Histone deacetylase inhibition attenuates cardiac hypertrophy and fibrosis through acetylation of mineralocorticoid receptor in spontaneously hypertensive rats

Molecular Pharmacology

Volumn 87, Issue 5, 2015, Pages 782-791

  Kang, Seol Hee ^a,b,c   Seok, Young Mi ^a,c   Song, Min Ji ^a,c   Lee, Hae Ahm ^a,c   Kurz, Thomas ^d   Kim, InKyeom ^a,b,c  

^a Department of Pharmacology ^*  (South Korea)

^b Kyungpook National University   (South Korea)

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

^d HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL LYSINE ANTIBODY; ANTIBODY; DRINKING WATER; HISTONE DEACETYLASE; HISTONE H3; LYSINE; MINERALOCORTICOID RECEPTOR; OROSOMUCOID 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN; RNA POLYMERASE II; UNCLASSIFIED DRUG; VALPROIC ACID; HISTONE; HISTONE DEACETYLASE INHIBITOR;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME INHIBITION; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; HISTONE METHYLATION; HISTONE MODIFICATION; IMMUNOPRECIPITATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPONTANEOUSLY HYPERTENSIVE RAT; STAINING; TREATMENT DURATION; WESTERN BLOTTING; WISTAR KYOTO RAT; ANIMAL; CARDIOMEGALY; DRUG EFFECTS; FIBROSIS; GENE EXPRESSION; GENETICS; METABOLISM; PROCEDURES;

ACETYLATION; ANIMALS; CARDIOMEGALY; CHROMATIN IMMUNOPRECIPITATION; FIBROSIS; GENE EXPRESSION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONES; MALE; PROMOTER REGIONS, GENETIC; RATS; RATS, INBRED SHR; RATS, INBRED WKY; RECEPTORS, MINERALOCORTICOID; RNA POLYMERASE II;

EID: 84929940868     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.114.096974     Document Type: Article

References (49)

