Mitochondrial reactive oxygen species (ROS) as signaling molecules of intracellular pathways triggered by the cardiac renin-angiotensin II-aldosterone system (RAAS)

Frontiers in Physiology

Volumn 4 MAY, Issue , 2013, Pages

  De Giusti, V C ^a   Caldiz, C I ^a   Ennis, I E ^a   Perez N G ^a   Cingolani, H E ^a   Aiello, E A ^a  

^a FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

Author keywords

Cardiac myocyte; Reactive oxygen species; Second messenger systems; Sodium bicarbonate symporters; Sodium hydrogen antiporter

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; ALDOSTERONE; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; ANTIOXIDANT; BICARBONATE SODIUM COTRANSPORTER; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CATALASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYTOCHROME C; ENDOTHELIN 1; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; G PROTEIN COUPLED RECEPTOR 30; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 1;

DRUG TARGETING; ENZYME ACTIVATION; HEART FAILURE; HEART LEFT VENTRICLE HYPERTROPHY; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION DISTURBANCE; HEART VENTRICLE HYPERTROPHY; HUMAN; NONHUMAN; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SIGNAL TRANSDUCTION;

EID: 84883802115     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00126     Document Type: Review

References (113)

1. Abadir, P. M., Foster, D. B., Crow, M., Cooke, C. A., Rucker, J. J., Jain, A., et al. (2011). Identification and characterization of a functional mitochondrial angiotensin system. Proc. Natl. Acad. Sci. U.S.A. 108, 14849-14854. doi: 10.1073/pnas.1101507108
2. Aiello, E. A., and De Giusti, V. C. (2012). Regulation of the cardiac sodium/bicarbonate cotransporter by angiotensin II: potential contribution to sodium and calcium overload. Curr. Cardiol. Rev. 9, 24-32. doi: 10.2174/1573403X11309010005
3. Aiello, E. A., Villa-Abrille, M. C., Dulce, R. A., Cingolani, H. E., and Perez, N. G. (2005). Endothelin-1 stimulates the Na+/Ca2+ exchanger reverse mode through intracellular Na+ (Na+i)-dependent and Na+i-independent pathways. Hypertension 45, 288-293. doi: 10.1161/01.HYP.0000152700.58940.b2
4. Andrukhiv, A., Costa, A. D., West, I. C., and 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. doi: 10.1152/ajpheart.00272.2006
5. Baetz, D., Haworth, R. S., Avkiran, M., and Feuvray, D. (2002). The ERK pathway regulates Na+-HCO3- cotransport activity in adult rat cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 283, H2102-H2109. doi: 10.1152/ajpheart.01071.2001
6. Bartosz, G. (2009). Reactive oxygen species: destroyers or messengers? Biochem. Pharmacol. 77, 1303-1315. doi: 10.1016/j.bcp.2008.11.009
7. Bedard, K., and Krause, K. H. (2007). The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313. doi: 10.1152/physrev.00044.2005
8. Bienert, G. P., Moller, A. L., Kristiansen, K. A., Schulz, A., Moller, I. M., Schjoerring, J. K., et al. (2007). Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282, 1183-1192. doi: 10.1074/jbc.M603761200
9. Bril, A. (2003). Ion transporters and cardiovascular diseases: pH control or modulation of intracellular calcium concentration. Ann. Cardiol. Angeiol. (Paris) 52, 41-51.
