexpression uniquely alters cardiac myocyte Ca2+ handling: reduced SR Ca2+ load and activated SR Ca2+ release. Circ. Res 92: 904-911; 2003. (Pubitemid 36542532)
4. Wehrens, X. H.; Lehnart, S. E.; Reiken, S.; Vest, J. A.; Wronska, A.; Marks, A. R. Ryanodine receptor/calcium release channel PKA phosphorylation: a critical mediator of heart failure progression. Proc. Natl. Acad. Sci. USA 103: 511-518; 2006. (Pubitemid 43153055)
5. Maack, C.; Kartes, T.; Kilter, H.; Schäfers, H. J.; Nickenig, G.; Böhm, M.; Laufs, U. Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment. Circulation 108: 1567-1574; 2003. (Pubitemid 37187782)
6. Sag, C. M.; Köhler, A. C.; Anderson, M. E.; Backs, J.; Maier, L. S.; CaMKII-dependent, S. R. Ca leak contributes to doxorubicin-induced impaired Ca handling in isolated cardiac myocytes. J. Mol. Cell. Cardiol 51: 749 -759; 2011.
7. Wagner, S.; Ruff, H. M.; Weber, S. L.; Bellmann, S.; Sowa, T.; Schulte, T.; Anderson, M. E.; Grandi, E.; Bers, D. M.; Backs, J.; Belardinelli, L.; Maier, L. S. Reactive oxygen species-activated Ca/calmodulin kinase IId is required for late INa augmentation leading to cellular Na and Ca overload. Circ. Res 108: 555-565; 2011.
8. Zima, A. V.; Blatter, L. A. Redox regulation of cardiac calcium channels and transporters. Cardiovasc. Res 71: 310-321; 2006.
9. Santos, C. X.; Anilkumar, N.; Zhang, M.; Brewer, A. C.; Shah, A. M. Redox signaling in cardiac myocytes. Free Radic. Biol. Med. 50: 777-793; 2011.
10. Burgoyne, J. R.; Mongue-Din, H.; Eaton, P.; Shah, A. M. Redox signaling in cardiac physiology and pathology. Circ. Res 111 : 1091-1106; 2012.
11. Kohlhaas, M.; Maack, C. Interplay of defective excitation-contraction coupling, energy starvation, and oxidative stress in heart failure. Trends Cardi-ovasc. Med 21: 69-73; 2011.
12. Terentyev, D.; Györke, I.; Belevych, A. E.; Terentyeva, R.; Sridhar, A.; Nishijima, Y. de Blanco EC; Khanna S; Sen CK; Cardounel AJ; Carnes CA; Györke S. Redox modification of ryanodine receptors contributes to sarco-plasmic reticulum Ca2+ leak in chronic heart failure. Circ. Res 103: 1466-1472; 2008.
13. Bers, D. M. Calcium cycling and signaling in cardiac myocytes. Annu. Rev. Physiol. 70: 23-49; 2008. (Pubitemid 351738170)
14. Sossalla, S.; Fluschnik, N.; Schotola, H.; Ort, K. R.; Neef, S.; Schulte, T.; Wittköpper, K.; Renner, A.; Schmitto, J. D.; Gummert, J.; El-Armouche, A.; Hasenfuss, G.; Maier, L. S. Inhibition of elevated Ca2+/calmodulin- dependent protein kinase II improves contractility in human failing myocardium. Circ. Res 107: 115 0 -1161 ; 2010 .
15. Hobai, I. A.; O'Rourke, B. Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation 103: 1577-1584; 2001. (Pubitemid 32226268)
16. Sossalla, S.; Wagner, S.; Rasenack, E. C.; Ruff, H.; Weber, S. L.; Schöndube, F. A.; Tirilomis, T.; Tenderich, G.; Hasenfuss, G.; Belardinelli, L.; Maier, L. S. Ranolazine improves diastolic dysfunction in isolated myocardium from failing human hearts - role of late sodium current and intracellular ion accumulation. J. Mol. Cell. Cardiol 45: 32-43; 2008.
17. Zhu, W. Z.; Wang, S. Q.; Chakir, K.; Yang, D.; Zhang, T.; Brown, J. H.; Devic, E.; Kobilka, B. K.; Cheng, H.; Xiao, R. P. Linkage of beta1-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2+/calmodulin kinase II. J. Clin. Invest 111 : 617-625; 2003. (Pubitemid 36278580)
18. Wagner, S.; Dybkova, N.; Rasenack, E. C. L.; Jacobshagen, C.; Fabritz, L.; Kirchhof, P.; Maier, S. K. G.; Zhang, T.; Hasenfuss, G.; Brown, J. H.; Bers, D. M.; Maier, L. S. Ca2+/calmodulin-dependent protein kinase II regulates cardiac Na+ channels. J. Clin. Invest 116 : 3127-3138; 2006. (Pubitemid 44878627)
19. Baartscheer, A.; Schumacher, C. A.; van Borren, M. M.; Belterman, C. N.; Coronel, R.; Fiolet, J. W. Increased Na+/H+-exchange activity is the cause of increased [Na+]i and underlies disturbed calcium handling in the rabbit pressure and volume overload heart failure model. Cardiovasc. Res 57: 1015-1024; 2003. (Pubitemid 36324606)
20. Baartscheer, A.; Schumacher, C. A.; van Borren, M. M.; Belterman, C. N.; Coronel, R.; Opthof, T.; Fiolet, J. W. Chronic inhibition of Na+/H+-exchanger attenuates cardiac hypertrophy and prevents cellular remodeling in heart failure. Cardiovasc. Res 65: 83-92; 2005. (Pubitemid 40038481)
21. Pieske, B.; Maier, L. S.; Piacentino 3rd V.; Weisser, J.; Hasenfuss, G.; Houser, S. Rate dependence of [Na+]i and contractility in nonfailing and failing human myocardium. Circulation 106: 447-453; 2002. (Pubitemid 34803689)
22. Armoundas, A. A.; Hobai, I. A.; Tomaselli, G. F.; Winslow, R. L.; O'Rourke, B. Role of sodium-calcium exchanger in modulating the action potential of ventricular myocytes from normal and failing hearts. Circ. Res 93: 46-53; 2003. (Pubitemid 36859040)
23. Baartscheer, A.; Schumacher, C. A.; Belterman, C. N.; Coronel, R.; Fiolet, J. W. [Na+]i and the driving force of the Na+/Ca2+-exchanger in heart failure. Cardiovasc. Res 57: 986-995; 2003.
