Upregulation of steroidogenic acute regulatory protein by hypoxia stimulates aldosterone synthesis in pulmonary artery endothelial cells to promote pulmonary vascular fibrosis

Circulation

Volumn 130, Issue 2, 2014, Pages 168-179

  Maron, Bradley A ^a,b   Oldham, William M ^a   Chan, Stephen Y ^a   Vargas, Sara O ^c   Arons, Elena ^a   Zhang, Ying Yi ^a   Loscalzo, Joseph ^a   Leopold, Jane A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Aldosterone; Cell hypoxia; Fibrosis; Hypertension; Pulmonary

Indexed keywords

ALDOSTERONE; ALDOSTERONE SYNTHASE; CHOLESTEROL; COLLAGEN TYPE 3; CONNECTIVE TISSUE GROWTH FACTOR; ENDOTHELIN 1; EPLERENONE; GELATINASE A; GELATINASE B; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN C FOS; PROTEIN C JUN; PROTEIN INHIBITOR; SEMAXANIB; SMALL INTERFERING RNA; SPIRONOLACTONE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TRANSCRIPTION FACTOR AP 1; VASCULOTROPIN A;

ADRENAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOLE; ARTICLE; CHOLESTEROL SIDE CHAIN CLEAVAGE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME IMMUNOASSAY; GENE EXPRESSION; HEART RIGHT ATRIUM PRESSURE; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LEYDIG CELL; LIQUID CHROMATOGRAPHY; LUNG ARTERY PRESSURE; LUNG FIBROBLAST; LUNG FIBROSIS; LUNG VASCULAR RESISTANCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PULMONARY ARTERY; PULMONARY HYPERTENSION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TANDEM MASS SPECTROMETRY; UPREGULATION; VASCULAR FIBROSIS;

ALDOSTERONE; CELL HYPOXIA; FIBROSIS; HYPERTENSION, PULMONARY;

ALDOSTERONE; ANIMALS; ANOXIA; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; PHOSPHOPROTEINS; PULMONARY ARTERY; PULMONARY FIBROSIS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; UP-REGULATION;

EID: 84904048558     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.007690     Document Type: Article

References (45)