10. Brown, G. C., and Borutaite, V. (2012). There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells. Mitochondrion 12, 1-4. doi: 10.1016/j.mito.2011.02.001
11. Caldiz, C. I., Diaz, R. G., Nolly, M. B., Chiappe De Cingolani, G. E., Ennis, I. L., Cingolani, H. E., et al. (2011). Mineralocorticoid receptor activation is crucial in the signaling pathway leading to the Anrep effect. J. Physiol. 589, 6051-6061. doi: 10.1113/jphysiol.2011.218750
12. Caldiz, C. I., Garciarena, C. D., Dulce, R. A., Novaretto, L. P., Yeves, A. M., Ennis, I. L., et al. (2007). Mitochondrial reactive oxygen species activate the slow force response to stretch in feline myocardium. J. Physiol. 584, 895-905. doi: 10.1113/jphysiol.2007.141689
13. Camara, A. K., Lesnefsky, E. J., and Stowe, D. F. (2010). Potential therapeutic benefits of strategies directed to mitochondria. Antioxid. Redox Signal. 13, 279-347. doi: 10.1089/ars.2009.2788
14. Chai, W., and Danser, A. H. (2006). Why are mineralocorticoid receptor antagonists cardioprotective? Naunyn Schmiedebergs. Arch. Pharmacol. 374, 153-162. doi: 10.1007/s00210-006-0107-9
15. Chai, W., Garrelds, I. M., Arulmani, U., Schoemaker, R. G., Lamers, J. M., and Danser, A. H. (2005). Genomic and nongenomic effects of aldosterone in the rat heart: why is spironolactone cardioprotective? Br. J. Pharmacol. 145, 664-671. doi: 10.1038/sj.bjp.0706220
16. Choudhary, R., Baker, K. M., and Pan, J. (2008). All-trans retinoic acid prevents angiotensin II- and mechanical stretch-induced reactive oxygen species generation and cardiomyocyte apoptosis. J. Cell. Physiol. 215, 172-181. doi: 10.1002/jcp.21297
17. Cingolani, H. E., Ennis, I. L., Aiello, E. A., and Perez, N. G. (2011). Role of autocrine/paracrine mechanisms in response to myocardial strain. Pflugers Arch. 462, 29-38. doi: 10.1007/s00424-011-0930-9
18. Cingolani, H. E., Perez, N. G., Aiello, E. A., and De Hurtado, M. C. (2005). Intracellular signaling following myocardial stretch: an autocrine/paracrine loop. Regul. Pept. 128, 211-220. doi: 10.1016/j.regpep.2004.12.011
19. Cingolani, H. E., Perez, N. G., Aiello, E. A., Ennis, I. L., Garciarena, C. D., Villa-Abrille, M. C., et al. (2008). Early signals after stretch leading to cardiac hypertrophy. Key role of NHE-1. Front. Biosci. 13, 7096-7114. doi: 10.2741/3213
20. Cingolani, H. E., Perez, N. G., and Camilion De Hurtado, M. C. (2001). An autocrine/paracrine mechanism triggered by myocardial stretch induces changes in contractility. News Physiol. Sci. 16, 88-91.
21. Cingolani, H. E., Perez, N. G., Cingolani, O. H., and Ennis, I. L. (2013). The Anrep effect: 100 years later. Am. J. Physiol. Heart Circ. Physiol. 304, H175-H182. doi: 10.1152/ajpheart.00508.2012
22. Cingolani, H. E., Perez, N. G., Pieske, B., Von Lewinski, D., and Camilion De Hurtado, M. C. (2003). Stretch-elicited Na+/H+ exchanger activation: the autocrine/paracrine loop and its mechanical counterpart. Cardiovasc. Res. 57, 953-960. doi: 10.1016/S0008-6363(02)00768-X
23. Cingolani, H. E., Villa-Abrille, M. C., Cornelli, M., Nolly, A., Ennis, I. L., Garciarena, C., et al. (2006). The positive inotropic effect of angiotensin II: role of endothelin-1 and reactive oxygen species. Hypertension 47, 727-734. doi: 10.1161/01.HYP.0000208302.62399.68
24. Costa, A. D., and Garlid, K. D. (2008). Intramitochondrial signaling: interactions among mitoKATP, PKCepsilon, ROS, and MPT. Am. J. Physiol. Heart Circ. Physiol. 295, H874-H882. doi: 10.1152/ajpheart.01189.2007