24. Piacentino 3rd V.; Weber, C. R.; Chen, X.; Weisser-Thomas, J.; Margulies, K. B.; Bers, D. M.; Houser, S. R. Cellular basis of abnormal calcium transients of failing human ventricular myocytes. Circ. Res 92: 651-658; 2003. (Pubitemid 36417700)
25. Weber, C. R.; Piacentino 3rd V.; Houser, S. R.; Bers, D. M. Dynamic regulation of sodium/calcium exchange function in human heart failure. Circulation 108: 2224-2229; 2003. (Pubitemid 37363039)
26. Weisser-Thomas, J.; Piacentino 3rd V.; Gaughan, J. P.; Margulies, K.; Houser, S. R. Calcium entry via Na/Ca exchange during the action potential directly contributes to contraction of failing human ventricular myocytes. Cardiovasc. Res 57: 974-985; 2003. (Pubitemid 36324602)
27. Wagner, S.; Seidler, T.; Picht, E.; Maier, L. S.; Kazanski, V.; Teucher, N.; Schillinger, W.; Pieske, B.; Isenberg, G.; Hasenfuss, G.; Kögler, H. Na+/Ca2+ exchanger overexpression predisposes to reactive oxygen species-induced injury. Cardiovasc. Res 60: 404-412; 2003. (Pubitemid 37412374)
28. Dipla, K.; Mattiello, J. A.; Margulies, K. B.; Jeevanandam, V.; Houser, S. R. The sarcoplasmic reticulum and the Na+/Ca2+ exchanger both contribute to the Ca2+ transient of failing human ventricular myocytes. Circ. Res 84: 435-444; 1999. (Pubitemid 29120009)
29. Weber, C. R.; Piacentino 3rd V.; Ginsburg, K. S.; Houser, S. R.; Bers, D. M. Na+-Ca2+ exchange current and submembrane [Ca2+] during the cardiac action potential. Circ. Res 90: 182-189; 2002. (Pubitemid 34627087)
30. Maack, C.; Cortassa, S.; Aon, M. A.; Ganesan, A. N.; Liu, T.; O'Rourke, B. Elevated cytosolic Na+ decreases mitochondrial Ca2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ. Res. 99: 17 2 -182; 2006. (Pubitemid 44297041)
31. Sag, C. M.; Wadsack, D. P.; Khabbazzadeh, S.; Abesser, M.; Grefe, C.; Neumann, K.; Opiela, M. K.; Backs, J.; Olson, E. N.; Brown, J. H.; Neef, S.; Maier, S. K.; Maier, L. S. Calcium/calmodulin-dependent protein kinase II contributes to cardiac arrhythmogenesis in heart failure. Circ. Heart Fail 2: 664-675; 2009.
32. Belevych, A. E.; Terentyev, D.; Terentyeva, R.; Nishijima, Y.; Sridhar, A.; Hamlin, R. L.; Carnes, C. A.; Györke, S. The relationship between arrhythmo-genesis and impaired contractility in heart failure: role of altered ryanodine receptor function. Cardiovasc. Res 90: 493-502; 2011.
33. Hoeker, G. S.; Katra, R. P.; Wilson, L. D.; Plummer, B. N.; Laurita, K. R. Spontaneous calcium release in tissue from the failing canine heart. Am. J. Physiol. Heart Circ. Physiol 297:H1235-H1242; 2009.
34. van Oort, R. J.; McCauley, M. D.; Dixit, S. S.; Pereira, L.; Yang, Y.; Respress, J. L.; Wang, Q.; De Almeida, A. C.; Skapura, D. G.; Anderson, M. E.; Bers, D. M.; Wehrens, X. H. Ryanodine receptor phosphorylation by calcium/calmodulin-dependent protein kinase II promotes life-threatening ventricular arrhythmias in mice with heart failure. Circulation 122: 2669-2679; 2010.
35. Sipido, K. R.; Callewaert, G.; Carmeliet, E. Inhibition and rapid recovery of Ca2 + current during Ca2+ release from the sarcoplasmic reticulum in guinea pig ventricular myocytes. Circ. Res. 76: 102-109; 1995.
36. Müller, I.; Niethammer, D.; Bruchelt, G. Anthracycline-derived chemother-apeutics in apoptosis and free radical cytotoxicity. Int. J. Mol. Med 1: 491-494; 1998.
37. Zuppinger, C.; Timolati, F.; Suter, T. M. Pathophysiology and diagnosis of cancer drug induced cardiomyopathy. Cardiovasc. Toxicol 7: 61-66; 2007. (Pubitemid 47339868)
38. Prosser, B. L.; Ward, C. W.; Lederer, W. J. X.- ROS signaling: rapid mechano-chemo transduction in heart. Science 333: 1440-1445; 2011.
39. Aon, M. A.; Cortassa, S.; O'Rourke, B.; Redox-optimized, R. O. S. balance: a unifying hypothesis. Biochim. Biophys. Acta 17 9 7: 865-877; 2010.
40. Palace, V.; Kumar, D.; Hill, M. F.; Khaper, N.; Singal, PK Regional differences in non-enzymatic antioxidants in the heart under control and oxidative stress conditions. J. Mol. Cell. Cardiol. 31: 193-202; 1999. (Pubitemid 29078230)
41. Ide, T.; Tsutsui, H.; Kinugawa, S.; Suematsu, N.; Hayashidani, S.; Ichikawa, K.; Utsumi, H.; Machida, Y.; Egashira, K.; Takeshita, A. Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ. Res 86: 152-157; 2000. (Pubitemid 30086175)
42. Ide, T.; Tsutsui, H.; Kinugawa, S.; Utsumi, H.; Kang, D.; Hattori, N.; Uchida, K.; Arimura, K.; Egashira, K.; Takeshita, A. Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ. Res 85: 357-363; 1999. (Pubitemid 29398868)
43. Perrelli, M. G.; Pagliaro, P.; Penna, C. Ischemia/reperfusion injury and cardioprotective mechanisms: role of mitochondria and reactive oxygen species. World J. Cardiol 3: 18 6 -200; 2011.
44. Kohlhaas, M.; Liu, T.; Knopp, A.; Zeller, T.; Ong, M. F.; Böhm, M.; O'Rourke, B.; Maack, C. Elevated cytosolic Na+ increases mitochondrial formation of reactive oxygen species in failing cardiac myocytes. Circulation 121(14): 1606-1613; 2010.
