The signaling pathway for aldosterone-induced mitochondrial production of superoxide anion in the myocardium

Journal of Molecular and Cellular Cardiology

Volumn 67, Issue , 2014, Pages 60-68

  Nolly, M B ^a   Caldiz, C I ^a   Yeves, A M ^a   Villa Abrille, M C ^a   Morgan, P E ^a   Amado Mondaca, Nicolas ^a   Portiansky, Enrique L ^a   Chiappe de Cingolani, G E ^a   Cingolani, H E ^a   Ennis, I L ^a  

^a UNIVERSIDAD NACIONAL DE LA PLATA   (Argentina)

Author keywords

Mineralocorticoid receptor; Oxidative stress; SiRNA; Transactivation

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; ALDOSTERONE; APOCYNIN; BONGKREKIC ACID; CYCLOSPORIN A; DIAZOXIDE; EPIDERMAL GROWTH FACTOR RECEPTOR; EPLERENONE; GLIBENCLAMIDE; LENTIVIRUS VECTOR; MINERALOCORTICOID RECEPTOR; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROTENONE; SMALL INTERFERING RNA; SPIRONOLACTONE; SUPEROXIDE; WORTMANNIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME SYNTHESIS; GENETIC CODE; HEART MITOCHONDRION; HEART MUSCLE; HORMONE ACTION; HORMONE INHIBITION; INTRACELLULAR SIGNALING; MALE; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; RECEPTOR BLOCKING; RESPIRATORY CHAIN;

5-HD; 5-HYDROXYDECANOATE; CSA; CYCLOSPORINE A; DHE; DIHYDROETHIDIUM; EGFR; EPIDERMAL GROWTH FACTOR RECEPTOR; HEART FAILURE; HF; MINERALOCORTICOID RECEPTOR; MITOCHONDRIAL ATP-DEPENDENT POTASSIUM; MK(ATP); MPT; MR; OXIDATIVE STRESS; PERMEABILITY TRANSITION PORE; REACTIVE OXYGEN SPECIES; ROS; SIRNA; TRANSACTIVATION;

ALDOSTERONE; ANIMALS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; MITOCHONDRIA; MODELS, BIOLOGICAL; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SUPEROXIDES;

EID: 84892847812     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.12.004     Document Type: Article

References (59)

