Physiological regulation of cardiac contractility by endogenous reactive oxygen species

Acta Physiologica

Volumn 205, Issue 1, 2012, Pages 26-40

  Perjes A ^a,b   Kubin, A M ^a   Konyi A ^a   Szabados, S ^a   Cziraki A ^a   Skoumal, R ^b   Ruskoaho, H ^b   Szokodi, I ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF OULU   (Finland)

Author keywords

Beta adrenergic; Cardiac contractility; Endothelin; Reactive oxygen species; Signal transduction

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; ENDOTHELIN 1; G PROTEIN COUPLED RECEPTOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ADRENERGIC SYSTEM; CONGESTIVE HEART FAILURE; HEART FUNCTION; HEART MITOCHONDRION; HEART MUSCLE CONTRACTILITY; HUMAN; INOTROPISM; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ENDOTHELIN-1; HEART; HUMANS; MYOCARDIAL CONTRACTION; MYOCARDIUM; REACTIVE OXYGEN SPECIES; RECEPTORS, ADRENERGIC, BETA; SIGNAL TRANSDUCTION;

EID: 84859120620     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2012.02391.x     Document Type: Review

References (135)

1. Andersson, D.C., Fauconnier, J., Yamada, T., Lacampagne, A., Zhang, S.-J., Katz, A. & Westerblad, H. 2011. Mitochondrial production of reactive oxygen species contributes to the beta-adrenergic stimulation of mouse cardiomyocytes. J Physiol 589, 1791-1801.
2. Andrukhiv, A., Costa, A.D., West, I.C. & Garlid, K.D. 2006. Opening mitoKATP increases superoxide generation from complex I of the electron transport chain. Am J Physiol Heart Circ Physiol 291, H2067-H2074.
3. Bedard, K. & Krause, K.-H. 2008. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87, 245-313.
4. Bers, D.M. 2007. Going to cAMP just got more complicated. J Physiol 583, 415-416.
5. Bogoyevitch, M.A., Glennon, P.E., Andersson, M.B., Clerk, A., Lazou, A., Marshall, C.J., Parker, P.J. & Sugden, P.H. 1994. Endothelin-1 and fibroblast growth factors stimulate the mitogen-activated protein kinase signaling cascade in cardiac myocytes. The potential role of the cascade in the integration of two signaling pathways leading to myocyte hypertrophy. J Biol Chem 269, 1110-1119.
6. Borbély, A., Tóth, A., Edes, I., Virág, L., Papp, J.G., Varró, A., Paulus, W.J., van der Velden, J., Stienen, G.J.M. & Papp, Z. 2005. Peroxynitrite-induced alpha-actinin nitration and contractile alterations in isolated human myocardial cells. Cardiovasc Res 67, 225-233.
7. Brennan, J.P., Bardswell, S.C., Burgoyne, J.R., Fuller, W., Schröder, E., Wait, R., Begum, S., Kentish, J.C. & Eaton, P. 2006. Oxidant-induced activation of type I protein kinase A is mediated by RI subunit interprotein disulfide bond formation. J Biol Chem 281, 21827-21836.
8. Brunner, F., Bras-Silva, C., Cerdeira, A.S. & Leite-Moreira, A.F. 2006. Cardiovascular endothelins : essential regulators of cardiovascular homeostasis. Pharmacol Ther 111, 508-531.
9. Bueno, O.F. & Molkentin, J.D. 2002. Involvement of extracellular signal-regulated kinases 1/2 in cardiac hypertrophy and cell death. Circ Res 91, 776-781.
10. Caldiz, C.I., Garciarena, C.D., Dulce, R.A., Novaretto, L.P., Yeves, A.M., Ennis, I.L., Cingolani, H.E., Chiappe de Cingolani, G.E. & Pérez, N.G. 2007. Mitochondrial reactive oxygen species activate the slow force response to stretch in feline myocardium. J Physiol 584, 895-905.
11. Callera, G.E., Touyz, R.M., Teixeira, S.A., Muscara, M.N., Carvalho, M.H.C., Fortes, Z.B., Nigro, D., Schiffrin, E.L. & Tostes, R.C. 2003. ETA receptor blockade decreases vascular superoxide generation in DOCA-salt hypertension. Hypertension 42, 811-817.
12. Campbell, D.L., Stamler, J.S. & Strauss, H.C. 1996. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J Gen Physiol 108, 277-293.