45. Pacher, P.; Beckman, J. S.; Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev 87: 315-424; 2007. (Pubitemid 46217686)
46. Zorov, D. B.; Filburn, C. R.; Klotz, L. O.; Zweier, J. L.; Sollott, S. J. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J. Exp. Med 192: 1001-1014; 200 0.
47. Bedard, K.; Krause, K. H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev 87: 245-313; 2007. (Pubitemid 46209993)
48. Dai, D. F.; Rabinovitch, P. Mitochondrial oxidative stress mediates induction of autophagy and hypertrophy in angiotensin-II treated mouse hearts. Autophagy 7: 917-918; 2011.
49. Dai, D. F.; Chen, T.; Szeto, H.; Nieves-Cintrón, M.; Kutyavin, V.; Santana, L. F.; Rabinovitch, P. S. Mitochondrial targeted antioxidant peptide ameliorates hypertensive cardiomyopathy. J. Am. Coll. Cardiol 58: 73-82; 2011.
50. Dai, D. F.; Hsieh, E. J.; Liu, Y.; Chen, T.; Beyer, R. P.; Chin, M. T.; MacCoss, M. J.; Rabinovitch, P. S. Mitochondrial proteome remodelling in pressure overload-induced heart failure: the role of mitochondrial oxidative stress. Cardiovasc. Res. 93: 79-88; 2012.
51. Dai, D. F.; Johnson, S. C.; Villarin, J. J.; Chin, M. T.; Nieves-Cintrón, M.; Chen, T.; Marcinek, D. J.; Dorn 2nd G. W.; Kang, Y. J.; Prolla, T. A.; Santana, L. F.; Rabinovitch, P. S. Mitochondrial oxidative stress mediates angiotensin II-induced cardiac hypertrophy and Gaq overexpression-induced heart failure. Circ. Res 108: 837-846; 2011.
52. Heymes, C.; Bendall, J. K.; Ratajczak, P.; Cave, A. C.; Samuel, J. L.; Hasenfuss, G.; Shah, A. M. Increased myocardial NADPH oxidase activity in human heart failure. J. Am. Coll. Cardiol 41: 2164-2171; 2003. (Pubitemid 36724261)
53. Sirker, A.; Zhang, M.; Shah, A. M. NADPH oxidases in cardiovascular disease: insights from in vivo models and clinical studies. Basic Res. Cardiol 106: 735-747; 2011.
54. Byrne, J. A.; Grieve, D. J.; Bendall, J. K.; Li, J. M.; Gove, C.; Lambeth, JD; Cave, AC; Shah, AM Contrasting roles of NADPH oxidase isoforms in pressure-overload versus angiotensin II-induced cardiac hypertrophy. Circ. Res 93(9): 802-805; 2003.
55. Ago, T.; Kuroda, J.; Pain, J.; Fu, C.; Li, H.; Sadoshima, J. Upregulation of NOX4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ. Res. 106: 1253-1264; 2010.
56. Zhang, M.; Brewer, A. C.; Schroder, K.; Santos, C. X.; Grieve, D. J.; Wang, M.; Anilkumar, N.; Yu, B.; Dong, X.; Walker, S. J.; Brandes, R. P.; Shah, A. M. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc. Natl. Acad. Sci. USA 107: 18 121 -18126; 2011.
57. Grieve, D. J.; Byrne, J. A.; Siva, A.; Layland, J.; Johar, S.; Cave, A. C.; Shah, A. M. Involvement of the nicotinamide adenosine dinucleotide phosphate oxidase isoform NOX2 in cardiac contractile dysfunction occurring in response to pressure overload. J. Am. Coll. Cardiol 47: 817-826; 2006. (Pubitemid 43243107)
58. Kuroda, J.; Ago, T.; Matsushima, S.; Zhai, P.; Schneider, M. D.; Sadoshima, J. NADPH oxidase 4 (NOX4) is a major source of oxidative stress in the failing heart. Proc. Natl. Acad. Sci. USA 107: 15565-15570; 2010.
59. Sánchez, 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. 39: 982-991; 2005. (Pubitemid 41572331)
60. Zhao, Z.; Fefelova, N.; Shanmugam, M.; Bishara, P.; Babu, G. J.; Xie, L. H. Angiotensin II induces afterdepolarizations via reactive oxygen species and calmodulin kinase II signaling. J. Mol. Cell. Cardiol 50: 128-136; 2011.
61. Cappola, T. P.; Kass, D. A.; Nelson, G. S.; Berger, R. D.; Rosas, G. O.; Kobeissi, Z. A.; Marban, E.; Hare, J. M. Allopurinol improves myocardial efficiency in patients with idiopathic dilated cardiomyopathy. Circulation 10 4 : 2407-2411; 2001. (Pubitemid 33108372)
62. Boueiz, A.; Damarla, M.; Hassoun, P. M. Xanthine oxidoreductase in respiratory and cardiovascular disorders. Am. J. Physiol. Lung Cell Mol. Physiol 294: L830-L840; 2008.
63. Minhas, K. M.; Saraiva, R. M.; Schuleri, K. H.; Lehrke, S.; Zheng, M.; Saliaris, A. P.; Berry, C. E.; Barouch, L. A.; Vandegaer, K. M.; Li, D.; Hare, J. M. Xanthine oxidoreductase inhibition causes reverse remodeling in rats with dilated cardiomyopathy. Circ. Res 98: 271-279; 2006.
64. Khan, S. A.; Lee, K.; Minhas, K. M.; Gonzalez, D. R.; Raju, S. V.; Tejani, A. D.; Li, D.; Berkowitz, D. E.; Hare, J. M. Neuronal nitric oxide synthase negatively regulates xanthine oxidoreductase inhibition of cardiac excitation-contraction coupling. Proc. Natl. Acad. Sci. USA 101: 15944-15948; 2004. (Pubitemid 39507906)
65. Zhang, Y. H.; Casadei, B. Sub-cellular targeting of constitutive NOS in health and disease. J. Mol. Cell. Cardiol. 52: 341-350; 2012.
66. Chen, C. A.; Wang, T. Y.; Varadharaj, S.; Reyes, L. A.; Hemann, C.; Talukder, M. A.; Chen, Y. R.; Druhan, L. J.; Zweier, J. L. S-Glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 468: 111 5 -1118; 2010.