1. Pitt B., Zannad F., Remme W.J., Cody R., Castaigne A., Perez A., et al. The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N Engl J Med 1999, 341:709-717.
2. Pitt B., Remme W., Zannad F., Neaton J., Martinez F., Roniker B., et al. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med 2003, 348:1309-1321.
3. Zannad F., McMurray J.J., Krum H., van Veldhuisen D.J., Swedberg K., Shi H., et al. Eplerenone in patients with systolic heart failure and mild symptoms. N Engl J Med 2011, 364:11-21.
4. Martinez F.A. Aldosterone inhibition and cardiovascular protection: more important than it once appeared. Cardiovasc Drugs Ther 2010, 24:345-350.
5. Grossmann C., Gekle M. New aspects of rapid aldosterone signaling. Mol Cell Endocrinol 2009, 308:53-62.
6. Giordano F.J. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 2005, 115:500-508.
7. Gonzalez D.R., Treuer A.V., Castellanos J., Dulce R.A., Hare J.M. Impaired S-nitrosylation of the ryanodine receptor caused by xanthine oxidase activity contributes to calcium leak in heart failure. J Biol Chem 2010, 285:28938-28945.
8. Cingolani H.E., Plastino J.A., Escudero E.M., Mangal B., Brown J., Perez N.G. The effect of xanthine oxidase inhibition upon ejection fraction in heart failure patients: La Plata Study. J Card Fail 2006, 12:491-498.
9. Tamariz L., Harzand A., Palacio A., Verma S., Jones J., Hare J. Uric acid as a predictor of all-cause mortality in heart failure: a meta-analysis. Congest Heart Fail 2011, 17:25-30.
10. Rude M.K., Duhaney T.A., Kuster G.M., Judge S., Heo J., Colucci W.S., et al. Aldosterone stimulates matrix metalloproteinases and reactive oxygen species in adult rat ventricular cardiomyocytes. Hypertension 2005, 46:555-561.
11. Hayashi H., Kobara M., Abe M., Tanaka N., Gouda E., Toba H., et al. Aldosterone nongenomically produces NADPH oxidase-dependent reactive oxygen species and induces myocyte apoptosis. Hypertens Res 2008, 31:363-375.
12. Fraccarollo D., Berger S., Galuppo P., Kneitz S., Hein L., Schutz G., et al. Deletion of cardiomyocyte mineralocorticoid receptor ameliorates adverse remodeling after myocardial infarction. Circulation 2011, 123:400-408.
13. Zhu X., Manning R.D., Lu D., Gomez-Sanchez C.E., Fu Y., Juncos L.A., et al. Aldosterone stimulates superoxide production in macula densa cells. Am J Physiol Renal Physiol 2011, 301:F529-F535.
14. Perez N.G., Nolly M.B., Roldan M.C., Villa-Abrille M.C., Cingolani E., Portiansky E.L., et al. Silencing of NHE-1 blunts the slow force response to myocardial stretch. J Appl Physiol 2011, 111:874-880.
15. Wang X., Skelley L., Cade R., Sun Z. AAV delivery of mineralocorticoid receptor shRNA prevents progression of cold-induced hypertension and attenuates renal damage. Gene Ther 2006, 13:1097-1103.
16. Caldiz C.I., Garciarena C.D., Dulce R.A., Novaretto L.P., Yeves A.M., Ennis I.L., et al. Mitochondrial reactive oxygen species activate the slow force response to stretch in feline myocardium. J Physiol 2007, 584:895-905.
17. Aiello E.A., Cingolani H.E. Angiotensin II stimulates cardiac L-type Ca(2+) current by a Ca(2+)- and protein kinase C-dependent mechanism. Am J Physiol 2001, 280:H1528-H1536.
18. Li Y., Zhu H., Kuppusamy P., Roubaud V., Zweier J.L., Trush M.A. Validation of lucigenin (bis-N-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J Biol Chem 1998, 273:2015-2023.
19. Gioda C.R., de Oliveira Barreto T., Primola-Gomes T.N., de Lima D.C., Campos P.P., Capettini Ldos S., et al. Cardiac oxidative stress is involved in heart failure induced by thiamine deprivation in rats. Am J Physiol 2010, 298:H2039-H2045.
20. Chai W., Garrelds I.M., Arulmani U., Schoemaker R.G., Lamers J.M., Danser A.H. Genomic and nongenomic effects of aldosterone in the rat heart: why is spironolactone cardioprotective?. Br J Pharmacol 2005, 145:664-671.
21. Maron B.A., Zhang Y.Y., Handy D.E., Beuve A., Tang S.S., Loscalzo J., et al. Aldosterone increases oxidant stress to impair guanylyl cyclase activity by cysteinyl thiol oxidation in vascular smooth muscle cells. J Biol Chem 2009, 284:7665-7672.