13. Canton, M., Menazza, S., Sheeran, F.L., Polverino de Laureto, P., Di Lisa, F. & Pepe, S. 2011. Oxidation of myofibrillar proteins in human heart failure. J Am Coll Cardiol 57, 300-309.
14. 2+ signaling in contractile regulation induced by crosstalk between endothelin-1 and norepinephrine in dog ventricular myocardium. Circ Res 92, 1024.
15. 2+ transients induced by endothelin-1 in rabbit ventricular myocytes. Naunyn Schmiedeberg Arch Pharmacol 371, 185-194.
16. Cingolani, H.E., Villa-Abrille, M.C., Cornelli, M., Nolly, A., Ennis, I.L., Garciarena, C., Suburo, A.M., Torbidoni, V., Correa, M.V., de Hurtado, M.C.C. & Aiello, E.A. 2006. The positive inotropic effect of angiotensin II: role of endothelin-1 and reactive oxygen species. Hypertension 47, 727.
17. Clerk, A. & Sugden, P.H. 2006. Ras: the stress and the strain. J Mol Cell Cardiol 41, 595-600.
18. Czóbel, M., Kaszaki, J., Molnár, G., Nagy, S. & Boros, M. 2009. Nonspecific inhibition of nitric oxide synthesis evokes endothelin-dependent increases in myocardial contractility. Nitric Oxide 21, 201-209.
19. De Giusti, V., Correa, M.V., Villa-Abrille, M.C., Beltrano, C., Yeves, A., Chiappe de Cingolani, G.E., Cingolani, H.E. & Aiello, E.A. 2008. The positive inotropic effect of endothelin-1 is mediated by mitochondrial reactive oxygen species. Life Sci 83, 264-271.
20. Devaraj, S. & Jialal, I. 2005. Failure of vitamin E in clinical trials: is gamma-tocopherol the answer? Nutr Rev 63, 290-293.
21. Dhalla, N.S., Temsah, R.M. & Netticadan, T. 2000. Role of oxidative stress in cardiovascular diseases. J Hypertens 18, 655-673.
22. Dong, F., Zhang, X. & Ren, J. 2006. Leptin regulates cardiomyocyte contractile function through endothelin-1 receptor-NADPH oxidase pathway. Hypertension 47, 222-229.
23. Dzimiri, N. 1999. Regulation of β-adrenoceptor signaling in cardiac function and disease. Pharmacol Rev 51, 465-501.
24. 2+ signaling in intact myocardium. J Pharmacol Sci 100, 525-537.
25. 2+ channel α1C subunits by redox agents and hypoxia. J Physiol 514, 629-637.
26. Forbes, R.A., Steenbergen, C. & Murphy, E. 2001. Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res 88, 802-809.
27. Fuller, S.J., Sivarajah, K. & Sugden, P.H. 2008. ErbB receptors, their ligands, and the consequences of their activation and inhibition in the myocardium. J Mol Cell Cardiol 44, 831-854.
28. ATP in response to inotropic stress. Am J Physiol Heart Circ Physiol 291, H152-H160.
29. Geiszt, M. 2006. NADPH oxidases: new kids on the block. Cardiovasc Res 71, 289-299.
30. 2+ currents in isolated guinea-pig ventricular myocytes. Eur J Pharmacol 292, 337-340.
31. Giordano, F.J. 2005. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115, 500-508.
32. Goldberg, A.T., Bond, B.R., Mukherjee, R., New, R.B., Zellner, J.L., Crawford, F.A. & Spinale, F.G. 2000. Endothelin receptor pathway in human left ventricular myocytes: relation to contractility. Ann Thorac Surg 69, 711-715.
33. 2+ exchange in ventricular myocytes. Am J Physiol Heart Circ Physiol 271, H823-H833.
34. Griendling, K.K., Sorescu, D. & Ushio-Fukai, M. 2000. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86, 494.
35. 2-mediated cell death. Free Radic Biol Med 36, 53-64.
36. Hare, J.M., Mangal, B., Brown, J., Fisher, C., Freudenberger, R., Colucci, W.S., Mann, D.L., Liu, P., Givertz, M.M. & Schwarz, R.P. 2008. Impact of oxypurinol in patients with symptomatic heart failure. Results of the OPT-CHF study. J Am Coll Cardiol 51, 2301-2309.