67. Takimoto, E.; Champion, H. C.; Li, M.; Ren, S.; Rodriguez, E. R.; Tavazzi, B.; Lazzarino, G.; Paolocci, N.; Gabrielson, K. L.; Wang, Y.; Kass, D. A. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J. Clin. Invest. 115 : 1221-1231; 2005. (Pubitemid 40629040)
68. Barouch, L. A.; Harrison, R. W.; Skaf, M. W.; Rosas, G. O.; Cappola, T. P.; Kobeissi, Z. A.; Hobai, I. A.; Lemmon, C. A.; Burnett, A. L.; O'Rourke, B.; Rodriguez, E. R.; Huang, P. L.; Lima, J. A.; Berkowitz, D. E.; Hare, J. M. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 416: 337-339; 2002.
69. Burkard, N.; Rokita, A. G.; Kaufmann, S. G.; Hallhuber, M.; Wu, R.; Hu, K.; Hofmann, U.; Bonz, A.; Frantz, S.; Cartwright, E. J.; Neyses, L.; Maier, L. S.; Maier, S. K.; Renné, T.; Schuh, K.; Ritter, O. Conditional neuronal nitric oxide synthase overexpression impairs myocardial contractility. Circ. Res. 10 0: e32-e44; 2007.
70. Damy, T.; Ratajczak, P.; Shah, A. M.; Camors, E.; Marty, I.; Hasenfuss, G.; Marotte, F.; Samuel, J. L.; Heymes, C. Increased neuronal nitric oxide synthase-derived NO production in the failing human heart. Lancet 363: 1365-1367; 2004. (Pubitemid 38529877)
71. Sears, C. E.; Bryant, S. M.; Ashley, E. A.; Lygate, C. A.; Rakovic, S.; Wallis, H. L.; Neubauer, S.; Terrar, D. A.; Casadei, B. Cardiac neuronal nitric oxide synthase isoform regulates myocardial contraction and calcium handling. Circ. Res. 92: e52-e59; 2003.
72. Ziolo, M. T.; Maier, L. S.; Piacentino 3rd V.; Bossuyt, J.; Houser, S. R.; Bers, D. M. Myocyte nitric oxide synthase 2 contributes to blunted ß-adrenergic response in failing human hearts by decreasing Ca2+ transients. Circulation 109: 1886-18 9 1 ; 2 0 0 4 . (Pubitemid 38509124)
73. Bendall, J. K.; Damy, T.; Ratajczak, P.; Loyer, X.; Monceau, V.; Marty, I.; Milliez, P.; Robidel, E.; Marotte, F.; Samuel, J. L.; Heymes, C. Role of myocardial neuronal nitric oxide synthase-derived nitric oxide in beta-adrenergic hyporesponsiveness after myocardial infarction-induced heart failure in rat. Circulation 11 0 : 2368-2375; 2004. (Pubitemid 39407341)
74. van Oort, R. J.; McCauley, M. D.; Dixit, S. S.; Pereira, L.; Yang, Y.; Respress, J. L.; Wang, Q.; De Almeida, A. C.; Skapura, D. G.; Anderson, M. E.; Bers, D. M.; Wehrens, X. H. Ryanodine receptor phosphorylation by calcium/calmodulin- dependent protein kinase II promotes life-threatening ventricular arrhythmias in mice with heart failure. Circulation 122: 2669-2679; 2011.
75. Grueter, C. E.; Abiria, S. A.; Dzhura, I.; Wu, Y.; Ham, A. J.; Mohler, P. J.; Anderson, M. E.; Colbran, R. J. L-type Ca2+ channel facilitation mediated by phosphorylation of the beta subunit by CaMKII. Mol. Cell 23: 641-650; 2006. (Pubitemid 44292555)
76. Koval, O. M.; Guan, X.; Wu, Y.; Joiner, M. L.; Gao, Z.; Chen, B.; Grumbach, I. M.; Luczak, E. D.; Colbran, R. J.; Song, L. S.; Hund, T. J.; Mohler, P. J.; Anderson, M. E. CaV1. 2 ß-subunit coordinates CaMKII-triggered cardiomyocyte death and afterdepolarizations. Proc. Natl. Acad. Sci. USA 107: 4996-5000; 2010.
77. Maier, L. S.; Bers, D. M. Role of Ca2+/calmodulin-dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. Cardiovasc. Res 73: 631-640; 2007. (Pubitemid 46227343)
78. Hund, T. J.; Koval, O. M.; Li, J.; Wright, P. J.; Qian, L.; Snyder, J. S.; Gudmundsson, H.; Kline, C. F.; Davidson, N. P.; Cardona, N.; Rasband, M. N.; Anderson, M. E.; Mohler, P. J. A. ßIV-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J. Clin. Invest. 120: 3508-3519; 2010.
79. Grandi, E.; Puglisi, J. L.; Wagner, S.; Maier, L. S.; Severi, S.; Bers, D. M. Simulation of Ca/calmodulin-dependent pro-tein kinase II on rabbit ventricular myocyte ion currents and action potentials. Biophys. J. 93: 3835-3847; 2007. (Pubitemid 350223802)
80. Schulman, H.; Greengard, P. Stimulation of brain membrane protein phos-phorylation by calcium and an endogenous heat-stable protein. Nature 271 (5644): 478-479; 1978. (Pubitemid 8257927)
81. Kuret, J.; Schulman, H. Mechanism of autophosphorylation of the multifunctional Ca2+/calmodulin-dependent protein kinase. J. Biol. Chem. 260: 6427-6433; 1985. (Pubitemid 15051783)
82. Schworer, C. M.; Colbran, R. J.; Soderling, T. R. Reversible generation of a Ca2 +-independent form of Ca2+/calmodulin-dependent protein kinase II by an autophosphorylation mechanism. J. Biol. Chem 261: 8581-8584; 1986. (Pubitemid 17205046)
83. Erickson, J. R.; Joiner, M. L.; Guan, X.; Kutschke, W.; Yang, J.; Oddis, C. V.; Bartlett, R. K.; Lowe, J. S.; O'Donnell, S. E.; Aykin-Burns, N.; Zimmerman, M. C.; Zimmerman, K.; Ham, A. J.; Weiss, R. M.; Spitz, D. R.; Shea, M. A.; Colbran, R. J.; Mohler, P. J.; Anderson, M. E. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133: 462-474; 2008. (Pubitemid 351608692)
84. Swaminathan, P. D.; Purohit, A.; Soni, S.; Voigt, N.; Singh, M. V.; Glukhov, A. V.; Gao, Z.; He, B. J.; Luczak, E. D.; Joiner, M. L.; Kutschke, W.; Yang, J.; Donahue, J. K.; Weiss, R. M.; Grumbach, I. M.; Ogawa, M.; Chen, P. S.; Efimov, I.; Dobrev, D.; Mohler, P. J.; Hund, T. J.; Anderson, M. E. Oxidized CaMKII causes cardiac sinus node dysfunction in mice. J. Clin. Invest. 121: 3277-3288; 2011.
