Histone deacetyltransferase inhibitors Trichostatin A and Mocetinostat differentially regulate MMP9, IL-18 and RECK expression, and attenuate Angiotensin II-induced cardiac fibroblast migration and proliferation

Hypertension Research

Volumn 39, Issue 10, 2016, Pages 709-716

  Somanna, Naveen K ^a   Valente, Anthony J ^b   Krenz, Maike ^c   McDonald, Kerry S ^c   Higashi, Yusuke ^c   Noda, Makoto ^d   Chandrasekar, Bysani ^c,e  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c University of Missouri   (United States)

^d KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

fibrosis; HDAC inhibitors; histone deacetyltransferases; hypertensive heart disease; inflammation; remodeling

Indexed keywords

ANGIOTENSIN II; COLLAGEN TYPE 1; COLLAGEN TYPE 3; FIBRONECTIN; GELATINASE B; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; MOCETINOSTAT; REGULATOR PROTEIN; REVERSION INDUCING CYSTEINE RICH PROTEIN; TRICHOSTATIN A; UNCLASSIFIED DRUG; BENZAMIDE DERIVATIVE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; PYRIMIDINE DERIVATIVE; RECK PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EXTRACELLULAR MATRIX; FIBROBLAST CULTURE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; HEART FIBROBLAST; MALE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; ANIMAL; CARDIAC MUSCLE; CELL DEATH; CELL MOTION; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; HEART; METABOLISM;

ANGIOTENSIN II; ANIMALS; BENZAMIDES; CELL DEATH; CELL MOVEMENT; CELL PROLIFERATION; FIBROBLASTS; GPI-LINKED PROTEINS; HEART; HISTONE DEACETYLASE INHIBITORS; HYDROXAMIC ACIDS; INTERLEUKIN-18; MATRIX METALLOPROTEINASE 9; MICE; MYOCARDIUM; PYRIMIDINES;

EID: 84989815385     PISSN: 09169636     EISSN: 13484214     Source Type: Journal    
DOI: 10.1038/hr.2016.54     Document Type: Article

References (41)