1. Weber KT, Sun Y, Bhattacharya SK, Ahokas RA, Gerling IC. Myofibroblast-mediated mechanisms of pathological remodelling of the heart. Nat Rev Cardiol. 2013; 10: 15-26.
2. Lipson KE, Wong C, Teng Y, Spong S. CTGF is a central mediator of tissue remodeling and fibrosis and its inhibition can reverse the process of fibrosis. Fibrogenesis Tissue Repair. 2012; 5(suppl 1): S24.
3. Chrobak I, Lenna S, Stawski L, Trojanowska M. Interferon-γ promotes vascular remodeling in human microvascular endothelial cells by upregulating endothelin (ET)-1 and transforming growth factor (TGF) β2. J Cell Physiol. 2013; 228: 1774-1783.
4. Archer SL, Weir EK, Wilkins MR. Basic science of pulmonary arterial hypertension for clinicians: new concepts and experimental therapies. Circulation. 2010; 121: 2045-2066.
5. Voelkel NF, Mizuno S, Bogaard HJ. The role of hypoxia in pulmonary vascular diseases: a perspective. Am J Physiol Lung Cell Mol Physiol. 2013; 304: L457-L465.
6. Preston IR, Sagliani KD, Warburton RR, Hill NS, Fanburg BL, Jaffe IZ. Mineralocorticoid receptor antagonism attenuates experimental pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2013; 304: L678-L688.
7. Maron BA, Zhang YY, White K, Chan SY, Handy DE, Mahoney CE, Loscalzo J, Leopold JA. Aldosterone inactivates the endothelin-B receptor via a cysteinyl thiol redox switch to decrease pulmonary endothelial nitric oxide levels and modulate pulmonary arterial hypertension. Circulation. 2012; 126: 963-974.
8. Maron BA, Opotowsky AR, Landzberg MJ, Loscalzo J, Waxman AB, Leopold JA. Plasma aldosterone levels are elevated in patients with pulmonary arterial hypertension in the absence of left ventricular heart failure: a pilot study. Eur J Heart Fail. 2013; 15: 277-283.
9. Takeda Y, Miyamori I, Yoneda T, Hatakeyama H, Inaba S, Furukawa K, Mabuchi H, Takeda R. Regulation of aldosterone synthase in human vascular endothelial cells by angiotensin II and adrenocorticotropin. J Clin Endocrinol Metab. 1996; 81: 2797-2800. (Pubitemid 26323867)
10. Ahmad N, Romero DG, Gomez-Sanchez EP, Gomez-Sanchez CE. Do human vascular endothelial cells produce aldosterone? Endocrinology. 2004; 145: 3626-3629. (Pubitemid 39037546)
11. MacKenzie SM, Connell JMC, Davies E. Non-adrenal synthesis of aldosterone: a reality check. Mol Cell Endocrinol. 2012; 350: 163-167.
12. Manna PR, Cohen-Tannoudji J, Counis R, Garner CW, Huhtaniemi I, Kraemer FB, Stocco DM. Mechanisms of action of hormone-sensitive lipase in mouse Leydig cells: its role in the regulation of the steroidogenic acute regulatory protein. J Biol Chem. 2013; 288: 8505-8518.
13. Mizutani T, Yazawa T, Ju Y, Imamichi Y, Uesaka M, Inaoka Y, Matsuura K, Kamiki Y, Oki M, Umezawa A, Miyamoto K. Identification of a novel distal control region upstream of the human steroidogenic acute regulatory protein (StAR) gene that participates in SF-1-dependent chromatin architecture. J Biol Chem. 2010; 285: 28240-28251.
14. Fantozzi I, Zhang S, Platoshyn O, Remillard CV, Cowling RT, Yuan JX. Hypoxia increases AP-1 binding activity by enhancing capacitative Ca2+ entry in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol. 2003; 285: L1233-L1245. (Pubitemid 37448794)
15. Wooton-Kee CR, Clark BJ. Steroidogenic factor-1 influences proteindeoxyribonucleic acid interactions within the cyclic adenosine 3, 5-monophosphate- responsive regions of the murine steroidogenic acute regulatory protein gene. Endocrinology. 2000; 141: 1345-1355. (Pubitemid 32269102)
16. Chan SY, Zhang YY, Hemann C, Mahoney CE, Zweier JL, Loscalzo J. MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab. 2009; 10: 273-284.