25. Costa, A. D., Jakob, R., Costa, C. L., Andrukhiv, K., West, I. C., and Garlid, K. D. (2006). The mechanism by which the mitochondrial ATP-sensitive K+ channel opening and H2O2 inhibit the mitochondrial permeability transition. J. Biol. Chem. 281, 20801-20808. doi: 10.1074/jbc.M600959200
26. D'autreaux, B., and Toledano, M. B. (2007). ROS as signaling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell. Biol. 8, 813-824. doi: 10.1038/nrm2256
27. Dai, D. F., Johnson, S. C., Villarin, J. J., Chin, M. T., Nieves-Cintron, M., Chen, T., et al. (2011). Mitochondrial oxidative stress mediates angiotensin II-induced cardiac hypertrophy and Galphaq overexpression-induced heart failure. Circ. Res. 108, 837-846. doi: 10.1161/CIRCRESAHA.110.232306
28. Daiber, A. (2010). Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim. Biophys. Acta 1797, 897-906. doi: 10.1016/j.bbabio.2010.01.032
29. De Giusti, V. C., Correa, M. V., Villa-Abrille, M. C., Beltrano, C., Yeves, A. M., De Cingolani, G. E., et al. (2008). The positive inotropic effect of endothelin-1 is mediated by mitochondrial reactive oxygen species. Life Sci. 83, 264-271. doi: 10.1016/j.lfs.2008.06.008
30. De Giusti, V. C., Garciarena, C. D., and Aiello, E. A. (2009). Role of reactive oxygen species (ROS) in angiotensin II-induced stimulation of the cardiac Na+/HCO3- cotransport. J. Mol. Cell. Cardiol. 47, 716-722. doi: 10.1016/j.yjmcc.2009.07.023
31. De Giusti, V. C., Nolly, M. B., Yeves, A. M., Caldiz, C. I., Villa-Abrille, M. C., Chiappe De Cingolani, G. E., et al. (2011). Aldosterone stimulates the cardiac Na+/H+ exchanger via transactivation of the epidermal growth factor receptor. Hypertension 58, 912-919. doi: 10.1161/HYPERTENSIONAHA.111.176024
32. Dedkova, E. N., Seidlmayer, L. K., and Blatter, L. A. (2013). Mitochondria-mediated cardioprotection by trimetazidine in rabbit heart failure. J. Mol. Cell. Cardiol. 59C, 41-54. doi: 10.1016/j.yjmcc.2013.01.016
33. Diez, J. (2008). Effects of aldosterone on the heart: beyond systemic hemodynamics? Hypertension 52, 462-464. doi: 10.1161/HYPERTENSIONAHA.108.117044
34. Dikalov, S. (2011). Cross talk between mitochondria and NADPH oxidases. Free Radic. Biol. Med. 51, 1289-1301. doi: 10.1016/j.freeradbiomed.2011.06.033
35. Domenighetti, A. A., Boixel, C., Cefai, D., Abriel, H., and Pedrazzini, T. (2007). Chronic angiotensin II stimulation in the heart produces an acquired long QT syndrome associated with IK1 potassium current downregulation. J. Mol. Cell. Cardiol. 42, 63-70. doi: 10.1016/j.yjmcc.2006.09.019
36. Doughan, A. K., Harrison, D. G., and Dikalov, S. I. (2008). Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ. Res. 102, 488-496. doi: 10.1161/CIRCRESAHA.107.162800
37. Drose, S. (2013). Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning. Biochim. Biophys. Acta 1827, 578-587. doi: 10.1016/j.bbabio.2013.01.004
38. Ebata, S., Muto, S., Okada, K., Nemoto, J., Amemiya, M., Saito, T., et al. (1999). Aldosterone activates Na+/H+ exchange in vascular smooth muscle cells by nongenomic and genomic mechanisms. Kidney Int. 56, 1400-1412. doi: 10.1046/j.1523-1755.1999.00674.x
39. Ennis, I. L., Garciarena, C. D., Escudero, E. M., Perez, N. G., Dulce, R. A., Camilion De Hurtado, M. C., et al. (2007). Normalization of the calcineurin pathway underlies the regression of hypertensive hypertrophy induced by Na+/H+ exchanger-1 (NHE-1) inhibition. Can. J. Physiol. Pharmacol. 85, 301-310. doi: 10.1139/y06-072
40. Fischer, R., Dechend, R., Gapelyuk, A., Shagdarsuren, E., Gruner, K., Gruner, A., et al. (2007). Angiotensin II-induced sudden arrhythmic death and electrical remodeling. Am. J. Physiol. Heart Circ. Physiol. 293, H1242-H1253. doi: 10.1152/ajpheart.01400.2006
