Histone deacetylase inhibition attenuates transcriptional activity of mineralocorticoid receptor through its acetylation and prevents development of hypertension

Circulation Research

Volumn 112, Issue 7, 2013, Pages 1004-1012

  Lee, Hae Ahm ^a   Lee, Dong Youb ^a   Cho, Hyun Min ^a   Kim, Sang Yeob ^a   Iwasaki, Yasumasa ^b   Kim, In Kyeom ^a  

^a Kyungpook National University School of Medicine   (South Korea)

^b KOCHI UNIVERSITY   (Japan)

Author keywords

animal model cardiovascular disease; gene transcription; HDAC inhibitor; hypertension; mineralocorticoid receptor

Indexed keywords

ANTIBODY; DEOXYCORTICOSTERONE ACETATE; DRINKING WATER; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; LUCIFERASE; MINERALOCORTICOID RECEPTOR; RNA POLYMERASE II;

ACETYLATION; ANIMAL EXPERIMENT; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; ENZYME INHIBITION; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HYPERALDOSTERONISM; HYPERTENSION; LIVER CELL; NEPHRECTOMY; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ACETYLATION; ALDOSTERONE; ANIMALS; DESOXYCORTICOSTERONE; DISEASE MODELS, ANIMAL; DNA POLYMERASE II; ENZYME INHIBITORS; GENE EXPRESSION; HEK293 CELLS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYPERTENSION, RENAL; MALE; MINERALOCORTICOIDS; NEPHRECTOMY; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, MINERALOCORTICOID; TRANSCRIPTION, GENETIC; VALPROIC ACID;

EID: 84876410004     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.113.301071     Document Type: Article

References (39)

