NADPH oxidase-derived H 2O 2 contributes to angiotensin II-induced aldosterone synthesis in human and rat adrenal cortical cells

Antioxidants and Redox Signaling

Volumn 17, Issue 3, 2012, Pages 445-459

  Rajamohan, Senthilkumar B ^a   Raghuraman, Gayatri ^a   Prabhakar, Nanduri R ^a   Kumar, Ganesh K ^a  

^a University of Chicago   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDOSTERONE; ALDOSTERONE SYNTHASE; ANGIOTENSIN II; HYDROGEN PEROXIDE; MALONALDEHYDE; MESSENGER RNA; NUCLEAR RECEPTOR RELATED PROTEIN 1; PHOSPHOLIPASE C; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADRENAL CORTEX; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STEROIDOGENESIS; UPREGULATION;

ADRENAL CORTEX; ALDOSTERONE; ALDOSTERONE SYNTHASE; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANIMALS; ANTIOXIDANTS; CELL LINE, TUMOR; ENZYME INHIBITORS; GENE EXPRESSION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; HYDROGEN PEROXIDE; ISOENZYMES; MALE; MEMBRANE GLYCOPROTEINS; MITOCHONDRIA; NADPH OXIDASE; NITRIC OXIDE SYNTHASE; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ANGIOTENSIN; SUPEROXIDES; TYPE C PHOSPHOLIPASES; UP-REGULATION;

EID: 84860554783     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4176     Document Type: Article

References (53)