1. Antos CL, McKinsey TA, Dreitz M, Hollingsworth LM, Zhang CL, Schreiber K, Rindt H, Gorczynski RJ, and Olson EN (2003) Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors. J Biol Chem 278:28930-28937.
2. Brown NJ, Vaughan DE, and Fogo AB (2002) Aldosterone and PAI-1: implications for renal injury. J Nephrol 15:230-235.
3. Cao DJ, Wang ZV, Battiprolu PK, Jiang N, Morales CR, Kong Y, Rothermel BA, Gillette TG, and Hill JA (2011) Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci USA 108:4123-4128.
4. Cardinale JP, Sriramula S, Pariaut R, Guggilam A, Mariappan N, Elks CM, and Francis J (2010) HDAC inhibition attenuates inflammatory, hypertrophic, and hypertensive responses in spontaneously hypertensive rats. Hypertension 56:437-444.
5. Cho YK, Eom GH, Kee HJ, Kim HS, Choi WY, Nam KI, Ma JS, and Kook H (2010) Sodium valproate, a histone deacetylase inhibitor, but not captopril, prevents right ventricular hypertrophy in rats. Circ J 74:760-770.
6. Chun TY and Pratt JH (2005) Aldosterone increases plasminogen activator inhibitor-1 synthesis in rat cardiomyocytes. Mol Cell Endocrinol 239:55-61.
7. Delcuve GP, Khan DH, and Davie JR (2012) Roles of histone deacetylases in epigenetic regulation: emerging paradigms from studies with inhibitors. Clinical Epigenetics 4:5.
8. Drouin J, Sun YL, Tremblay S, Lavender P, Schmidt TJ, de Léan A, and Nemer M (1992) Homodimer formation is rate-limiting for high affinity DNA binding by glucocorticoid receptor. Mol Endocrinol 6:1299-1309.
9. Engström G, Stavenow L, Hedblad B, Lind P, Eriksson KF, Janzon L, and Lindgärde F (2003) Inflammation-sensitive plasma proteins, diabetes, and mortality and incidence of myocardial infarction and stroke: a population-based study. Diabetes 52:442-447.
10. Faus H and Haendler B (2006) Post-translational modifications of steroid receptors. Biomed Pharmacother 60:520-528.
11. Fejes-Tóth G and Náray-Fejes-Tóth A (2007) Early aldosterone-regulated genes in cardiomyocytes: clues to cardiac remodeling? Endocrinology 148:1502-1510.
12. Fu M, Wang C, Reutens AT, Wang J, Angeletti RH, Siconolfi-Baez L, Ogryzko V, Avantaggiati ML, and Pestell RG (2000) p300 and p300/cAMP-response element-binding protein-associated factor acetylate the androgen receptor at sites governing hormone-dependent transactivation. J Biol Chem 275:20853-20860.
13. Fuqua SA, Wiltschke C, Zhang QX, Borg A, Castles CG, Friedrichs WE, Hopp T, Hilsenbeck S, Mohsin S, and O'Connell P et al. (2000) A hypersensitive estrogen receptor-alpha mutation in premalignant breast lesions. Cancer Res 60:4026-4029.
14. Gaughan L, Logan IR, Cook S, Neal DE, and Robson CN (2002) Tip60 and histone deacetylase 1 regulate androgen receptor activity through changes to the acetylation status of the receptor. J Biol Chem 277:25904-25913.
15. Guo W, Shan B, Klingsberg RC, Qin X, and Lasky JA (2009) Abrogation of TGF-beta1-induced fibroblast-myofibroblast differentiation by histone deacetylase inhibition. Am J Physiol Lung Cell Mol Physiol 297:L864-L870.
16. Gupta S, Young D, and Sen S (2005) Inhibition of NF-kappaB induces regression of cardiac hypertrophy, independent of blood pressure control, in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 289:H20-H29.
17. Ito K, Yamamura S, Essilfie-Quaye S, Cosio B, Ito M, Barnes PJ, and Adcock IM (2006) Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-kappaB suppression. J Exp Med 203:7-13.
18. Iyer A, Fenning A, Lim J, Le GT, Reid RC, Halili MA, Fairlie DP, and Brown L (2010) Antifibrotic activity of an inhibitor of histone deacetylases in DOCA-salt hypertensive rats. Br J Pharmacol 159:1408-1417.
19. Kanzaki Y, Terasaki F, Okabe M, Hayashi T, Toko H, Shimomura H, Fujioka S, Kitaura Y, Kawamura K, and Horii Y et al. (2001) Myocardial inflammatory cell infiltrates in cases of dilated cardiomyopathy as a determinant of outcome following partial left ventriculectomy. Jpn Circ J 65:797-802.
20. Kee HJ and Kook H (2009) Krüppel-like factor 4 mediates histone deacetylase inhibitor-induced prevention of cardiac hypertrophy. J Mol Cell Cardiol 47:770-780.
21. Kee HJ, Sohn IS, Nam KI, Park JE, Qian YR, Yin Z, Ahn Y, Jeong MH, Bang YJ, and Kim N et al. (2006) Inhibition of histone deacetylation blocks cardiac hypertrophy induced by angiotensin II infusion and aortic banding. Circulation 113:51-59.
22. Kim MY, Woo EM, Chong YT, Homenko DR, and Kraus WL (2006) Acetylation of estrogen receptor alpha by p300 at lysines 266 and 268 enhances the deoxyribonucleic acid binding and transactivation activities of the receptor. Mol Endocrinol 20:1479-1493.
23. Kong Y, Tannous P, Lu G, Berenji K, Rothermel BA, Olson EN, and Hill JA (2006) Suppression of class I and II histone deacetylases blunts pressure-overload cardiac hypertrophy. Circulation 113:2579-2588.
24. Kook H, Lepore JJ, Gitler AD, Lu MM, Wing-Man Yung W, Mackay J, Zhou R, Ferrari V, Gruber P, and Epstein JA (2003) Cardiac hypertrophy and histone deacetylase-dependent transcriptional repression mediated by the atypical homeodomain protein Hop. J Clin Invest 112:863-871.
25. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693-705.
26. Kudo H, Kai H, Kajimoto H, Koga M, Takayama N, Mori T, Ikeda A, Yasuoka S, Anegawa T, and Mifune H, et al. (2009) Exaggerated blood pressure variability superimposed on hypertension aggravates cardiac remodeling in rats via angiotensin II system-mediated chronic inflammation. Hypertension 54:832-838.
27. Kuo MH and Allis CD (1998) Roles of histone acetyltransferases and deacetylases in gene regulation. BioEssays 20:615-626.
28. Lee HA, Cho HM, Lee DY, Kim KC, Han HS, and Kim IK (2012) Tissue-specific upregulation of angiotensin-converting enzyme 1 in spontaneously hypertensive rats through histone code modifications. Hypertension 59:621-626.
29. Lee HA, Lee DY, Cho HM, Kim SY, Iwasaki Y, and Kim IK (2013) Histone deacetylase inhibition attenuates transcriptional activity of mineralocorticoid receptor through its acetylation and prevents development of hypertension. Circ Res 112:1004-1012.
30. Liao X, Haldar SM, Lu Y, Jeyaraj D, Paruchuri K, Nahori M, Cui Y, Kaestner KH, and Jain MK (2010) Krüppel-like factor 4 regulates pressure-induced cardiac hypertrophy. J Mol Cell Cardiol 49:334-338.
31. Massaad C, Houard N, Lombès M, and Barouki R (1999) Modulation of human mineralocorticoid receptor function by protein kinase A. Mol Endocrinol 13:57-65.
32. Messaoudi S, Gravez B, Tarjus A, Pelloux V, Ouvrard-Pascaud A, Delcayre C, Samuel J, Launay JM, Sierra-Ramos C, and Alvarez de la Rosa D et al. (2013) Aldosterone-specific activation of cardiomyocyte mineralocorticoid receptor in vivo. Hypertension 61:361-367.
33. Nader N, Chrousos GP, and Kino T (2009) 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 23:1572-1583.
34. Nightingale KP, Gendreizig S, White DA, Bradbury C, Hollfelder F, and Turner BM (2007) Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J Biol Chem 282:4408-4416.
35. Patel J, Pathak RR, and Mujtaba S (2011) The biology of lysine acetylation integrates transcriptional programming and metabolism (Abstract). Nutr Metab (Lond) 8:12.
36. Pitt B (2004) Effect of aldosterone blockade in patients with systolic left ventricular dysfunction: implications of the RALES and EPHESUS studies. Mol Cell Endocrinol 217:53-58.
37. Ratcliffe NR, Hutchins J, Barry B, and Hickey WF (2000) Chronic myocarditis induced by T cells reactive to a single cardiac myosin peptide: persistent inflammation, cardiac dilatation, myocardial scarring and continuous myocyte apoptosis. J Autoimmun 15:359-367.
38. Schellings MW, Pinto YM, and Heymans S (2004) Matricellular proteins in the heart: possible role during stress and remodeling. Cardiovasc Res 64:24-31.
39. Tokuda K, Kai H, Kuwahara F, Yasukawa H, Tahara N, Kudo H, Takemiya K, Koga M, Yamamoto T, and Imaizumi T (2004) Pressure-independent effects of angiotensin II on hypertensive myocardial fibrosis. Hypertension 43:499-503.
40. van der Laan S, Sarabdjitsingh RA, Van Batenburg MF, Lachize SB, Li H, Dijkmans TF, Vreugdenhil E, de Kloet ER, and Meijer OC (2008) Chromatin immunoprecipitation scanning identifies glucocorticoid receptor binding regions in the proximal promoter of a ubiquitously expressed glucocorticoid target gene in brain. J Neurochem 106:2515-2523.
41. Vannice JL, Taylor JM, and Ringold GM (1984) Glucocorticoid-mediated induction of alpha 1-acid glycoprotein: evidence for hormone-regulated RNA processing. Proc Natl Acad Sci USA 81:4241-4245.
42. Viengchareun S, Le Menuet D, Martinerie L, Munier M, Pascual-Le Tallec L, and Lombès M (2007) The mineralocorticoid receptor: insights into its molecular and (patho)physiological biology. Nucl Recept Signal 5:e012.
43. Walther RF, Atlas E, Carrigan A, Rouleau Y, Edgecombe A, Visentin L, Lamprecht C, Addicks GC, Haché RJ, and Lefebvre YA (2005) A serine/threonine-rich motif is one of three nuclear localization signals that determine unidirectional transport of the mineralocorticoid receptor to the nucleus. J Biol Chem 280:17549-17561.
44. Wang C, Fu M, Angeletti RH, Siconolfi-Baez L, Reutens AT, Albanese C, Lisanti MP, Katzenellenbogen BS, Kato S, and Hopp T et al. (2001) Direct acetylation of the estrogen receptor alpha hinge region by p300 regulates transactivation and hormone sensitivity. J Biol Chem 276:18375-18383.
45. Wang C, Tian L, Popov VM, and Pestell RG (2011) Acetylation and nuclear receptor action. J Steroid Biochem Mol Biol 123:91-100.
46. Wang JC, Derynck MK, Nonaka DF, Khodabakhsh DB, Haqq C, and Yamamoto KR (2004) Chromatin immunoprecipitation (ChIP) scanning identifies primary glucocorticoid receptor target genes. Proc Natl Acad Sci USA 101:15603-15608.
47. Yang J and Young MJ (2009) The mineralocorticoid receptor and its coregulators. J Mol Endocrinol 43:53-64.
48. Yang XJ and Seto E (2007) HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene 26:5310-5318.
49. Young MJ, Lam EY, and Rickard AJ (2007) Mineralocorticoid receptor activation and cardiac fibrosis. Clin Sci (Lond) 112:467-475.