41. Fliegel, L., and Karmazyn, M. (2004). The cardiac Na-H exchanger: a key downstream mediator for the cellular hypertrophic effects of paracrine, autocrine and hormonal factors. Biochem. Cell. Biol. 82, 626-635. doi: 10.1139/o04-129
42. Garciarena, C. D., Caldiz, C. I., Correa, M. V., Schinella, G. R., Mosca, S. M., Chiappe De Cingolani, G. E., et al. (2008). Na+/H+ exchanger-1 inhibitors decrease myocardial superoxide production via direct mitochondrial action. J. Appl. Physiol. 105, 1706-1713. doi: 10.1152/japplphysiol.90616.2008
43. Giordano, F. J. (2005). Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest. 115, 500-508. doi: 10.1172/JCI24408
44. Gomez-Sanchez, E. P., Ahmad, N., Romero, D. G., and Gomez-Sanchez, C. E. (2004). Origin of aldosterone in the rat heart. Endocrinology 145, 4796-4802. doi: 10.1210/en.2004-0295
45. Gros, R., Ding, Q., Liu, B., Chorazyczewski, J., and Feldman, R. D. (2013). Aldosterone mediates its rapid effects in vascular endothelial cells through Gper/Gpr30 activation. Am. J. Physiol. Cell Physiol. 304, C532-C540. doi: 10.1152/ajpcell.00203.2012
46. Gros, R., Ding, Q., Sklar, L. A., Prossnitz, E. E., Arterburn, J. B., Chorazyczewski, J., et al. (2011). GPR30 expression is required for the mineralocorticoid receptor-independent rapid vascular effects of aldosterone. Hypertension 57, 442-451. doi: 10.1161/HYPERTENSIONAHA.110.161653
47. Grossmann, C., and Gekle, M. (2007). Non-classical actions of the mineralocorticoid receptor: misuse of EGF receptors? Mol. Cell. Endocrinol. 277, 6-12. doi: 10.1016/j.mce.2007.07.001
48. Grossmann, C., and Gekle, M. (2009). New aspects of rapid aldosterone signaling. Mol. Cell Endocrinol. 308, 53-62. doi: 10.1016/j.mce.2009.02.005
49. Grossmann, C., Husse, B., Mildenberger, S., Schreier, B., Schuman, K., and Gekle, M. (2010). Colocalization of mineralocorticoid and EGF receptor at the plasma membrane. Biochim. Biophys. Acta 1803, 584-590. doi: 10.1016/j.bbamcr.2010.02.008
50. Grossmann, C., Krug, A. W., Freudinger, R., Mildenberger, S., Voelker, K., and Gekle, M. (2007). Aldosterone-induced EGFR expression: interaction between the human mineralocorticoid receptor and the human EGFR promoter. Am. J. Physiol. Endocrinol. Metab. 292, E1790-E1800. doi: 10.1152/ajpendo.00708.2006
51. Gul, R., Shawl, A. I., Kim, S. H., and Kim, U. H. (2012). Cooperative interaction between reactive oxygen species and Ca2+ signals contributes to angiotensin II-induced hypertrophy in adult rat cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 302, H901-H909. doi: 10.1152/ajpheart.00250.2011
52. Guo, P., Nishiyama, A., Rahman, M., Nagai, Y., Noma, T., Namba, T., et al. (2006). Contribution of reactive oxygen species to the pathogenesis of left ventricular failure in Dahl salt-sensitive hypertensive rats: effects of angiotensin II blockade. J. Hypertens. 24, 1097-1104. doi: 10.1097/01.hjh.0000226200.73065.5d
53. Hanna, I. R., Taniyama, Y., Szocs, K., Rocic, P., and Griendling, K. K. (2002). NAD(P)H oxidase-derived reactive oxygen species as mediators of angiotensin II signaling. Antioxid. Redox. Signal. 4, 899-914. doi: 10.1089/152308602762197443
54. Hayashi, H., Kobara, M., Abe, M., Tanaka, N., Gouda, E., Toba, H., et al. (2008). Aldosterone nongenomically produces NADPH oxidase-dependent reactive oxygen species and induces myocyte apoptosis. Hypertens. Res. 31, 363-375. doi: 10.1291/hypres.31.363
55. Husain, A., Kinoshita, A., Sung, S. S., Urata, H., and Bumpus, F. M. (1994). "Human heart chymase," in The Cardiac Renin-Angiotensin System, ed G. D. E. Lindpaintner (Armonk, NY: Futura Publishing), 309-332.