17. Parikh VN, Jin RC, Rabello S, Gulbahce N, White K, Hale A, Cottrill KA, Shaik RS, Waxman AB, Zhang YY, Maron BA, Hartner JC, Fujiwara Y, Orkin SH, Haley KJ, Barabási AL, Loscalzo J, Chan SY. MicroRNA-21 integrates pathogenic signaling to control pulmonary hypertension: results of a network bioinformatics approach. Circulation. 2012; 125: 1520-1532.
18. Raff H, Jankowski BM, Goodfriend TL, Baker JE, Papanek PE. Effect of exposure to hypoxia from birth on aldosterone in rabbits: role of unesterified fatty acids. Am J Physiol. 1997; 272: R1084-R1087.
19. Raff H, Jankowski B. O2 dependence of pregnenolone and aldosterone synthesis in mitochondria from bovine zona glomerulosa cells. J Appl Physiol (1985); 1995; 78: 1625-1628.
20. Raff H, Jankowski BM, Engeland WC, Oaks MK. Hypoxia in vivo inhibits aldosterone synthesis and aldosterone synthase mRNA in rats. J Appl Physiol (1985). 1996; 81: 604-610. (Pubitemid 26303209)
21. Elton TS, Oparil S, Taylor GR, Hicks PH, Yang RH, Jin H, Chen YF. Normobaric hypoxia stimulates endothelin-1 gene expression in the rat. Am J Physiol. 1992; 263: R1260-R1264. (Pubitemid 23019123)
22. Rincon Garriz JM, Suarez C, Capponi AM. c-Fos mediates angiotensin II-induced aldosterone production and protein synthesis in bovine adrenal glomerulosa cells. Endocrinology. 2009; 150: 1294-1302.
23. Catar R, Witowski J, Wagner P, Annett Schramm I, Kawka E, Philippe A, Dragun D, Jörres A. The proto-oncogene c-Fos transcriptionally regulates VEGF production during peritoneal inflammation. Kidney Int. 2013; 84: 1119-1128.
24. King SR, Matassa AA, White EK, Walsh LP, Jo Y, Rao RM, Stocco DM, Reyland ME. Oxysterols regulate expression of the steroidogenic acute regulatory protein. J Mol Endocrinol. 2004; 32: 507-517. (Pubitemid 38584652)
25. Sugawara T, Holt JA, Driscoll D, Strauss JF 3rd, Lin D, Miller WL, Patterson D, Clancy KP, Hart IM, Clark BJ, Stocco DM. Human steroidogenic acute regulatory protein: functional activity in COS-1 cells, tissue-specific expression, and mapping of the structural gene to 8p11.2 and a pseudogene to chromosome 13, Proc Natl Acad Sci U S A. 1995; 92: 4778-4782.
26. Abe K, Toba M, Alzoubi A, Ito M, Fagan KA, Cool CD, Voelkel NF, McMurtry IF, Oka M. Formation of plexiform lesions in experimental severe pulmonary arterial hypertension. Circulation. 2010; 121: 2747-2754.
27. Arai M, Widmaier EP. Steroidogenesis in isolated adrenocortical cells during development in rats. Mol Cell Endocrinol. 1993; 92: 91-97. (Pubitemid 23097755)
28. Raff H, Ball DL, Goodfriend TL. Low oxygen selectively inhibits aldosterone secretion from bovine adrenocortical cells in vitro. Am J Physiol. 1989; 256: E640-E644.
29. Shea-Eaton W, Sandhoff TW, Lopez D, Hales DB, McLean MP. Transcriptional repression of the rat steroidogenic acute regulatory (StAR) protein gene by the AP-1 family member c-Fos. Mol Cell Endocrinol. 2002; 188: 161-170. (Pubitemid 34242675)
30. Koal T, Schmiederer D, Pham-Tuan H, Röhring C, Rauh M. Standardized LC-MS/MS based steroid hormone profile-analysis. J Steroid Biochem Mol Biol. 2012; 129: 129-138.
31. Frid MG, Brunetti JA, Burke DL, Carpenter TC, Davie NJ, Reeves JT, Roedersheimer MT, van Rooijen N, Stenmark KR. Hypoxia-induced pulmonary vascular remodeling requires recruitment of circulating mesenchymal precursors of a monocyte/macrophage lineage. Am J Pathol. 2006; 168: 659-669. (Pubitemid 43271163)
32. Zhu P, Huang L, Ge X, Yan F, Wu R, Ao Q. Transdifferentiation of pulmonary arteriolar endothelial cells into smooth muscle-like cells regulated by myocardin involved in hypoxia-induced pulmonary vascular remodelling. Int J Exp Pathol. 2006; 87: 463-474. (Pubitemid 44813865)