22. Gros R., Ding Q., Sklar L.A., Prossnitz E.E., Arterburn J.B., Chorazyczewski J., et al. GPR30 expression is required for the mineralocorticoid receptor-independent rapid vascular effects of aldosterone. Hypertension 2011, 57:442-451.
23. Mihailidou A.S., Loan Le T.Y., Mardini M., Funder J.W. Glucocorticoids activate cardiac mineralocorticoid receptors during experimental myocardial infarction. Hypertension 2009, 54:1306-1312.
24. Kizana E., Chang C.Y., Cingolani E., Ramirez-Correa G.A., Sekar R.B., Abraham M.R., et al. Gene transfer of connexin43 mutants attenuates coupling in cardiomyocytes: novel basis for modulation of cardiac conduction by gene therapy. Circ Res 2007, 100:1597-1604.
25. Kimura S., Zhang G.X., Nishiyama A., Shokoji T., Yao L., Fan Y.Y., et al. Role of NAD(P)H oxidase- and mitochondria-derived reactive oxygen species in cardioprotection of ischemic reperfusion injury by angiotensin II. Hypertension 2005, 45:860-866.
26. Weinbrenner C., Liu G.S., Downey J.M., Cohen M.V. Cyclosporine A limits myocardial infarct size even when administered after onset of ischemia. Cardiovasc Res 1998, 38:676-684.
27. Brandes R.P. Triggering mitochondrial radical release: a new function for NADPH oxidases. Hypertension 2005, 45:847-848.
28. 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 MPT in cardiac myocytes. J Exp Med 2000, 192:1001-1014.
29. Lemarie C.A., Paradis P., Schiffrin E.L. New insights on signaling cascades induced by cross-talk between angiotensin II and aldosterone. J Mol Med 2008, 86:673-678.
30. Montezano A.C., Callera G.E., Yogi A., He Y., Tostes R.C., He G., et al. Aldosterone and angiotensin II synergistically stimulate migration in vascular smooth muscle cells through c-Src-regulated redox-sensitive RhoA pathways. Arterioscler Thromb Vasc Biol 2008, 28:1511-1518.
31. Huang S., Zhang A., Ding G., Chen R. Aldosterone-induced mesangial cell proliferation is mediated by EGF receptor transactivation. Am J Physiol Renal Physiol 2009, 296:F1323-F1333.
32. De Giusti V.C., Nolly M.B., Yeves A.M., Caldiz C.I., Villa-Abrille M.C., Chiappe de Cingolani G.E., et al. Aldosterone stimulates the cardiac Na(+)/H(+) exchanger via transactivation of the epidermal growth factor receptor. Hypertension 2011, 58:912-919.
33. Seshiah P.N., Weber D.S., Rocic P., Valppu L., Taniyama Y., Griendling K.K. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ Res 2002, 91:406-413.
34. Krieg T., Cui L., Qin Q., Cohen M.V., Downey J.M. Mitochondrial ROS generation following acetylcholine-induced EGF receptor transactivation requires metalloproteinase cleavage of proHB-EGF. J Mol Cell Cardiol 2004, 36:435-443.
35. Doughan A.K., Harrison D.G., Dikalov S.I. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 2008, 102:488-496.
36. Downey J.M., Krieg T., Cohen M.V. Mapping preconditioning's signaling pathways: an engineering approach. Ann N Y Acad Sci 2008, 1123:187-196.
37. Costa A.D., Quinlan C.L., Andrukhiv A., West I.C., Jaburek M., Garlid K.D. The direct physiological effects of mitoK(ATP) opening on heart mitochondria. Am J Physiol 2006, 290:H406-H415.
38. Garciarena C.D., Caldiz C.I., Correa M.V., Schinella G.R., Mosca S.M., Chiappe de Cingolani G.E. Na+/H+ exchanger-1 inhibitors decrease myocardial superoxide production via direct mitochondrial action. J Appl Physiol 2008, 105:1706-1713.
39. Wang W., Fang H., Groom L., Cheng A., Zhang W., Liu J., et al. Superoxide flashes in single mitochondria. Cell 2008, 134:279-290.
40. Touyz R.M., Wu X.H., He G., Salomon S., Schiffrin E.L. Increased angiotensin II-mediated Src signaling via epidermal growth factor receptor transactivation is associated with decreased C-terminal Src kinase activity in vascular smooth muscle cells from spontaneously hypertensive rats. Hypertension 2002, 39:479-485.