85. He, B. J.; Joiner, M. L.; Singh, M. V.; Luczak, E. D.; Swaminathan, P. D.; Koval, O. M.; Kutschke, W.; Allamargot, C.; Yang, J.; Guan, X.; Zimmerman, K.; Grumbach, I. M.; Weiss, R. M.; Spitz, D. R.; Sigmund, C. D.; Blankesteijn, W. M.; Heymans, S.; Mohler, P. J.; Anderson, M. E. Oxidation of CaMKII determines the cardiotoxic effects of aldosterone. Nat. Med 17: 1610-1618; 2011.
86. Erickson, J. R.; He, B. J.; Grumbach, I. M.; Anderson, M. E. CaMKII in the cardiovascular system: sensing redox states. Physiol. Rev 91: 889-915; 2011.
87. Xiang, Y.; Kobilka, B. K. Myocyte adrenoceptor signaling pathways. Science 300(5625): 1530-1532; 2003. (Pubitemid 36682874)
88. Ramirez-Correa, G. A.; Cortassa, S.; Stanley, B.; Gao, W. D.; Murphy, A. M. Calcium sensitivity, force frequency relationship and cardiac troponin I: critical role of PKA and PKC phosphorylation sites. J. Mol. Cell. Cardiol. 48: 943-953; 2010.
89. Sarma, G. N.; Kinderman, F. S.; Kim, C.; von Daake, S.; Chen, L.; Wang, B. C.; Taylor, S. S. Structure of D-AKAP2:PKA RI complex: insights into AKAP specificity and selectivity. Structure 18: 155-166; 2010.
90. Brennan, J.; Bardswell, S.; Burgoyne, J.; Fuller, W.; Schroder, E.; Wait, R.; Begum, S. Kentish J, and Eaton P. Oxidant-induced activation of type I protein kinase A is mediated by RI subunit interprotein disulfide bond formation. J. Biol. Chem 281: 21827-21836; 2006. (Pubitemid 44191910)
91. Dorn 2nd G. W.; Force, T. Protein kinase cascades in the regulation of cardiac hypertrophy. J. Clin. Invest 11 5 : 527-537; 2005. (Pubitemid 40322222)
92. House, C.; Kemp, B. E. Protein kinase C contains a pseudosubstrate prototope in its regulatory domain. Science 238(4834): 17 2 6 -1728; 1987. (Pubitemid 18046276)
93. Gopalakrishna, R.; Anderson, W. Ca2+-independent and phospholipid- independent activation of protein kinase C by selective oxidative modification of the regulatory domain. Proc. Natl. Acad. Sci. USA 86: 6758-6762; 1989.
94. Burgoyne, J. R.; Oka, S.; Ale-Agha, N.; Eaton, P. Hydrogen peroxide sensing and signaling by protein kinases in the cardiovascular system. Antioxid. Redox Signal 18: 1042-1052; 2013.
95. Malhotra, A.; Kang, B. P.; Opawumi, D.; Belizaire, W.; Meggs, L. G. Molecular biology of protein kinase C signaling in cardiac myocytes. Mol. Cell. Biochem. 225: 97-107; 2001. (Pubitemid 33014638)
96. Bogoyevitch, M. A.; Parker, P. J.; Sugden, P. H. Characterization of protein kinase C isotype expression in adult rat heart. Protein kinase C-epsilon is a major isotype present, and it is activated by phorbol esters, epinephrine, and endothelin. Circ. Res. 72: 757-767; 1993. (Pubitemid 23077766)
97. Takeishi, Y.; Ping, P.; Bolli, R.; Kirkpatrick, D. L.; Hoit, B. D.; Walsh, R. A. Transgenic overexpression of constitutively active protein kinase C epsilon causes concentric cardiac hypertrophy. Circ. Res 86: 1218-1223; 2000. (Pubitemid 30436661)
98. 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.; Bodi, I.; Wang, S.; Schwartz, A.; Lakatta, E. G.; DePaoli-Roach, A. A.; Robbins, J.; Hewett, T. E.; Bibb, J. A.; Westfall, M. V.; Kranias, J. D.; Molkentin, J. D. PKC-alpha regulates cardiac contractility and propensity toward heart failure. Nat. Med 10: 248-254; 2004. (Pubitemid 38667614)
99. Belin, R. J.; Sumandea, M. P.; Allen, E. J.; Schoenfelt, K.; Wang, H.; Solaro, R. J.; de Tombe, PP Augmented protein kinase C-a-induced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circ. Res. 101: 195-204; 2007. (Pubitemid 47196587)
100. Sumandea, M. P.; Pyle, W. G.; Kobayashi, T.; de Tombe, PP; Solaro, RJ Identification of a functionally critical protein kinase C phosphorylation residue of cardiac troponin. T.J. Biol. Chem. 278: 35135-35144; 2003. (Pubitemid 37102277)
101. Hidalgo, C; Hudson, B.; Bogomolovas, J.; Zhu, Y.; Anderson, B.; Greaser, M.; Labeit, S.; Granzier, H. P. K. C. phosphorylation of titin's PEVK element: a novel and conserved pathway for modulating myocardial stiffness. Circ. Res. 105: 631-638; 2009.
102. Huang, L.; Wolska, B. M.; Montgomery, D. E.; Burkart, E. M.; Buttrick, P. M.; Solaro, R. J. Increased contractility and altered Ca2+ transients of mouse heart myocytes conditionally expressing PKCp. Am. J. Physiol. Cell Physiol. 280: C1114-C1120; 2001.
103. Wang, H.; Grant,J. E.; Doede, C. M.; Sadayappan, S.; Robbins, J.; Walker,J. W PKC-pII sensitizes cardiac myofilaments to Ca2+ by phosphorylating troponin I on threonine-144. J. Mol. Cell. Cardiol. 41: 823-833; 2006. (Pubitemid 44635578)
104. 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. 280: 207-214; 2005. (Pubitemid 40164982)
105. Xu, L; Eu, J. P.; Meissner, G.; Stamler, J. S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-s-nitrosylation. Science 279: 234-237; 1998. (Pubitemid 28103882)
106. Abramson, J. J.; Salama, G. Critical sulfhydryls regulate calcium release from sarcoplasmic reticulum. J. Bioenerg. Biomembr. 21: 283-294; 1989. (Pubitemid 19143574)
107. Anzai, K.; Ogawa, K.; Kuniyasu, A.; Ozawa, T.; Yamamoto, H.; Nakayama, H. Effects of hydroxyl radical and sulfhydryl reagents on the open probability of the purified cardiac ryanodine receptor channel incorporated into planar lipid bilayers. Biochem. Biophys. Res. Commun. 249: 938-942; 1998. (Pubitemid 28441942)
108. Boraso, A.; Williams, A. J. Modification of the gating of the cardiac sarcoplasmic reticulum Ca2+-release channel by H2O2 and dithiothreitol. Am. J. Physiol. 267:H1010-H1016; 1994.