56. Inagami, T. (2011). Mitochondrial angiotensin receptors and aging. Circ. Res. 109, 1323-1324. doi: 10.1161/RES.0b013e31823f05e0
57. Javadov, S., Choi, A., Rajapurohitam, V., Zeidan, A., Basnakian, A. G., and Karmazyn, M. (2008). NHE-1 inhibition-induced cardioprotection against ischaemia/reperfusion is associated with attenuation of the mitochondrial permeability transition. Cardiovasc. Res. 77, 416-424. doi: 10.1093/cvr/cvm039
58. Karmazyn, M., Liu, Q., Gan, X. T., Brix, B. J., and Fliegel, L. (2003). Aldosterone increases NHE-1 expression and induces NHE-1-dependent hypertrophy in neonatal rat ventricular myocytes. Hypertension 42, 1171-1176. doi: 10.1161/01.HYP.0000102863.23854.0B
59. Kimura, S., Zhang, G. X., Nishiyama, A., Shokoji, T., Yao, L., Fan, Y. Y., et al. (2005a). Mitochondria-derived reactive oxygen species and vascular MAP kinases: comparison of angiotensin II and diazoxide. Hypertension 45, 438-444. doi: 10.1161/01.HYP.0000157169.27818.ae
60. Kimura, S., Zhang, G. X., Nishiyama, A., Shokoji, T., Yao, L., Fan, Y. Y., et al. (2005b). 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. doi: 10.1161/01.HYP.0000163462.98381.7f
61. Kindler, D. D., Thiffault, C., Solenski, N. J., Dennis, J., Kostecki, V., Jenkins, R., et al. (2003). Neurotoxic nitric oxide rapidly depolarizes and permeabilizes mitochondria by dynamically opening the mitochondrial transition pore. Mol. Cell. Neurosci. 23, 559-573. doi: 10.1016/S1044-7431(03)00074-5
62. Krieg, T., Landsberger, M., Alexeyev, M. F., Felix, S. B., Cohen, M. V., and Downey, J. M. (2003). Activation of Akt is essential for acetylcholine to trigger generation of oxygen free radicals. Cardiovasc. Res. 58, 196-202. doi: 10.1016/S0008-6363(02)00861-1
63. Krieg, T., Qin, Q., Mcintosh, E. C., Cohen, M. V., and Downey, J. M. (2002). ACh and adenosine activate PI3-kinase in rabbit hearts through transactivation of receptor tyrosine kinases. Am. J. Physiol. Heart Circ. Physiol. 283, H2322-H2330. doi: 10.1152/ajpheart.00474.2002
64. Krieg, T., Qin, Q., Philipp, S., Alexeyev, M. F., Cohen, M. V., and Downey, J. M. (2004). Acetylcholine and bradykinin trigger preconditioning in the heart through a pathway that includes Akt and NOS. Am. J. Physiol. Heart Circ. Physiol. 287, H2606-H2611. doi: 10.1152/ajpheart.00600.2004
65. Kubin, A. M., Skoumal, R., Tavi, P., Konyi, A., Perjes, A., Leskinen, H., et al. (2011). Role of reactive oxygen species in the regulation of cardiac contractility. J. Mol. Cell. Cardiol. 50, 884-893. doi: 10.1016/j.yjmcc.2011.02.005
66. Lemarie, C. A., Paradis, P., and Schiffrin, E. L. (2008). New insights on signaling cascades induced by cross-talk between angiotensin II and aldosterone. J. Mol. Med. (Berl.) 86, 673-678. doi: 10.1007/s00109-008-0323-5
67. Li, L., Zhang, Z. G., Lei, H., Wang, C., Wu, L. P., Wang, J. Y., et al. (2013). Angiotensin II reduces cardiac AdipoR1 expression through AT1 receptor/ROS/ERK1/2/c-Myc pathway. PLoS ONE 8:e49915. doi: 10.1371/journal.pone.0049915
68. Maulik, S. K., and Kumar, S. (2012). Oxidative stress and cardiac hypertrophy: a review. Toxicol. Mech. Methods 22, 359-366. doi: 10.3109/15376516.2012.666650
69. Mehta, P. K., and Griendling, K. K. (2007). Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am. J. Physiol. Cell Physiol. 292, C82-C97. doi: 10.1152/ajpcell.00287.2006