1. Bassett MH, Suzuki T, Sasano H, White PC, and Rainey WE. The orphan nuclear receptors NURR1 and NGFIB regulate adrenal aldosterone production. Mol Endocrinol 18: 279-290, 2004a. (Pubitemid 38183928)
2. Bassett MH, White PC, and Rainey WE. The regulation of aldosterone synthase expression. Mol Cell Endocrinol 217: 67-74, 2004b. (Pubitemid 38596630)
3. Bendall JK, Cave AC, Heymes C, Gall N, and Shah AM. Pivotal role of a gp91(phox)-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation 105: 293-296, 2002. (Pubitemid 34106175)
4. Bird IM, Hanley NA, Word RA, Mathis JM, McCarthy JL, Mason JI, and Rainey WE. Human NCI-H295 adrenocortical carcinoma cells: a model for angiotensin-II-responsive aldosterone secretion. Endocrinology 133: 1555-1561, 1993. (Pubitemid 23295179)
5. 2+ and aldosterone production in bovine adrenal glomerulosa cells. Evidence for a difference in the mode of action of angiotensin II and potassium. J Biol Chem 259: 8863-8869, 1984.
6. Catt KJ, Balla T, Baukal AJ, Hausdorff WP, and Aguilera G. Control of glomerulosa cell function by angiotensin II: transduction by G-proteins and inositol polyphosphates. Clin Exp Pharmacol Physiol 15: 501-515, 1988.
7. Chamulitrat W, Stremmel W, Kawahara T, Rokutan K, Fujii H, Wingler K, Schmidt HH, and Schmidt RA. Constitutive NADPH oxidase-like system containing gp91phox homologs in human keratinocytes. J Invest Dermatol 122: 1000-1009, 2004. (Pubitemid 38581003)
8. Dikalov SI, Dikalova AE, Bikineyeva AT, Schmidt HH, Harrison DG, and Griendling KK. Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production. Free Radic Biol Med 45: 1340-1351, 2008.
9. Doughan AK, Harrison DG, and Dikalov SI. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 102: 488-496, 2008. (Pubitemid 351651106)
10. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002. (Pubitemid 34654215)
11. Eid AA, Gorin Y, Fagg BM, Maalouf R, Barnes JL, Block K, and Abboud HE. Mechanisms of podocyte injury in diabetes: role of cytochrome P450 and NADPH oxidases. Diabetes 58: 1201-1211, 2009.
12. Garrido AM and Griendling KK. NADPH oxidases and angiotensin II receptor signaling. Mol Cell Endocrinol 302: 148-158, 2009.
13. Griendling KK, Minieri CA, Ollerenshaw JD, and Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74: 1141-1148, 1994. (Pubitemid 24176909)
14. Griendling KK, Sorescu D, and Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86: 494-501, 2000. (Pubitemid 30165039)
15. Groemping Y and Rittinger K. Activation and assembly of the NADPH oxidase: a structural perspective. Biochem J 386: 401-416, 2005. (Pubitemid 40445864)
16. Gu J, Wen Y, Mison A, and Nadler JL. 12-lipoxygenase pathway increases aldosterone production, 3,5-cyclic adenosine monophosphate response element-binding protein phosphorylation, and p38 mitogen-activated protein kinase activation in H295R human adrenocortical cells. Endocrinology 144: 534-543, 2003. (Pubitemid 36205225)
17. Hanna IR, Taniyama Y, Szöcs K, Rocic P, and Griendling KK. NAD(P)H oxidase-derived reactive oxygen species as mediators of angiotensin II signaling. Antioxid Redox Signal 4: 899-914, 2002. (Pubitemid 36042466)
18. Heumüller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schröder K, and Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51: 211-217, 2008. (Pubitemid 351159930)
19. Jaimes EA, Galceran JM, and Raij L. Angiotensin II induces superoxide anion production by mesangial cells. Kidney Int 54: 775-784, 1998. (Pubitemid 28397395)
20. Kearney PM, Whelton M, Reynolds K, Muntner P, Whelton PK, and He J. Global burden of hypertension: analysis of worldwide data. Lancet 365: 217-223, 2005. (Pubitemid 40138015)
21. Kimura S, Zhang GX, Nishiyama A, Shokoji T, Yao L, Fan YY, Rahman M, Suzuki T, Maeta H, and Abe Y. 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, 2005. (Pubitemid 40628929)
22. Levine RL, Garland D, Oliver CN, Amici A, Climent J, Lenz AG, Ahn BW, Shaltiel S, and Stadtman ER. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186: 464-478, 1990. (Pubitemid 20279989)
23. Lijnen PJ, van Pelt JF, and Fagard RH. Downregulation of manganese superoxide dismutase by angiotensin II in cardiac fibroblasts of rats: association with oxidative stress in myocardium. Am J Hypertens 23: 1128-1135, 2010.
24. Lisurek M and Bernhardt R. Modulation of aldosterone and cortisol synthesis on the molecular level. Mol Cell Endocrinol 215: 149-159, 2004. (Pubitemid 38333254)
25. Liu D, Jia H, Holmes DIR, Stannard A, and Zachary I. Vascular endothelial growth factor-regulated gene expression in endothelial cells. Arterioscler Thromb Vasc Biol 23: 2002-2007, 2003.
26. Nogueira EF and Rainey WE. Regulation of aldosterone synthase by activator transcription factor/cAMP response element-binding protein family members. Endocrinology 151: 1060-1070, 2010.
27. Nogueira EF, Bollag WB, and Rainey WE. Angiotensin II regulation of adrenocortical gene transcription. Mol Cell Endocrinol 302: 230-236, 2009a.
28. Nogueira EF, Vargas CA, Otis M, Gallo-Payet N, Bollag WB, and Rainey WE. Angiotensin-II acute regulation of rapid response genes in human, bovine, and rat adrenocortical cells. J Mol Endocrinol 39: 365-374, 2007.