37. Heinzel, F.R., Luo, Y., Li, X., Boengler, K., Buechert, A., García-Dorado, D., Di Lisa, F., Schulz, R. & Heusch, G. 2005. Impairment of diazoxide-induced formation of reactive oxygen species and loss of cardioprotection in connexin 43 deficient mice. Circ Res 97, 583-586.
38. Heinzel, F.R., Luo, Y., Dodoni, G., Boengler, K., Petrat, F., Di Lisa, F., de Groot, H., Schulz, R. & Heusch, G. 2006. Formation of reactive oxygen species at increased contraction frequency in rat cardiomyocytes. Cardiovasc Res 71, 374-382.
39. 2+ sensitivity in human cardiomyocytes. Antioxid Redox Signal 10, 1175-1184.
40. Heusch, G. & Schulz, R. 2011. A radical view on the contractile machinery in human heart failure. J Am Coll Cardiol 57, 310-312.
41. 2+ channels by S-nitrosothiol nitric oxide donors. Circ Res 81, 742-752.
42. Humphries, K.M., Juliano, C. & Taylor, S.S. 2002. Regulation of cAMP-dependent protein kinase activity by glutathionylation. J Biol Chem 277, 43505-43511.
43. Humphries, K.M., Deal, M.S. & Taylor, S.S. 2005. Enhanced dephosphorylation of cAMP-dependent protein kinase by oxidation and thiol modification. J Biol Chem 280, 2750-2758.
44. Humphries, K.M., Pennypacker, J.K. & Taylor, S.S. 2007. Redox regulation of cAMP-dependent protein kinase signaling: kinase versus phosphatase inactivation. J Biol Chem 282, 22072-22079.
45. Inoue, A., Yanagisawa, M., Kimura, S., Kasuya, Y., Miyauchi, T., Goto, K. & Masaki, T. 1989. The human endothelin family: three structurally and pharmacologically distinct isopeptides predicted by three separate genes. Proc Natl Acad Sci U S A 86, 2863-2867.
46. Ishikawa, T., Yanagisawa, M., Kimura, S., Goto, K. & Masaki, T. 1988. Positive inotropic action of novel vasoconstrictor peptide endothelin on guinea pig atria. Am J Physiol 255, H970.
47. Kanski, J., Behring, A., Pelling, J. & Schöneich, C. 2005. Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: effects of biological aging. Am J Physiol Heart Circ Physiol 288, H371-H381.
48. Kelly, R.A., Eid, H., Krämer, B.K., O'Neill, M., Liang, B.T., Reers, M. & Smith, T.W. 1990. Endothelin enhances the contractile responsiveness of adult rat ventricular myocytes to calcium by a pertussis toxin-sensitive pathway. J Clin Invest 86, 1164-1171.
49. Kimura, S., Zhang, G.-X., Nishiyama, A., Shokoji, T., Yao, L., Fan, Y.-Y., Rahman, M., Suzuki, T., Maeta, H. & Abe, Y. 2005. Role of NAD(P)H oxidase- and mitochondria-derived reactive oxygen species in cardioprotection of ischemic reperfusion injury by angiotensin II. Hypertension 45, 860-866.
50. Kinnunen, P., Szokodi, I., Nicholls, M.G. & Ruskoaho, H. 2000. Impact of NO on ET-1-and AM-induced inotropic responses: potentiation by combined administration. Am J Physiol Regul Integr Comp Physiol 279, R569-R575.
51. Kirkman, H.N. & Gaetani, G.F. 1984. Catalase, a tetrameric enzyme with four tightly bound molecules of NADPH. Proc Natl Acad Sci U S A 81, 4343-4347.
52. Kirkman, H.N., Rolfo, M., Ferraris, A.M. & Gaetani, G.F. 1999. Mechanisms of protection of catalase by NADPH. Kinetics and stoichiometry. J Biol Chem 274, 13908-13914.
53. + exchanger. Circ Res 68, 269-279.
54. Kubin, A.-M., Skoumal, R., Tavi, P., Kónyi, A., Perjés, A., Leskinen, H., Ruskoaho, H. & Szokodi, I. 2011. Role of reactive oxygen species in the regulation of cardiac contractility. J Mol Cell Cardiol 50, 884-893.
55. 2+ depletion in cardiac myocytes. Free Radic Biol Med 48, 1182-1187.