33. Podowski M, Calvi C, Metzger S, Misono K, Poonyagariyagorn H, Lopez- Mercado A, Ku T, Lauer T, McGrath-Morrow S, Berger A, Cheadle C, Tuder R, Dietz HC, Mitzner W, Wise R, Neptune E. Angiotensin receptor blockade attenuates cigarette smoke-induced lung injury and rescues lung architecture in mice. J Clin Invest. 2012; 122: 229-240.
34. Ji WJ, Ma YQ, Zhou X, Zhang YD, Lu RY, Guo ZZ, Sun HY, Hu DC, Yang GH, Li YM, Wei LQ. Spironolactone attenuates bleomycin-induced pulmonary injury partially via modulating mononuclear phagocyte phenotype switching in circulating and alveolar compartments. PLoS One. 2013; 8: e81090.
35. Chabot A, Jiang BH, Shi Y, Tardif JC, Dupuis J. Role of aldosterone on lung structural remodelling and right ventricular function in congestive heart failure. BMC Cardiovasc Disord. 2011; 11: 72.
36. de Man FS, Tu L, Handoko ML, Rain S, Ruiter G, François C, Schalij I, Dorfmüller P, Simonneau G, Fadel E, Perros F, Boonstra A, Postmus PE, van der Velden J, Vonk-Noordegraaf A, Humbert M, Eddahibi S, Guignabert C. Dysregulated renin-angiotensin-aldosterone system contributes to pulmonary arterial hypertension. Am J Respir Crit Care Med. 2012; 186: 780-789.
37. Yamanaka R, Otsuka F, Nakamura K, Yamashita M, Otani H, Takeda M, Matsumoto Y, Kusano KF, Ito H, Makino H. Involvement of the bone morphogenetic protein system in endothelin- and aldosterone-induced cell proliferation of pulmonary arterial smooth muscle cells isolated from human patients with pulmonary arterial hypertension. Hypertens Res. 2010; 33: 435-445.
38. Kokubu T, Kazatani Y, Hamada M, Matsuzaki K, Ito T, Nishimura K, Ochi T, Daimon F, Joh T. Is captopril effective in primary pulmonary hypertension? Jpn Circ J. 1982; 46: 1095-1097. (Pubitemid 13213556)
39. Ali Z, Mishra A, Kumar R, Alam P, Pandey P, Ram R, Thinlas T, Mohammad G, Pasha MA. Interactions among vascular-tone modulators contribute to high altitude pulmonary edema and augmented vasoreactivity in highlanders. PLoS One. 2012; 7: e44049.
40. Maron BA, Waxman AB, Opotowsky AR, Gillies H, Blair C, Aghamohammadzadeh R, Loscalzo J, Leopold JA. Effectiveness of spironolactone plus ambrisentan for treatment of pulmonary arterial hypertension (from the [ARIES] study 1 and 2 trials). Am J Cardiol. 2013; 112: 720-725.
41. Leopold JA, Dam A, Maron BA, Scribner AW, Liao R, Handy DE, Stanton RC, Pitt B, Loscalzo J. Aldosterone impairs vascular reactivity by decreasing glucose-6-phosphate dehydrogenase activity. Nat Med. 2007; 13: 189-197.
42. Lemarié CA, Simeone SM, Nikonova A, Ebrahimian T, Deschênes ME, Coffman TM, Paradis P, Schiffrin EL. Aldosterone-induced activation of signaling pathways requires activity of angiotensin type 1a receptors. Circ Res. 2009; 105: 852-859.
43. Batenburg WW, Jansen PM, van den Bogaerdt AJ, J Danser AH. Angiotensin II-aldosterone interaction in human coronary microarteries involves GPR30, EGFR, and endothelial NO synthase. Cardiovasc Res. 2012; 94: 136-143.
44. Elinoff JM, Rame JE, Forfia PR, Hall MK, Sun J, Gharib AM, Abd- Elmoniem K, Graninger G, Harper B, Danner RL, Solomon MA. A pilot study of the effect of spironolactone therapy on exercise capacity and endothelial dysfunction in pulmonary arterial hypertension: study protocol for a randomized controlled trial. Trials. 2013; 14: 91.
45. Gomberg-Maitland M, Bull TM, Saggar R, Barst RJ, Elgazayerly A, Fleming TR, Grimminger F, Rainisio M, Stewart DJ, Stockbridge N, Ventura C, Ghofrani AH, Rubin LJ. New trial designs and potential therapies for pulmonary artery hypertension. J Am Coll Cardiol. 2013; 62(suppl 25): D82-D91.