29. Nogueira EF, Xing Y, Morris CA, and Rainey WE. Role of angiotensin II-induced rapid response genes in the regulation of enzymes needed for aldosterone synthesis. J Mol Endocrinol 42: 319-330, 2009b.
30. Paulis L and Unger T. Novel therapeutic targets for hypertension. Nat Rev Cardiol 7: 431-441, 2010.
31. Raff H, Ball DL, and Goodfriend TL. Low oxygen selectively inhibits aldosterone secretion from bovine adrenocortical cells in vitro. Am J Physiol 256: E640-E644, 1989.
32. Raghuraman G, Kalari A, Dhingra R, Prabhakar NR, and Kumar GK. Enhanced neuropeptide Y synthesis during intermittent hypoxia in the rat adrenal medulla: role of reactive oxygen species-dependent alterations in precursor peptide processing. Antioxid Redox Signal 14: 1179-1190, 2011.
33. Raghuraman G, Prabhakar NR, and Kumar GK. Posttranslational modification of glutamic acid decarboxylase 67 by intermittent hypoxia: evidence for the involvement of dopamine D1 receptor signaling. J Neurochem 115: 1568-1578, 2010.
34. Rainey WE, Bird IM, and Mason JI. The NCI-H295 cell line: a pluripotent model for human adrenocortical studies. Mol Cell Endocrinol 100: 45-50, 1994. (Pubitemid 24109525)
35. Rajagopalan S, Kurz S, Münzel T, Tarpey M, Freeman BA, Griendling KK, and Harrison DG. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation Contribution to alterations of vasomotor tone. J Clin Invest 97: 1916-1923, 1996.
36. Rigel DF, Fu F, Beil M, Hu C-W, Liang G, and Jeng AY. Pharmacodynamic and pharmacokinetic characterization of the aldosterone synthase inhibitor FAD286 in two rodent models of hyperaldosteronism: comparison with the 11βhydroxylase inhibitor metyrapone. J Pharmacol Exp Ther 334: 232-243, 2010.
37. Rodríguez-Puyol M, Griera-Merino M, Pérez-Rivero G, Díez-Marqués ML, Ruiz-Torres MP, and Rodríguez-Puyol D. Ang II induces a rapid and transient increase of reactive oxygen species. Antioxid Redox Signal 4: 869-875, 2002. (Pubitemid 36042462)
38. Romero DG, Rilli S, Plonczynski MW, Yanes LL, Zhou MY, Gomez-Sanchez EP, and Gomez-Sanchez CE. Adrenal transcription regulatory genes modulated by angiotensin II and their role in steroidogenesis. Physiol Genomics 30: 26-34, 2007. (Pubitemid 47173286)
39. Schalekamp MA, Wenting GJ, and Man in't Veld AJ. Pathogenesis of mineralocorticoid hypertension. Clin Endocrinol Metab 10: 397-418, 1981.
40. Shen WL, Gao PJ, Che ZQ, Ji KD, Yin M, Yan C, Berk BC, and Zhu DL. NADPH oxidase-derived reactive oxygen species regulate angiotensin II-induced adventitial fibroblast phenotypic differentiation. Biochem Biophys Res Commun 339: 337-343, 2006. (Pubitemid 41697555)
41. Sirianni R, Carr BR, Pezzi V, and Rainey WE. A role for src tyrosine kinase in regulating adrenal aldosterone production. J Mol Endocrinol 26: 207-215, 2001. (Pubitemid 32514611)
42. Szekeres M, Turu G, Orient A, Szalai B, Supeki K, Cserzo M, Varnai P, and Hunyady L. Mechanisms of angiotensin II-mediated regulation of aldosterone synthase expression in H295R human adrenocortical and rat adrenal glomerulosa cells. Mol Cell Endocrinol 302: 244-253, 2009.
43. ten Freyhaus H, Huntgeburth M, Wingler K, Schnitker J, Bäumer AT, Vantler M, Bekhite MM, Wartenberg M, Sauer H, and Rosenkranz S. Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation. Cardiovasc Res 71: 331-341, 2006.
44. Tomaschitz A, Pilz S, Ritz E, Obermayer-Pietsch B, and Pieberet TR. Aldosterone and arterial hypertension. Nat Rev Endocrinol 6: 83-93, 2010.
45. Touyz RM and Schiffrin EL. Ang II-stimulated superoxide production is mediated via phospholipase D in human vascular smooth muscle cells. Hypertension 34: 976-982, 1999. (Pubitemid 29501333)
46. Touyz RM, Yao G, Viel E, Amiri F, and Schiffrin EL. Angiotensin II and endothelin-1 regulate MAP kinases through different redox-dependent mechanisms in human vascular smooth muscle cells. J Hypertens 22: 1141-1149, 2004. (Pubitemid 38721006)
47. Ulick S. Selective defects in the biosynthesis of aldosterone. In: Adrenal Diseases in Childhood, edited by New MI, Levine LS, and Laron Z. Basel, Switzerland: Karger, 1984, pp.145-155.
48. Vallotton MB, Rossier MF, and Capponi AM. Potassium-angiotensin interplay in the regulation of aldosterone biosynthesis. Clin Endocrinol 42: 111-119, 1995.
49. Wu S, Gao J, Ohlemeyer C, Roos D, Niessen H, Köttgen E, and Gessner R. Activation of AP-1 through reactive oxygen species by angiotensin II in rat cardiomyocytes. Free Radic Biol Med 39: 1601-1610, 2005. (Pubitemid 41642591)
50. Yamashiro T, Kuge H, Zhang J, and Honke K. Calcineurin mediates the angiotensin II-induced aldosterone synthesis in the adrenal glands by up- regulation of transcription of the CYP11B2 gene. J Biochem 48: 115-123, 2010.
51. Yang W, Zhang J, Wang H, Gao P, Singh M, Shen K, and Fang N. Angiotensin II downregulates catalase expression and activity in vascular adventitial fibroblasts through an AT1R/ERK1/2-dependent pathway. Mol Cell Biochem 358: 21-29, 2011.
52. 2 in angiotensin II-induced vascular hypertrophy. Hypertension 32: 488-495, 1998.
53. Zhou M, Diwu Z, Panchuk-Voloshina N, and Haugland RP. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal Biochem 253: 162-168, 1997. (Pubitemid 27508167)