56. Lancel, S., Zhang, J., Evangelista, A., Trucillo, M.P., Tong, X.Y., Siwik, D.A., Cohen, R.A. & Colucci, W.S. 2009. Nitroxyl activates SERCA in cardiac myocytes via glutathiolation of cysteine 674. Circ Res 104, 720-723.
57. Layland, J., Grieve, D.J., Cave, A.C., Sparks, E., Solaro, R.J. & Shah, A.M. 2004. Essential role of troponin I in the positive inotropic response to isoprenaline in mouse hearts contracting auxotonically. J Physiol 556, 835-847.
58. Layland, J., Solaro, R.J. & Shah, A.M. 2005. Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc Res 66, 12-21.
59. 2+-ATPase and myosin heavy chain isozyme switch. Diabetologia 49, 1434-1446.
60. Li, S., Li, X., Zheng, H., Xie, B., Bidasee, K.R. & Rozanski, G.J. 2008. Pro-oxidant effect of transforming growth factor-beta1 mediates contractile dysfunction in rat ventricular myocytes. Cardiovasc Res 77, 107-117.
61. 2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ Res 99, 172-182.
62. A receptor antagonist. Circulation 101, 142-147.
63. MacLennan, D.H. & Kranias, E.G. 2003. Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 4, 566-577.
64. Maejima, Y., Kuroda, J., Matsushima, S., Ago, T. & Sadoshima, J. 2011. Regulation of myocardial growth and death by NADPH oxidase. J Mol Cell Cardiol 50, 408-416.
65. Mak, S. & Newton, G.E. 2001. Vitamin C augments the inotropic response to dobutamine in humans with normal left ventricular function. Circulation 103, 826-830.
66. Mak, S. & Newton, G.E. 2004. Redox modulation of the inotropic response to dobutamine is impaired in patients with heart failure. Am J Physiol Heart Circ Physiol 286, H789-H795.
67. Masaki, T. 1995. Possible role of endothelin in endothelial regulation of vascular tone. Annu Rev Pharmacol Toxicol 35, 235-255.
68. Meng, T.C., Fukada, T. & Tonks, N.K. 2002. Reversible oxidation and inactivation of protein tyrosine phophatases in vivo. Mol Cell 9, 387-399.
69. Molenaar, P., O'Reilly, G., Sharkey, A., Kuc, R.E., Harding, D.P., Plumpton, C., Gresham, G.A. & Davenport, A.P. 1993. Characterization and localization of endothelin receptor subtypes in the human atrioventricular conducting system and myocardium. Circ Res 72, 526-538.
70. +-exchanger in the rat myocardium by mitogen-activated protein kinase-dependent pathways. J Biol Chem 274, 22985-22992.
71. Morimoto, S. 2008. Sarcomeric proteins and inherited cardiomyopathies. Cardiovasc Res 77, 659-666.
72. 2+-pump dysfunction in rat cardiomyocytes briefly exposed to hydoxyl radicals. Free Radic Biol Med 22, 37-47.
73. Murdoch, C.E., Zhang, M., Cave, A.C. & Shah, A.M. 2006. NADPH oxidase-dependent redox signalling in cardiac hypertrophy, remodelling and failure. Cardiovasc Res 71, 208-215.
74. Murphy, A.J. 1976. Sulfhydryl group modification of sarcoplasmic reticulum membranes. Biochemistry 15, 4492-4496.
75. Nishida, M., Maruyama, Y., Tanaka, R., Kontani, K., Nagao, T. & Kurose, H. 2000. G alpha(i) and G alpha(o) are target proteins of reactive oxygen species. Nature 408, 492-495.
76. Nishimaru, K., Miura, Y. & Endoh, M. 2007. Mechanisms of endothelin-1-induced decrease in contractility in adult mouse ventricular myocytes. Br J Pharmacol 152, 456-463.
77. 2+ transients and cell shortening in mouse ventricular myocytes. J Mol Cell Cardiol 44, 520-526.
78. Nordberg, J. & Arner, E.S. 2001. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31, 1287-1312.
79. ATP channel opening. J Mol Cell Cardiol 35, 653-660.
80. Opie, L.H. 2002. The neuroendocrinology of congestive heart failure. Cardiovasc J S Afr 13, 171-178.
81. ATP channels triggers the preconditioned state by generating free radicals. Circ Res 87, 460-466.
82. Palomeque, J., Sapia, L., Hajjar, R.J., Mattiazzi, A. & Vila Petroff, M. 2006. Angiotensin II-induced negative inotropy in rat ventricular myocytes: role of reactive oxygen species and p38 MAPK. Am J Physiol Heart Circ Physiol 290, H96-H106.