109. Favero, T. G.; Zable, A. C; Abramson, J. J. Hydrogen peroxide stimulates the Ca2+ release channel from skeletal muscle sarcoplasmic reticulum. J. Biol. Chem 270: 25557-25563; 1995.
110. Liu, G.; Abramson, J. J.; Zable, A. C; Pessah, I. N. 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-Vmaleimidylphenyl)-4- methylcoumarin. Mol. Pharmacol. 45: 189-200; 1994.
111. Zissimopoulos, S.; Docrat, N.; Lai, F. A. Redox sensitivity of the ryanodine receptor interaction with FK506-binding protein. J. Biol. Chem. 282: 6976-6983; 2007. (Pubitemid 47093660)
112. Yan, Y; Liu, J.; Wei, C; Li, K.; Xie, W.; Wang, Y; Cheng, H. Bidirectional regulation of Ca2+ sparks by mitochondria-derived reactive oxygen species in cardiac myocytes. Cardiovasc. Res. 77: 432-441; 2008. (Pubitemid 351197642)
113. Marengo, J. J.; Hidalgo, C; Bull, R. Sulfhydryl oxidation modifies the calcium dependence of ryanodine-sensitive calcium channels of excitable cells. Biophys. J. 74: 1263-1277; 1998. (Pubitemid 28108536)
114. Eager, K. R.; Dulhunty, A. F. Activation of the cardiac ryanodine receptor by sulfhydryl oxidation is modified by Mg2+ and ATP. J. Membr. Biol. 163: 9-18; 1998. (Pubitemid 28221602)
115. Niwano, K.; Arai, M.; Koitabashi, N.; Watanabe, A.; Ikeda, Y; Miyoshi, H.; Kurabayashi, M. Lentiviral vector-mediated SERCA2 gene transfer protects against heart failure and left ventricular remodeling after myocardial infarction in rats. Mol. Ther. 16: 1026-1032; 2008. (Pubitemid 351737066)
116. Kukreja, R. C; Okabe, E.; Schrier, G. M.; Hess, M. L Oxygen radical- mediated lipid peroxidation and inhibition of Ca2+ ATPase activity of cardiac sarcoplasmic reticulum. Arch. Biochem. Biophys. 261: 447-457; 1988. (Pubitemid 18078296)
117. Morris, T. E.; Sulakhe, P. V. Sarcoplasmic reticulum Ca2+-pump dysfunction in rat cardiomyocytes briefly exposed to hydroxyl radicals. Free Radic. Biol. Med. 22: 37-47; 1997. (Pubitemid 26399309)
118. Scherer, N. M.; Deamer, D. W Oxidative stress impairs the function of sarcoplasmic reticulum by oxidation of sulfhydryl groups in the Ca2+-ATPase. Arch. Biochem. Biophys. 246: 589-601; 1986. (Pubitemid 16072580)
119. Xu, K. Y.; Zweier, J. L.; Becker, L C. Hydroxyl radical inhibits sarcoplasmic reticulum Ca2+-ATPase function by direct attack on the ATP binding site. Circ. Res. 80: 76-81; 1997. (Pubitemid 27030371)
120. Sag, C. M.; Dybkova, N.; Neef, S.; Maier, L. S. Effects on recovery during acidosis in cardiac myocytes overexpressing CaMKII. J. Mol. Cell. Cardiol. 43: 696-709; 2007. (Pubitemid 350166388)
121. Nicoll D.A., Ottolia M., Lu L, Lu Y, and Philipson K.D. A new topological model of the cardiac sarcolemmal Na+-Ca2+ exchanger. J. Biol. Chem. 27 52.
122. Goldhaber, J. I. Free radicals enhance Na+/Ca2+ exchange in ventricular myocytes. Am. J. Physiol. 271:H823-H833; 1999.
123. Kato, M.; Kako, K. J. Na+/Ca2+ exchange of isolated sarcolemmal membrane: effects of insulin, oxidants and insulin deficiency. Mol. Cell. Biochem 83: 15-25; 1988.
124. Reeves, J. P.; Bailey, C. A.; Hale, C. C. Redox modification of sodium - calcium exchange activity in cardiac sarcolemmal vesicles. J. Biol. Chem 261: 4948-4955; 1986. (Pubitemid 17204285)
125. Santacruz-Toloza, L; Ottolia, M.; Nicoll, D. A.; Philipson, K. D. Functional analysis of a disulfide bond in the cardiac Na+-Ca2+ exchanger. J. Biol. Chem 275: 182-188; 2000. (Pubitemid 30038970)
126. Kuster, G. M.; Lancel, S.; Zhang, J.; Communal, C; Trucillo, MP; Lim, CC; Pfister, O; Weinberg, EO; Cohen, RA; Liao, R; Siwik, DA; Colucci, WS Redox-mediated reciprocal regulation of SERCA and Na+-Ca2+ exchanger contributes to sarcoplasmic reticulum Ca2+ depletion in cardiac myocytes. Free Radic. Biol. Med. 48: 118 2 -1187; 2010.
127. Hilgemann, D. W.; Nicoll, D. A.; Philipson, K. D. Charge movement during Na+ translocation by native and cloned cardiac Na+/Ca2+ exchanger. Nature 352: 715-718; 1991. (Pubitemid 21912413)
128. Iwamoto, T.; Pan, Y.; Wakabayashi, S.; Imagawa, T.; Yamanaka, H. I.; Shigekawa, M. Phosphorylation-dependent regulation of cardiac Na+/Ca2+ exchanger via protein kinase C. J. Biol. Chem 271: 13609-13615; 1996.
129. Zhong, J.; Hwang, T. C.; Adams, H. R.; Rubin, L. J. Reduced L-type calcium current in ventricular myocytes from endotoxemic guinea pigs. Am. J. Physiol. 273:H2312-H2324; 1997.