70. Meyer, M. R., Prossnitz, E. R., and Barton, M. (2011). The G protein-coupled estrogen receptor GPER/GPR30 as a regulator of cardiovascular function. Vascul. Pharmacol. 55, 17-25. doi: 10.1016/j.vph.2011.06.003
71. Mihailidou, A. S., Mardini, M., and Funder, J. W. (2004). Rapid, nongenomic effects of aldosterone in the heart mediated by epsilon protein kinase C. Endocrinology 145, 773-780. doi: 10.1210/en.2003-1137
72. Miller, E. W., Dickinson, B. C., and Chang, C. J. (2010). Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc. Natl. Acad. Sci. U.S.A. 107, 15681-15686. doi: 10.1073/pnas.1005776107
73. Morgan, P. E., Correa, M. V., Ennis, I. L., Diez, A. A., Perez, N. G., and Cingolani, H. E. (2011). Silencing of sodium/hydrogen exchanger in the heart by direct injection of naked siRNA. J. Appl. Physiol. 111, 566-572. doi: 10.1152/japplphysiol.00200.2011
74. Nishio, S., Teshima, Y., Takahashi, N., Thuc, L. C., Saito, S., Fukui, A., et al. (2012). Activation of CaMKII as a key regulator of reactive oxygen species production in diabetic rat heart. J. Mol. Cell Cardiol. 52, 1103-1111. doi: 10.1016/j.yjmcc.2012.02.006
75. Oldenburg, O., Qin, Q., Krieg, T., Yang, X. M., Philipp, S., Critz, S. D., et al. (2004). Bradykinin induces mitochondrial ROS generation via NO, cGMP, PKG, and mitoKATP channel opening and leads to cardioprotection. Am. J. Physiol. Heart Circ. Physiol. 286, H468-H476. doi: 10.1152/ajpheart.00360.2003
76. Pain, T., Yang, X. M., Critz, S. D., Yue, Y., Nakano, A., Liu, G. S., et al. (2000). Opening of mitochondrial KATP channels triggers the preconditioned state by generating free radicals. Circ. Res. 87, 460-466. doi: 10.1161/01.RES.87.6.460
77. Palomeque, J., Delbridge, L., and Petroff, M. V. (2009). Angiotensin II: a regulator of cardiomyocyte function and survival. Front. Biosci. 14:5118-5133. doi: 10.2741/3590
78. Perez, N. G., De Hurtado, M. C., and Cingolani, H. E. (2001). Reverse mode of the Na+-Ca2+ exchange after myocardial stretch: underlying mechanism of the slow force response. Circ. Res. 88, 376-382. doi: 10.1161/01.RES.88.4.376
79. Perez, N. G., Villa-Abrille, M. C., Aiello, E. A., Dulce, R. A., Cingolani, H. E., and Camilion De Hurtado, M. C. (2003). A low dose of angiotensin II increases inotropism through activation of reverse Na+/Ca2+ exchange by endothelin release. Cardiovasc. Res. 60, 589-597. doi: 10.1016/j.cardiores.2003.09.004
80. Qin, W., Rudolph, A. E., Bond, B. R., Rocha, R., Blomme, E. A., Goellner, J. J., et al. (2003). Transgenic model of aldosterone-driven cardiac hypertrophy and heart failure. Circ. Res. 93, 69-76. doi: 10.1161/01.RES.0000080521.15238.E5
81. Rothstein, E. C., Byron, K. L., Reed, R. E., Fliegel, L., and Lucchesi, P. A. (2002). H2O2-induced Ca2+ overload in NRVM involves ERK1/2 MAP kinases: role for an NHE-1-dependent pathway. Am. J. Physiol. Heart Circ. Physiol. 283, H598-H605. doi: 10.1152/ajpheart.00198.2002
82. Sabri, A., Byron, K. L., Samarel, A. M., Bell, J., and Lucchesi, P. A. (1998). Hydrogen peroxide activates mitogen-activated protein kinases and Na+-H+ exchange in neonatal rat cardiac myocytes. Circ. Res. 82, 1053-1062. doi: 10.1161/01.RES.82.10.1053
83. Sadoshima, J., and Izumo, S. (1996). Autocrine secretion of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Contrib. Nephrol. 118, 214-221.