83. Penna, C., Mancardi, D., Rastaldo, R. & Pagliaro, P. 2009. Cardioprotection: a radical view - free radicals in pre and postconditioning. Biochim Biophys Acta 1787, 781-793.
84. 2+ exchange after myocardial stretch: underlying mechanism of the slow force response. Circ Res 88, 376-382.
85. Persad, S., Elimban, V., Kaila, J. & Dhalla, N.S. 1997. Biphasic alterations in cardiac beta-adrenoceptor signal transduction mechanism due to oxyradicals. J Pharmacol Exp Ther 282, 1623-1631.
86. Petersen, A.C., McKenna, M.J., Medved, I., Murphy, K.T., Brown, M.J., Della Gatta, P. & Cameron-Smith, D. 2011. Infusion with the antioxidant N-acetylcysteine attenuates early adaptive responses to exercise in human skeletal muscle. Acta Physiol (Oxf), doi: 10.1111/j.1748-1716.2011.02344.x. [Epub ahead of print].
87. Pi, Y., Kemnitz, K.R., Zhang, D., Kranias, E.G. & Walker, J.W. 2002. Phosphorylation of troponin I controls cardiac twitch dynamics: evidence from phosphorylation site mutants expressed on a troponin I-null background in mice. Circ Res 90, 649-656.
88. Pieske, B., Beyermann, B., Breu, V., Loffler, B.M., Schlotthauer, K., Maier, L.S., Schmidt-Schweda, S., Just, H. & Hasenfuss, G. 1999. Functional effects of endothelin and regulation of endothelin receptors in isolated human nonfailing and failing myocardium. Circulation 99, 1802-1809.
89. Pimentel, D.R., Adachi, T., Ido, Y., Heibeck, T., Jiang, B., Lee, Y., Melendez, J.A., Cohen, R.a. & Colucci, W.S. 2006. Strain-stimulated hypertrophy in cardiac myocytes is mediated by reactive oxygen species-dependent Ras S-glutathiolation. J Mol Cell Cardiol 41, 613-622.
90. B receptors in regulation of cardiac contractile function in mice. Am J Physiol Heart Circ Physiol 285, H112-H118.
91. Piuhola, J., Szokodi, I., Kinnunen, P., Ilves, M., de Châtel, R., Vuolteenaho, O. & Ruskoaho, H. 2003b. Endothelin-1 contributes to the Frank-Starling response in hypertrophic rat hearts. Hypertension 41, 93-98.
92. Pourova, J., Kottova, M., Voprsalova, M. & Pour, M. 2010. Reactive oxygen and nitrogen species in normal physiological processes. Acta Physiol (Oxf) 198, 15-35.
93. Queliconi, B.B., Wojtovich, A.P., Nadtochiy, S.M., Kowaltowski, A.J. & Brookes, P.S. 2011. Redox regulation of the mitochondrial K(ATP) channel in cardioprotection. Biochim Biophys Acta 1813, 1309-1315.
94. Rao, V.S., La Bonte, L.R., Xu, Y., Yang, Z., French, B.A. & Guilford, W.H. 2007. Alterations to myofibrillar protein function in nonischemic regions of the heart early after myocardial infarction. Am J Physiol Heart Circ Physiol 293, H654-H659.
95. Reeves, J.P., Bailey, C.A. & Hale, C.C. 1986. Redox modification of sodium-calcium exchange activity in cardiac sarcolemmal vesicles. J Biol Chem 261, 4948-4955.
96. Rose, B.A., Force, T. & Wang, Y. 2010. Mitogen-activated protein kinase signaling in the heart: angels versus demons in a heart-breaking tale. Physiol Rev 90, 1507-1546.
97. Rubanyi, G.M. & Polokoff, M.A. 1994. Endothelins: molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol Rev 46, 325-415.
98. Saitoh, S.-I., Zhang, C., Tune, J.D., Potter, B., Kiyooka, T., Rogers, P.A., Knudson, J.D., Dick, G.M., Swafford, A. & Chilian, W.M. 2006. Hydrogen peroxide: a feed-forward dilator that couples myocardial metabolism to coronary blood flow. Arterioscler Thromb Vasc Biol 26, 2614-2621.