130. Mikami, A.; Imoto, K.; Tanabe, T.; Niidome, T.; Mori, Y.; Takeshima, H.; Narumiya, S.; Numa, S. Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel. Nature 340: 230-233; 1989. (Pubitemid 19171586)
131. Blaich, A.; Welling, A.; Fischer, S.; Wegener, J. W.; Köstner, K.; Hofmann, F.; Moosmang, S. Facilitation of murine cardiac L-type CaV1.2 channel is modulated by calmodulin kinase II-dependent phosphorylation of S1512 and S1570. Proc. Natl. Acad. Sci. USA 107: 10285-10289; 2010.
132. Dzhura, I.; Wu, Y.; Colbran, R. J.; Balser, J. R.; Anderson, M. E. Calmodulin kinase determines calcium-dependent facilitation of L-type calcium
133. Hudmon, A.; Schulman, H.; Kim, J.; Maltez, J. M.; Tsien, R. W.; Pitt, G. S. CaMKII tethers to L-type Ca2+ channels, establishing a local and dedicated integrator of Ca2+ signals for facilitation. J. Cell Biol 17 1 : 537-547; 2005. (Pubitemid 41586942)
134. Kohlhaas, M.; Zhang, T.; Seidler, T.; Zibrova, D.; Dybkova, N.; Steen, A.; Wagner, S.; Chen, L.; Brown, J. H.; Bers, D. M.; Maier, L. S. Increased sarcoplasmic reticulum calcium leak but unaltered contractility by acute CaMKII overexpression in isolated rabbit cardiac myocytes. Circ. Res. 98: 235-244; 2006.
135. Catterall, W. A. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol 16: 521-555; 2000. (Pubitemid 32037516)
136. De Jongh, K. S.; Murphy, B. J.; Colvin, A. A.; Hell, J. W.; Takahashi, M.; Catterall, W. A. Specific phosphorylation of a site in the full-length form of the a1 subunit of the cardiac L-type calcium channel by adenosine 3',5'-cyclic monophosphate-dependent protein kinase. Biochemistry 35: 10392-10402; 1996. (Pubitemid 26277298)
137. Hulme, J. T.; Westenbroek, R. E.; Scheuer, T.; Catterall, W. A. Phosphorylation of serine 1928 in the distal C-terminal domain of cardiac CaV1.2 channels during ß1-adrenergic regulation. Proc. Natl. Acad. Sci. USA 103: 16574-16579; 2006. (Pubitemid 44715237)
138. Gill, J. S.; McKenna, W. J.; Camm, A. Free radicals irreversibly decrease Ca2+ currents in isolated guinea-pig ventricular myocytes. Eur. J. Pharmacol. 292: 337-340; 1995.
139. Goldhaber, J. I.; Ji, S.; Lamp, S. T.; Weiss, J. N. Effects of exogenous free radicals on electromechanical function and metabolism in isolated rabbit and guinea pig ventricle. Implications for ischemia and reperfusion injury. J. Clin. Invest 83: 18 0 0 -1809; 1989. (Pubitemid 19148847)
140. Lacampagne, A.; Duittoz, A.; Bolanos, P.; Peineau, N.; Argibay, J. A. Effect of sulfhydryl oxidation on ionic and gating currents associated with L-type calcium channels in isolated guinea-pig ventricular myocytes. Cardiovasc. Res. 30: 799-806; 1995.
141. Song, Y. H.; Cho, H.; Ryu, S. Y.; Yoon, J. Y.; Park, S. H.; Noh, C. I.; Lee, S. H.; Ho, W. K. L-type Ca2+ channel facilitation mediated by H2O2-induced activation of CaMKII in rat ventricular myocytes. J. Mol. Cell. Cardiol. 48: 773-780; 2010.
142. Kassmann, M.; Hansel, A.; Leipold, E.; Birkenbeil, J.; Lu, S. Q.; Hoshi, T.; Heinemann, S. H. Oxidation of multiple methionine residues impairs rapid sodium channel inactivation. Pflugers Arch 456: 1085-1095; 2008.
143. Maier, L. S. CaMKII regulation of voltage-gated sodium channels and cell excitability. Heart Rhythm 8: 474-477; 2011.
144. Song, Y.; Shryock, J.; Wagner, S.; Maier, L. S.; Belardinelli, L. Blocking late sodium current reduces hydrogen peroxide-induced arrhythmogenic activity and contractile dysfunction. J. Pharmacol. Exp. Ther 318: 214-222; 2006.
145. Yao, L.; Fan, P.; Jiang, Z.; Viatchenko-Karpinski, S.; Wu, Y.; Kornyeyev, D.; Hirakawa, R.; Budas, G. R.; Rajamani, S.; Shryock, J. C.; Belardinelli, L. Nav1.5-dependent persistent Na+ influx activates CaMKII in rat ventricular myocytes and N1325S mice. Am. J. Physiol. Cell Physiol. 301:C577-C586; 2011.
146. Fukuda, K.; Davies, S. S.; Nakajima, T.; Ong, B. H.; Kupershmidt, S.; Fessel, J.; Amarnath, V.; Anderson, M. E.; Boyden, P. A.; Viswanathan, P. C.; Roberts 2nd L. J.; Balser, J. R. Oxidative mediated lipid peroxidation recapitulates proar-rhythmic effects on cardiac sodium channels. Circ. Res 97: 1262-1269; 2005.
147. Valdivia, C. R.; Ueda, K.; Ackerman, M. J.; Makielski, J. C. GPD1L links redox state to cardiac excitability by PKC-dependent phosphorylation of the sodium channel SCN5A. Am. J. Physiol. Heart Circ. Physiol 297:H1446-H1452; 2009.
148. Ashpole, N. M.; Herren, A. W.; Ginsburg, K. S.; Brogan, J. D.; Johnson, D. E.; Cummins, T. R.; Bers, D. M.; Hudmon, A. Ca2+/calmodulin-dependent protein kinase II (CaMKII) regulates cardiac sodium channel NaV1.5 gating by multiple phosphorylation sites. J. Biol. Chem. 287: 19856-19869; 2012.
149. Koval, O. M.; Snyder, J. S.; Wolf, R. M.; Pavlovicz, R. E.; Glynn, P.; Curran, J.; Leymaster, N. D.; Dun, W.; Wright, P. J.; Cardona, N.; Qian, L.; Mitchell, C. C.; Boyden, P. A.; Binkley, P. F.; Li, C.; Anderson, M. E.; Mohler, P. J.; Hund, T. J. Ca2 +/calmodulin-dependent protein kinase II-based regulation of voltage-gated Na+ channel in cardiac disease. Circulation 126: 2084-2094; 2012.