84. Sadoshima, J., Xu, Y., Slayter, H. S., and Izumo, S. (1993). Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell 75, 977-984. doi: 10.1016/0092-8674(93)90541-W
85. Sato, T., O'rourke, B., and Marban, E. (1998). Modulation of mitochondrial ATP-dependent K+ channels by protein kinase C. Circ. Res. 83, 110-114. doi: 10.1161/01.RES.83.1.110
86. Seshiah, P. N., Weber, D. S., Rocic, P., Valppu, L., Taniyama, Y., and Griendling, K. K. (2002). Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ. Res. 91, 406-413. doi: 10.1161/01.RES.0000033523.08033.16
87. Shah, B. H., and Catt, K. J. (2003). A central role of EGF receptor transactivation in angiotensin II-induced cardiac hypertrophy. Trends Pharmacol. Sci. 24, 239-244. doi: 10.1016/S0165-6147(03)00079-8
88. Silvestre, J. S., Heymes, C., Oubenaissa, A., Robert, V., Aupetit-Faisant, B., Carayon, A., et al. (1999). Activation of cardiac aldosterone production in rat myocardial infarction: effect of angiotensin II receptor blockade and role in cardiac fibrosis. Circulation 99, 2694-2701. doi: 10.1161/01.CIR.99.20.2694
89. Silvestre, J. S., Robert, V., Heymes, C., Aupetit-Faisant, B., Mouas, C., Moalic, J. M., et al. (1998). Myocardial production of aldosterone and corticosterone in the rat. Physiological regulation. J. Biol. Chem. 273, 4883-4891. doi: 10.1074/jbc.273.9.4883
90. Smaili, S. S., and Russell, J. T. (1999). Permeability transition pore regulates both mitochondrial membrane potential and agonist-evoked Ca2+ signals in oligodendrocyte progenitors. Cell. Calcium 26, 121-130. doi: 10.1054/ceca.1999.0061
91. Snabaitis, A. K., Hearse, D. J., and Avkiran, M. (2002). Regulation of sarcolemmal Na+/H+ exchange by hydrogen peroxide in adult rat ventricular myocytes. Cardiovasc. Res. 53, 470-480. doi: 10.1016/S0008-6363(01)00464-3
92. Song, Y. H., Choi, E., Park, S. H., Lee, S. H., Cho, H., Ho, W. K., et al. (2011). Sustained CaMKII activity mediates transient oxidative stress-induced long-term facilitation of L-type Ca2+ current in cardiomyocytes. Free Radic. Biol. Med. 51, 1708-1716. doi: 10.1016/j.freeradbiomed.2011.07.022
93. Sorescu, D., and Griendling, K. K. (2002). Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest. Heart Fail. 8, 132-140. doi: 10.1111/j.1527-5299.2002.00717.x
94. Szokodi, I., Kerkela, R., Kubin, A. M., Sarman, B., Pikkarainen, S., Konyi, A., et al. (2008). Functionally opposing roles of extracellular signal-regulated kinase 1/2 and p38 mitogen-activated protein kinase in the regulation of cardiac contractility. Circulation 118, 1651-1658. doi: 10.1161/CIRCULATIONAHA.107.758623
95. Takeda, Y., Yoneda, T., Demura, M., Miyamori, I., and Mabuchi, H. (2000). Cardiac aldosterone production in genetically hypertensive rats. Hypertension 36, 495-500. doi: 10.1161/01.HYP.36.4.495
96. Terentyev, D., Gyorke, I., Belevych, A. E., Terentyeva, R., Sridhar, A., Nishijima, Y., et al. (2008). Redox modification of ryanodine receptors contributes to sarcoplasmic reticulum Ca2+ leak in chronic heart failure. Circ. Res. 103, 1466-1472. doi: 10.1161/CIRCRESAHA.108.184457
97. Toda, T., Kadono, T., Hoshiai, M., Eguchi, Y., Nakazawa, S., Nakazawa, H., et al. (2007). Na+/H+ exchanger inhibitor cariporide attenuates the mitochondrial Ca2+ overload and PTP opening. Am. J. Physiol. Heart Circ. Physiol. 293, H3517-H3523. doi: 10.1152/ajpheart.00483.2006
98. Trebak, M., Ginnan, R., Singer, H. A., and Jourd'heuil, D. (2010). Interplay between calcium and reactive oxygen/nitrogen species: an essential paradigm for vascular smooth muscle signaling. Antioxid. Redox. Signal 12, 657-674. doi: 10.1089/ars.2009.2842
99. Varagic, J., and Frohlich, E. D. (2002). Local cardiac renin-angiotensin system: hypertension and cardiac failure. J. Mol. Cell Cardiol. 34, 1435-1442. doi: 10.1006/jmcc.2002.2075
100. Vaughan-Jones, R. D., Villafuerte, F. C., Swietach, P., Yamamoto, T., Rossini, A., and Spitzer, K. W. (2006). pH-Regulated Na+ influx into the mammalian ventricular myocyte: the relative role of Na+-H+ exchange and Na+-HCO Co-transport. J. Cardiovasc. Electrophysiol. 17(Suppl. 1), S134-S140. doi: 10.1111/j.1540-8167.2006.00394.x
101. Villa-Abrille, M. C., Caldiz, C. I., Ennis, I. L., Nolly, M. B., Casarini, M. J., Chiappe De Cingolani, G. E., et al. (2010). The Anrep effect requires transactivation of the epidermal growth factor receptor. J. Physiol. 588, 1579-1590. doi: 10.1113/jphysiol.2009.186619
102. Villa-Abrille, M. C., Cingolani, H. E., Garciarena, C. D., Ennis, I. L., and Aiello, E. A. (2006). [Angiotensin II-induced endothelin-1 release in cardiac myocytes]. Medicina (B Aires) 66, 229-236.