99. Salazar, N.C., Chen, J. & Rockman, H.A. 2007. Cardiac GPCRs: GPCR signaling in healthy and failing hearts. Biochim Biophys Acta 1768, 1006-1018.
100. Sanchez, G., Pedrozo, Z., Domenech, R.J., Hidalgo, C. & Donoso, P. 2005. Tachycardia increases NADPH oxidase activity and RyR2 S-glutathionylation in ventricular muscle. J Mol Cell Cardiol 39, 982-991.
101. Santos, C.X.C., Anilkumar, N., Zhang, M., Brewer, A.C. & Shah, A.M. 2011. Redox signaling in cardiac myocytes. Free Radic Biol Med 50, 777-793.
102. Saxena, S., Shukla, D., Saxena, S., Khan, Y.A., Singh, M., Bansal, A., Sairam, M. & Jain, S.K. 2010. Hypoxia preconditioning by cobalt chloride enhances endurance performance and protects skeletal muscles from exercise-induced oxidative damage in rats. Acta Physiol (Oxf) 200, 249-263.
103. 2+-ATPase. Arch Biochem Biophys 246, 589-601.
104. Shinke, T., Shite, J., Takaoka, H., Hata, K., Inoue, N., Yoshikawa, R., Matsumoto, H., Masai, H., Watanabe, S., Ozawa, T., Otake, H., Matsumoto, D., Hirata, K. & Yokoyama, M. 2007. Vitamin C restores the contractile response to dobutamine and improves myocardial efficiency in patients with heart failure after anterior myocardial infarction. Am Heart J 154, 645.e1-645.e8.
105. Snook, J.H., Li, J., Helmke, B.P. & Guilford, W.H. 2008. Peroxynitrite inhibits myofibrillar protein function in an in vitro assay of motility. Free Radic Biol Med 44, 14-23.
106. Solaro, R.J. 2008. Multiplex kinase signaling modifies cardiac function at the level of sarcomeric proteins. J Biol Chem 283, 26829-26833.
107. Sovershaev, M.A., Egorina, E.M., Andreasen, T.V., Jonassen, A.K. & Ytrehus, K. 2006. Preconditioning by 17-beta-estradiol in isolated rat heart depends on PI3-K/PKB pathway, PKC, and ROS. Am J Physiol Heart Circ Physiol 291, H1554-H1562.
108. Stolk, J., Hiltermann, T.J., Dijkman, J.H. & Verhoeven, A.J. 1994. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol. Am J Respir Cell Mol Biol 11, 95-102.
109. Sugden, P.H. 2003. An overview of endothelin signaling in the cardiac myocyte. J Mol Cell Cardiol 35, 871-886.
110. Sumandea, M.P. & Steinberg, S.F. 2011. Redox signaling and cardiac sarcomeres. J Biol Chem 286, 9921-9927.
111. Szokodi, I., Tavi, P., Földes, G., Voutilainen-myllylä, S., Ilves, M., Tokola, H., Pikkarainen, S., Piuhola, J., Rysä, J., Tóth, M. & Ruskoaho, H. 2002. Apelin, the novel endogenous ligand of the orphan receptor APJ, regulates cardiac contractility. Circ Res 91, 434-440.
112. Szokodi, I., Kerkelä, R., Kubin, A.-M., Sármán, B., Kónyi, A., Horváth, I.G., Papp, L., Tóth, M., Skoumal, R. & Ruskoaho, H. 2008. Functionally opposing roles of extracellular protein kinase in the regulation of cardiac contractility. Circulation 118, 1651-1658.
113. + exchanger isoform-1 kinase. J Biol Chem 274, 20206-20214.
114. Takeuchi, Y., Kihara, Y., Inagaki, K., Yoneda, T. & Sasayama, S. 2001. Endothelin-1 has a unique oxygen-saving effect by increasing contractile efficiency in the isolated rat heart. Circulation 103, 1557-1563.
115. Takimoto, E., Soergel, D.G., Janssen, P.M.L., Stull, L.B., Kass, D.A. & Murphy, A.M. 2004. Frequency- and afterload-dependent cardiac modulation in vivo by troponin I with constitutively active protein kinase A phosphorylation sites. Circ Res 94, 496-504.