41. Villa-Abrille M.C., Caldiz C.I., Ennis I.L., Nolly M.B., Casarini M.J., de Cingolani GE Chiappe, et al. The Anrep effect requires transactivation of the epidermal growth factor receptor. J Physiol 2010, 588:1579-1590.
42. Ulu N., Henning R.H., Guner S., Zoto T., Duman-Dalkilic B., Duin M., et al. Intracellular transactivation of epidermal growth factor receptor by alpha1A-adrenoceptor is mediated by phosphatidylinositol 3-kinase independently of activation of extracellular signal regulated kinases 1/2 and serine-threonine kinases in Chinese hamster ovary cells. J Pharmacol Exp Ther 2013, 347:47-56.
43. Ohtsu H., Dempsey P.J., Eguchi S. ADAMs as mediators of EGF receptor transactivation by G protein-coupled receptors. Am J Physiol Cell Physiol 2006, 291:C1-C10.
44. Dikalov S., Griendling K.K., Harrison D.G. Measurement of reactive oxygen species in cardiovascular studies. Hypertension 2007, 49:717-727.
45. Hoyal C.R., Gutierrez A., Young B.M., Catz S.D., Lin J.H., Tsichlis P.N., et al. Modulation of p47PHOX activity by site-specific phosphorylation: Akt-dependent activation of the NADPH oxidase. Proc Natl Acad Sci U S A 2003, 100:5130-5135.
46. Maejima Y., Kuroda J., Matsushima S., Ago T., Sadoshima J. Regulation of myocardial growth and death by NADPH oxidase. J Mol Cell Cardiol 2011, 50:408-416.
47. 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 2010, 106:1253-1264.
48. Oakley F.D., Abbott D., Li Q., Engelhardt J.F. Signaling components of redox active endosomes: the redoxosomes. Antioxid Redox Signal 2009, 11:1313-1333.
49. Zhang D.X., Chen Y.F., Campbell W.B., Zou A.P., Gross G.J., Li P.L. Characteristics and superoxide-induced activation of reconstituted myocardial mitochondrial ATP-sensitive potassium channels. Circ Res 2001, 89:1177-1183.
50. Krieg T., Landsberger M., Alexeyev M.F., Felix S.B., Cohen M.V., Downey J.M. Activation of Akt is essential for acetylcholine to trigger generation of oxygen free radicals. Cardiovasc Res 2003, 58:196-202.
51. Krieg T., Qin Q., McIntosh E.C., Cohen M.V., Downey J.M. ACh and adenosine activate PI3-kinase in rabbit hearts through transactivation of receptor tyrosine kinases. Am J Physiol 2002, 283:H2322-H2330.
52. Krieg T., Qin Q., Philipp S., Alexeyev M.F., Cohen M.V., Downey J.M. Acetylcholine and bradykinin trigger preconditioning in the heart through a pathway that includes Akt and NOS. Am J Physiol 2004, 287:H2606-H2611.
53. Baartscheer A., Hardziyenka M., Schumacher C.A., Belterman C.N., van Borren M.M., Verkerk A.O., et al. Chronic inhibition of the Na+/H+-exchanger causes regression of hypertrophy, heart failure, and ionic and electrophysiological remodelling. Br J Pharmacol 2008, 154:1266-1275.
54. Engelhardt S., Hein L., Keller U., Klambt K., Lohse M.J. Inhibition of Na(+)-H(+) exchange prevents hypertrophy, fibrosis, and heart failure in beta(1)-adrenergic receptor transgenic mice. Circ Res 2002, 90:814-819.
55. Nakamura T.Y., Iwata Y., Arai Y., Komamura K., Wakabayashi S. Activation of Na+/H+ exchanger 1 is sufficient to generate Ca2+ signals that induce cardiac hypertrophy and heart failure. Circ Res 2008, 103:891-899.
56. Cook A.R., Bardswell S.C., Pretheshan S., Dighe K., Kanaganayagam G.S., Jabr R.I., et al. Paradoxical resistance to myocardial ischemia and age-related cardiomyopathy in NHE1 transgenic mice: a role for ER stress?. J Mol Cell Cardiol 2009, 46:225-233.
57. Garciarena C.D., Fantinelli J.C., Caldiz C.I., Chiappe de Cingolani G., Ennis I.L., Perez N.G., et al. Myocardial reperfusion injury: reactive oxygen species vs. NHE-1 reactivation. Cell Physiol Biochem 2011, 27:13-22.
58. Sabri A., Byron K.L., Samarel A.M., Bell J., Lucchesi P.A. Hydrogen peroxide activates mitogen-activated protein kinases and Na+-H+ exchange in neonatal rat cardiac myocytes. Circ Res 1998, 82:1053-1062.
59. Saotome M., Katoh H., Yaguchi Y., Tanaka T., Urushida T., Satoh H., et al. Transient opening of mitochondrial permeability transition pore by reactive oxygen species protects myocardium from ischemia-reperfusion injury. Am J Physiol 2009, 296:H1125-H1132.