103. Wang, Y. H., Shi, C. X., Dong, F., Sheng, J. W., and Xu, Y. F. (2008). Inhibition of the rapid component of the delayed rectifier potassium current in ventricular myocytes by angiotensin II via the AT1 receptor. Br. J. Pharmacol. 154, 429-439. doi: 10.1038/bjp.2008.95
104. Wenzel, P., Mollnau, H., Oelze, M., Schulz, E., Wickramanayake, J. M., Muller, J., et al. (2008). First evidence for a crosstalk between mitochondrial and NADPH oxidase-derived reactive oxygen species in nitroglycerin-triggered vascular dysfunction. Antioxid. Redox. Signal. 10, 1435-1447. doi: 10.1089/ars.2007.1969
105. Wojtovich, A. P., Smith, C. O., Haynes, C. M., Nehrke, K. W., and Brookes, P. S. (2013). Physiological consequences of complex II inhibition for aging, disease, and the mKATP channel. Biochim. Biophys. Acta 1827 (5), 598-611. doi: 10.1016/j.bbabio.2012.12.007
106. Xiao, F., Puddefoot, J. R., Barker, S., and Vinson, G. P. (2004). Mechanism for aldosterone potentiation of angiotensin II-stimulated rat arterial smooth muscle cell proliferation. Hypertension 44, 340-345. doi: 10.1161/01.HYP.0000140771.21243.ed
107. Yoshida, K., Kim-Mitsuyama, S., Wake, R., Izumiya, Y., Izumi, Y., Yukimura, T., et al. (2005). Excess aldosterone under normal salt diet induces cardiac hypertrophy and infiltration via oxidative stress. Hypertens. Res. 28, 447-455. doi: 10.1291/hypres.28.447
108. Zeng, Q., Zhou, Q., Yao, F., O'rourke, S. T., and 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. doi: 10.1124/jpet.108.140301
109. Zhai, P., Galeotti, J., Liu, J., Holle, E., Yu, X., Wagner, T., et al. (2006). An angiotensin II type 1 receptor mutant lacking epidermal growth factor receptor transactivation does not induce angiotensin II-mediated cardiac hypertrophy. Circ. Res. 99, 528-536. doi: 10.1161/01.RES.0000240147.49390.61
110. Zhang, D. X., Chen, Y. F., Campbell, W. B., Zou, A. P., Gross, G. J., and Li, P. L. (2001). Characteristics and superoxide-induced activation of reconstituted myocardial mitochondrial ATP-sensitive potassium channels. Circ. Res. 89, 1177-1183. doi: 10.1161/hh2401.101752
111. Zhang, G. X., Lu, X. M., Kimura, S., and Nishiyama, A. (2007). Role of mitochondria in angiotensin II-induced reactive oxygen species and mitogen-activated protein kinase activation. Cardiovasc. Res. 76, 204-212. doi: 10.1016/j.cardiores.2007.07.014
112. Zhao, Z., Fefelova, N., Shanmugam, M., Bishara, P., Babu, G. J., and Xie, L. H. (2011). Angiotensin II induces afterdepolarizations via reactive oxygen species and calmodulin kinase II signaling. J. Mol. Cell Cardiol. 50, 128-136. doi: 10.1016/j.yjmcc.2010.11.001
113. Zorov, D. B., Filburn, C. R., Klotz, L. O., Zweier, J. L., and Sollott, S. J. (2000). Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial perme-ability transition in cardiac myo-cytes. J. Exp. Med. 192, 1001-1014. doi: 10.1084/jem.192.7.1001