116. Talukder, M., Norota, I., Sakurai, K. & Endoh, M. 2001. Inotropic response of rabbit ventricular myocytes to endothelin-1: difference from isolated papillary muscles. Am J Physiol Heart Circ Physiol 281, H596-H605.
117. Tang, W.H., Kravtsov, G.M., Sauert, M., Tong, X.Y., Hou, X.Y., Wong, T.M., Chung, S.K. & Man Chung, S.S. 2010. Polyol pathway impairs the function of SERCA and RyR in ischemic-reperfused rat hearts by increasing oxidative modifications of these proteins. J Mol Cell Cardiol 49, 58-69.
118. Tejero-Taldo, M.I., Caffrey, J.L., Sun, J. & Mallet, R.T. 1999. Antioxidant properties of pyruvate mediate its potentiation of beta-adrenergic inotropism in stunned myocardium. J Mol Cell Cardiol 31, 1863-1872.
119. Tian, J., Liu, J., Garlid, K.D., Shapiro, J.I. & Xie, Z. 2003. Involvement of mitogen-activated protein kinases and reactive oxygen species in the inotropic action of ouabain on cardiac myocytes. A potential role for mitochondrial K(ATP) channels. Mol Cell Biochem 242, 181-187.
120. Ukai, T., Cheng, C.P., Tachibana, H., Igawa, A., Zhang, Z.S., Cheng, H.J. & Little, W.C. 2001. Allopurinol enhances the contractile response to dobutamine and exercise in dogs with pacing-induced heart failure. Circulation 103, 750-755.
121. Ursini, F., Maiorino, M., Brigelius-Flohé, R., Aumann, K.D., Roveri, A., Schomburg, D. & Flohé, L. 1995. Diversity of glutathione peroxidases. Methods Enzymol 252, 38-53.
122. Villa-Abrille, M.C., Caldiz, C.I., Ennis, I.L., Nolly, M.B., Casarini, M.J., Chiappe de Cingolani, G.E., Cingolani, H.E. & Pérez, N.G. 2010. The Anrep effect requires transactivation of the epidermal growth factor receptor. J Physiol 588, 1579-1590.
123. 2+ signalling in rabbit ventricular myocytes. Br J Pharmacol 131, 638-644.
124. 2+ current in rabbit ventricular myocytes. Naunyn Schmiedeberg Arch Pharmacol 360, 654-664.
125. Wetzker, R. & Böhmer, F.D. 2003. Transactivation joins multiple tracks to the ERK/MAPK cascade. Nat Rev Mol Cell Biol 4, 651-657.
126. Wolska, B.M., Arteaga, G.M., Pena, J.R., Nowak, G., Phillips, R.M., Sahai, S., de Tombe, P.P., Martin, A.F., Kranias, E.G. & Solaro, R.J. 2002. Expression of slow skeletal troponin I in hearts of phospholamban knockout mice alters the relaxant effect of beta-adrenergic stimulation. Circ Res 90, 882-888.
127. Xiao, R., Zhu, W., Zheng, M., Cao, C. & Zhang, Y. 2006. Subtype-specific alpha-1- and beta-adrenoceptor signaling in the heart. Trends Pharmacol Sci 27, 330-337.
128. 2+-ATPase function by direct attack on the ATP binding site. Circ Res 80, 76-81.
129. Yanagisawa, M., Kurihara, H., Kimura, S., Tomobe, Y., Kobayashi, M., Mitsui, Y., Yazaki, Y., Goto, K. & Masaki, T. 1988. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332, 411-415.
130. 2+ transient and contractility in rabbit ventricular myocytes: pharmacological analysis with KB-R7943. Br J Pharmacol 126, 1785-1795.
131. Yusuf, S., Dagenais, G., Pogue, J., Bosch, J. & Sleight, P. 2000. Vitamin E supplementation and cardiovascular events in high risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med 342, 154-160.
132. Zeng, Q., Zhou, Q., Yao, F., O'Rourke, S.T. & 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.
133. Zima, A.V. & Blatter, L.A. 2006. Redox regulation of cardiac calcium channels and transporters. Cardiovasc Res 71, 310-321.
134. Zolk, O., Münzel, F. & Eschenhagen, T. 2004. Effects of chronic endothelin-1 stimulation on cardiac myocyte contractile function. Am J Physiol Heart Circ Physiol 286, H1248-H1257.
135. Zorov, D.B., Juhaszova, M. & Sollott, S.J. 2006. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta 1757, 509-517.