1. Iyer A, Fenning A, Lim J, Le GT, Reid RC, Halili MA, Fairlie DP, Brown L. Antifbrotic activity of an inhibitor of histone deacetylases in DOCA-salt hypertensive rats. Br J Pharmacol. 2010;159:1408-1417.
2. Cardinale JP, Sriramula S, Pariaut R, Guggilam A, Mariappan N, Elks CM, Francis J. HDAC inhibition attenuates infammatory, hypertro-phic, and hypertensive responses in spontaneously hypertensive rats. Hypertension. 2010;56:437-444.
3. Strahl BD, Allis CD. The language of covalent histone modifcations. Nature. 2000;403:41-45.
4. Shahbazian MD, Grunstein M. Functions of site-specifc histone acetyla-tion and deacetylation. Annu Rev Biochem. 2007;76:75-100.
5. Kong Y, Tannous P, Lu G, Berenji K, Rothermel BA, Olson EN, Hill JA. Suppression of class I and II histone deacetylases blunts pressure-overload cardiac hypertrophy. Circulation. 2006;113:2579-2588.
6. Chang S, Pikaard CS. Transcript profling in Arabidopsis reveals complex responses to global inhibition of DNA methylation and histone deacetylation. J Biol Chem. 2005;280:796-804.
7. Rössig L, Li H, Fisslthaler B, Urbich C, Fleming I, Förstermann U, Zeiher AM, Dimmeler S. Inhibitors of histone deacetylation downregu-late the expression of endothelial nitric oxide synthase and compromise endothelial cell function in vasorelaxation and angiogenesis. Circ Res. 2002;91:837-844.
8. Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, Alvarez JG, Downes M, Evans RM, Montminy M, Shaw RJ. Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell. 2011;145:607-621.
9. Barlev NA, Liu L, Chehab NH, Mansfeld K, Harris KG, Halazonetis TD, Berger SL. Acetylation of p53 activates transcription through recruitment of coactivators/histone acetyltransferases. Mol Cell. 2001;8:1243-1254.
10. Qiu Y, Stavreva DA, Luo Y, Indrawan A, Chang M, Hager GL. Dynamic interaction of HDAC1 with a glucocorticoid receptor-regulated gene is modulated by the activity state of the promoter. J Biol Chem. 2011;286:7641-7647.
11. Qiu Y, Zhao Y, Becker M, et al. HDAC1 acetylation is linked to progressive modulation of steroid receptor-induced gene transcription. Mol Cell. 2006;22:669-679.
12. Escriva H, Bertrand S, Laudet V. The evolution of the nuclear receptor superfamily. Essays Biochem. 2004;40:11-26.
13. Faus H, Haendler B. Post-translational modifcations of steroid receptors. Biomed Pharmacother. 2006;60:520-528.
14. Leader JE, Wang C, Fu M, Pestell RG. Epigenetic regulation of nuclear steroid receptors. Biochem Pharmacol. 2006;72:1589-1596.
15. Connell JM, MacKenzie SM, Freel EM, Fraser R, Davies E. A lifetime of aldosterone excess: long-term consequences of altered regulation of aldosterone production for cardiovascular function. Endocr Rev. 2008;29:133-154.
16. Viengchareun S, Le Menuet D, Martinerie L, Munier M, Pascual-Le Tallec L, Lombès M. The mineralocorticoid receptor: insights into its molecular and (patho)physiological biology. Nucl Recept Signal. 2007;5:e012.
17. Nagai Y, Miyata K, Sun GP, Rahman M, Kimura S, Miyatake A, Kiyomoto H, Kohno M, Abe Y, Yoshizumi M, Nishiyama A. Aldosterone stimulates collagen gene expression and synthesis via activation of ERK1/2 in rat renal fbroblasts. Hypertension. 2005;46:1039-1045.
18. Rocha R, Rudolph AE, Frierdich GE, Nachowiak DA, Kekec BK, Blomme EA, McMahon EG, Delyani JA. Aldosterone induces a vascular infammatory phenotype in the rat heart. Am J Physiol Heart Circ Physiol. 2002;283:H1802-H1810.
19. Cavasin MA, Demos-Davies K, Horn TR, et al. Selective class I his-tone deacetylase inhibition suppresses hypoxia-induced cardiopulmo-nary remodeling through an antiproliferative mechanism. Circ Res. 2012;110:739-748.
20. Gurvich N, Tsygankova OM, Meinkoth JL, Klein PS. Histone deacety-lase is a target of valproic acid-mediated cellular differentiation. Cancer Res. 2004;64:1079-1086.
21. Dokmanovic M, Clarke C, Marks PA. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res. 2007;5:981-989.
22. van der Laan S, Sarabdjitsingh RA, Van Batenburg MF, Lachize SB, Li H, Dijkmans TF, Vreugdenhil E, de Kloet ER, Meijer OC. Chromatin immunoprecipitation scanning identifes glucocorticoid receptor binding regions in the proximal promoter of a ubiquitously expressed glucocorticoid target gene in brain. J Neurochem. 2008;106:2515-2523.
23. Kuo MH, Allis CD. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays. 1998;20:615-626.
24. Nader N, Chrousos GP, Kino T. Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: potential physiological implications. FASEB J. 2009;23:1572-1583.
25. Shibata H, Ando T, Suzuki T, Kurihara I, Hayashi K, Hayashi M, Saito I, Murai M, Saruta T. COUP-TFI expression in human adrenocortical adenomas: possible role in steroidogenesis. J Clin Endocrinol Metab. 1998;83:4520-4523.
26. Lee HA, Cho HM, Lee DY, Kim KC, Han HS, Kim IK. Tissue-specifc upregulation of angiotensin-converting enzyme 1 in spontaneously hypertensive rats through histone code modifcations. Hypertension. 2012;59:621-626.
27. Wang JC, Derynck MK, Nonaka DF, Khodabakhsh DB, Haqq C, Yamamoto KR. Chromatin immunoprecipitation (ChIP) scanning iden-tifes primary glucocorticoid receptor target genes. Proc Natl Acad Sci USA. 2004;101:15603-15608.
28. Pascual-Le Tallec L, Lombes M. The mineralocorticoid receptor: A journey exploring its diversity and specifcity of action. Mol Endocrinol. 2005;19:2211-2221.
29. Yoshida Y, Morimoto T, Takaya T, Kawamura T, Sunagawa Y, Wada H, Fujita M, Shimatsu A, Kita T, Hasegawa K. Aldosterone signaling associates with p300/GATA4 transcriptional pathway during the hypertro-phic response of cardiomyocytes. Circ J. 2010;74:156-162.
30. Hultman ML, Krasnoperova NV, Li S, Du S, Xia C, Dietz JD, Lala DS, Welsch DJ, Hu X. The ligand-dependent interaction of mineralocorticoid receptor with coactivator and corepressor peptides suggests multiple activation mechanisms. Mol Endocrinol. 2005;19:1460-1473.
31. Faus H, Haendler B. Androgen receptor acetylation sites differentially regulate gene control. J Cell Biochem. 2008;104:511-524.
32. Fuqua SA, Wiltschke C, Zhang QX, Borg A, Castles CG, Friedrichs WE, Hopp T, Hilsenbeck S, Mohsin S, O'Connell P, Allred DC. A hypersensitive estrogen receptor-alpha mutation in premalignant breast lesions. Cancer Res. 2000;60:4026-4029.
33. Wang C, Fu M, Angeletti RH, Siconolf-Baez L, Reutens AT, Albanese C, Lisanti MP, Katzenellenbogen BS, Kato S, Hopp T, Fuqua SA, Lopez GN, Kushner PJ, Pestell RG. Direct acetylation of the estrogen receptor alpha hinge region by p300 regulates transactivation and hormone sensitivity. J Biol Chem. 2001;276:18375-18383.
34. Daniel AR, Gaviglio AL, Czaplicki LM, Hillard CJ, Housa D, Lange CA. The progesterone receptor hinge region regulates the kinetics of transcriptional responses through acetylation, phosphorylation, and nuclear retention. Mol Endocrinol. 2010;24:2126-2138.
35. Shimojo M, Ricketts ML, Petrelli MD, Moradi P, Johnson GD, Bradwell AR, Hewison M, Howie AJ, Stewart PM. Immunodetection of 11 beta-hydroxysteroid dehydrogenase type 2 in human mineralocorti-coid target tissues: evidence for nuclear localization. Endocrinology. 1997;138:1305-1311.
36. Sugiyama T, Yoshimoto T, Tsuchiya K, Gochou N, Hirono Y, Tateno T, Fukai N, Shichiri M, Hirata Y. Aldosterone induces angiotensin converting enzyme gene expression via a JAK2-dependent pathway in rat endo-thelial cells. Endocrinology. 2005;146:3900-3906.
37. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, Palensky J, Wittes J. 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.
38. Pitt B, Remme W, Zannad F, Neaton J, Martinez F, Roniker B, Bittman R, Hurley S, Kleiman J, Gatlin M; Eplerenone Post-Acute Myocardial Infarction Heart Failure Effcacy and Survival Study Investigators. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med. 2003;348:1309-1321.
39. Shibata S, Nagase M, Yoshida S, Kawarazaki W, Kurihara H, Tanaka H, Miyoshi J, Takai Y, Fujita T. Modifcation of mineralocorticoid receptor function by Rac1 GTPase: implication in proteinuric kidney disease. Nat Med. 2008;14:1370-1376.