150. Ono, K.; Fozzard, H. A.; Hanck, D. A. Mechanism of cAMP-dependent modulation of cardiac sodium channel current kinetics. Circ. Res 72: 807-815; 1993. (Pubitemid 23077771)
151. Chandra, R.; Chauhan, V. S.; Starmer, C. F.; Grant, A. O. Beta-Adrenergic action on wild-type and KPQ mutant human cardiac Na+ channels: shift in gating but no change in Ca2+:Na+ selectivity. Cardiovasc. Res 42: 490-502; 1999. (Pubitemid 29243174)
152. Baba, S.; Dun, W.; Boyden, P. A.; Can, P. K. A. activators rescue Na+ channel function in epicardial border zone cells that survive in the infarcted canine heart? Cardiovasc. Res. 64: 260-267; 2004. (Pubitemid 39361687)
153. Zhou, J.; Yi,J.; Hu, N.; George Jr A. L; Murray, K.T. Activation of protein kinase A modulates trafficking of the human cardiac sodium channel in Xenopus oocytes. Circ. Res 87: 33-38; 2000. (Pubitemid 30456932)
154. Lu, T.; Lee, H. C; Kabat, J. A.; Shibata, E. F. Modulation of rat cardiac sodium channel by the stimulatory G protein alpha subunit. J. Physiol 518: 371-384; 1999. (Pubitemid 29366736)
155. Yarbrough, T. L; Lu, T.; Lee, H. C; Shibata, E. F. Localization of cardiac sodium channels in caveolin-rich membrane domains: regulation of sodium current amplitude. Circ. Res 90: 443-449; 2002. (Pubitemid 34633914)
156. Murphy, B.J.; Rogers, J.; Perdichizzi, A. P.; Colvin, A. A.; Catterall, W. A. cAMP- dependent phosphorylation of two sites in the alpha subunit of the cardiac sodium channel. J. Biol. Chem 271: 28837-28843; 1996. (Pubitemid 26382582)
157. Frohnwieser, B.; Chen, L. Q.; Schreibmayer, W.; Kallen, R. G. Modulation of the human cardiac sodium channel alpha-subunit by cAMP-dependent protein kinase and the responsible sequence domain. J. Physiol 498: 309-318; 1997. (Pubitemid 27073377)
158. Hallaq, H.; Yang, Z.; Viswanathan, P. C; Fukuda, K.; Shen, W.; Wang, D. W.; Wells, K. S.; Zhou, J.; Yi, J.; Murray, K. T. Quantitation of protein kinase A-mediated trafficking of cardiac sodium channels in living cells. Cardiovasc. Res. 72: 250-261; 2006. (Pubitemid 44511919)
159. Ward, C. A.; Giles, W R. Ionic mechanism of the effects of hydrogen peroxide in rat ventricular myocytes. J. Physiol 500: 631-642; 1997. (Pubitemid 27207825)
160. Qu, Y; Rogers, J.; Tanada, T.; Catterall, W; Scheuer, T. Phosphorylation of S1505 in the cardiac Na+ channel inactivation gate is required for modulation by protein kinase C. J. Gen. Physiol 108: 375-379; 1996. (Pubitemid 26374748)
161. Liu, M.; Liu, H.; Dudley Jr. S. C. Reactive oxygen species originating from mitochondria regulate the cardiac sodium channel. Circ. Res 107: 967-974; 2010.
162. Sossalla, S; Kallmeyer, B; Wagner, S; Mazur, M; Maurer, U; Toischer, K; Schmitto, JD; Seipelt, R; Schöndube, F; Hasenfuss, G; Belardinelli, L; Maier, LS. Altered Na+ currents in atrial fibrillation: effects of ranolazine on arrhythmias and contractility in human atrial myocardium. J. Am. Coll. Cardiol. 55: 2330-2342; 2010.
163. Maier, L. S.; Layug, B.; Karwatowska-Prokopczuk, E.; Belardinelli, L.; Lee, S.; Sander, J.; Lang, C.; Wachter, R.; Edelmann, F.; Hasenfuss, G.; Jacobshagen, C. RAnoLazIne for the treatment of diastolic heart failure in patients with preserved ejection fraction: the RALI-DHF proof-of-concept study. JACC: Heart Fail 1: 115 -122; 2013.
164. Kim, M. S.; Akera, T. O2 free radicals: cause of ischemia-reperfusion injury to cardiac Na+-K+-ATPase. Am J. Physiol 252:H252-H257; 1987.
165. Kukreja, R. C.; Weaver, A. B.; Hess, M. L. Sarcolemmal Na+-K+-ATPase: inactivation by neutrophil-derived free radicals and oxidants. Am. J. Physiol 259:H1330-H1336; 1990. (Pubitemid 20385729)
166. Despa, S.; Bossuyt, J.; Han, F.; Ginsburg, K. S.; Jia, L. G.; Kutchai, H.; Tucker, A. L.; Bers, D. M. Phospholemman-phosphorylation mediates the beta-adrenergic effects on Na/K pump function in cardiac myocytes. Circ. Res. 97: 252-259; 2005. (Pubitemid 41105451)
167. Penna, C.; Mancardi, D.; Rastaldo, R.; Pagliaro, P. Cardioprotection: a radical view Free radicals in pre and postconditioning. Biochim. Biophys. Acta 17 8 7: 781-793; 2009.
168. Murdoch, C. E.; Alom-Ruiz, S. P.; Wang, M.; Zhang, M.; Walker, S.; Yu, B.; Brewer, A.; Shah, A. M. Role of endothelial NOX2 NADPH oxidase in angiotensin II-induced hypertension and vasomotor dysfunction. Basic Res. Cardiol 106: 527-538; 2011.
169. Schröder, K.; Zhang, M.; Benkhoff, S.; Mieth, A.; Pliquett, R.; Kosowski, J.; Kruse, C.; Luedike, P.; Michaelis, U. R.; Weissmann, N.; Dimmeler, S.; Shah, A. M.; Brandes, R. P. NOX4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ. Res. 11 0 : 1217-1225; 2012.
170. Luo, M.; Guan, X.; Luczak, E. D.; Di, L.; Kutschke, W.; Gao, Z.; Yang, J.; Glynn, P.; Sossalla, S.; Swaminathan, P. D.; Weiss, R. M.; Yang, B.; Rokita, A. G.; Maier, L. S.; Efimov, I.; Hund, T. J.; Anderson, M. E. Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. J. Clin. Invest. 123: 1262-1274; 2013.)