1. Montgomery RL, Davis CA, Potthoff MJ, Haberland M, Fielitz J, Qi X, Hill JA, Richardson JA, Olson EN. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 2007; 21: 1790-1802.
2. Williams SM, Golden-Mason L, Ferguson BS, Schuetze KB, Cavasin MA, Demos-Davies K, Yeager ME, Stenmark KR, McKinsey TA. Class I HDACs regulate angiotensin II-dependent cardiac fibrosis via fibroblasts and circulating fibrocytes. J Mol Cell Cardiol 2014; 67: 112-125.
3. Pang M, Zhuang S. Histone deacetylase: a potential therapeutic target for fibrotic disorders. J Pharmacol Exp Ther 2010; 335: 266-272.
4. Kang SH, Seok YM, Song MJ, Lee HA, Kurz T, Kim I. Histone deacetylase inhibition attenuates cardiac hypertrophy and fibrosis through acetylation of mineralocorticoid receptor in spontaneously hypertensive rats. Mol Pharmacol 2015; 87: 782-791.
5. Schuetze KB, McKinsey TA, Long CS. Targeting cardiac fibroblasts to treat fibrosis of the heart: focus on HDACs. J Mol Cell Cardiol 2014; 70: 100-107.
6. Xie M, Hill JA. HDAC-dependent ventricular remodeling. Trends Cardiovasc Med 2013; 23: 229-235.
7. McKinsey TA. Targeting inflammation in heart failure with histone deacetylase inhibitors. Mol Med 2011; 17: 434-441.
8. Mani SK, Kern CB, Kimbrough D, Addy B, Kasiganesan H, Rivers WT, Patel RK, Chou JC, Spinale FG, Mukherjee R, Menick DR. Inhibition of class I histone deacetylase activity represses matrix metalloproteinase-2 and -9 expression and preserves LV function postmyocardial infarction. Am J Physiol Heart Circ Physiol 2015; 308: H1391-H1401.
9. Fix C, Bingham K, Carver W. Effects of interleukin-18 on cardiac fibroblast function and gene expression. Cytokine 2011; 53: 19-28.
10. Yu Q, Vazquez R, Khojeini EV, Patel C, Venkataramani R, Larson DF. IL-18 induction of osteopontin mediates cardiac fibrosis and diastolic dysfunction in mice. Am J Physiol Heart Circ Physiol 2009; 297: H76-H85.
11. Valente AJ, Sakamuri SS, Siddesha JM, Yoshida T, Gardner JD, Prabhu R, Siebenlist U, Chandrasekar B. TRAF3IP2 mediates interleukin-18-induced cardiac fibroblast migration and differentiation. Cell Signal 2013; 25: 2176-2184.
12. Siddesha JM, Valente AJ, Sakamuri SS, Gardner JD, Delafontaine P, Noda M, Chandrasekar B. Acetylsalicylic acid inhibits IL-18-induced cardiac fibroblast migration through the induction of RECK. J Cell Physiol 2014; 229: 845-855.
13. Chandrasekar B, Mummidi S, Mahimainathan L, Patel DN, Bailey SR, Imam SZ, Greene WC, Valente AJ. Interleukin-18-induced human coronary artery smooth muscle cell migration is dependent on NF-kappaB- and AP-1-mediated matrix metalloproteinase-9 expression and is inhibited by atorvastatin. J Biol Chem 2006; 281: 15099-15109.
14. Chandrasekar B, Marelli-Berg FM, Tone M, Bysani S, Prabhu SD, Murray DR. Beta-adrenergic stimulation induces interleukin-18 expression via beta2-AR, PI3K, Akt, IKK, and NF-kappaB. Biochem Biophys Res Commun 2004; 319: 304-311.
15. Takahashi C, Sheng Z, Horan TP, Kitayama H, Maki M, Hitomi K, Kitaura Y, Takai S, Sasahara RM, Horimoto A, Ikawa Y, Ratzkin BJ, Arakawa T. Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc Natl Acad Sci USA 1998; 95: 13221-13226.
16. Takagi S, Simizu S, Osada H. RECK negatively regulates matrix metalloproteinase-9 transcription. Cancer Res 2009; 69: 1502-1508.
17. Noda M, Takahashi C. Recklessness as a hallmark of aggressive cancer. Cancer Sci 2007; 98: 1659-1665.
18. Hsu MC, Chang HC, Hung WC. HER-2/neu represses the metastasis suppressor RECK via ERK and Sp transcription factors to promote cell invasion. J Biol Chem 2006; 281: 4718-4725.
19. Mikami D, Kimura H, Kamiyama K, Torii K, Kasuno K, Takahashi N, Yoshida H, Iwano M. Telmisartan activates endogenous peroxisome proliferator-activated receptor-delta and may have anti-fibrotic effects in human mesangial cells. Hypertens Res 2014; 37: 422-431.
20. Zhang Y, Shao L, Ma A, Guan G, Wang J, Wang Y, Tian G. Telmisartan delays myocardial fibrosis in rats with hypertensive left ventricular hypertrophy by TGF-beta1/Smad signal pathway. Hypertens Res 2014; 37: 43-49.
21. Yu C, Chen J, Guan W, Han Y, Wang WE, Wang X, Wang H, Jose PA, Zeng C. Activation of the D4 dopamine receptor attenuates proliferation and migration of vascular smooth muscle cells through downregulation of AT1a receptor expression. Hypertens Res 2015; 38: 588-596.
22. Siddesha JM, Valente AJ, Sakamuri SS, Yoshida T, Gardner JD, Somanna N, Takahashi C, Noda M, Chandrasekar B. Angiotensin II stimulates cardiac fibroblast migration via the differential regulation of matrixins and RECK. J Mol Cell Cardiol 2013; 65: 9-18.
23. Siddesha JM, Valente AJ, Yoshida T, Sakamuri SS, Delafontaine P, Iba H, Noda M, Chandrasekar B. Docosahexaenoic acid reverses angiotensin II-induced RECK suppression and cardiac fibroblast migration. Cell Signal 2014; 26: 933-941.
24. Valente AJ, Yoshida T, Gardner JD, Somanna N, Delafontaine P, Chandrasekar B. Interleukin-17A stimulates cardiac fibroblast proliferation and migration via negative regulation of the dual-specificity phosphatase MKP-1/DUSP-1. Cell Signal 2012; 24: 560-568.
25. Valente AJ, Clark RA, Siddesha JM, Siebenlist U, Chandrasekar B. CIKS (Act1 or TRAF3IP2) mediates Angiotensin-II-induced Interleukin-18 expression, and Nox2-dependent cardiomyocyte hypertrophy. J Mol Cell Cardiol 2012; 53: 113-124.
26. Somanna NK, Valente AJ, Krenz M, Fay WP, Delafontaine P, Chandrasekar B. The Nox1/4 Dual Inhibitor GKT137831 or Nox4 Knockdown Inhibits Angiotensin-II-Induced Adult Mouse Cardiac Fibroblast Proliferation and Migration. AT1 Physically Associates With Nox4. J Cell Physiol 2015; 231: 1130-1141.
27. Sasahara RM, Takahashi C, Noda M. Involvement of the Sp1 site in ras-mediated downregulation of the RECK metastasis suppressor gene. Biochem Biophys Res Commun 1999; 264: 668-675.
28. Valente AJ, Yoshida T, Izadpanah R, Delafontaine P, Siebenlist U, Chandrasekar B. Interleukin-18 enhances IL-18R/Nox1 binding, and mediates TRAF3IP2-dependent smooth muscle cell migration. Inhibition by simvastatin. Cell Signal 2013; 25: 1447-1456.
29. Khan DH, He S, Yu J, Winter S, Cao W, Seiser C, Davie JR. Protein kinase CK2 regulates the dimerization of histone deacetylase 1 (HDAC1) and HDAC2 during mitosis. J Biol Chem 2013; 288: 16518-16528.
30. Ma Z, Shah RC, Chang MJ, Benveniste EN. Coordination of cell signaling, chromatin remodeling, histone modifications, and regulator recruitment in human matrix metalloproteinase 9 gene transcription. Mol Cell Biol 2004; 24: 5496-5509.
31. Ailenberg M, Silverman M. Differential effects of trichostatin A on gelatinase A expression in 3T3 fibroblasts and HT-1080 fibrosarcoma cells: implications for use of TSA in cancer therapy. Biochem Biophys Res Commun 2003; 302: 181-185.
32. Kaneko F, Saito H, Saito Y, Wakabayashi K, Nakamoto N, Tada S, Suzuki H, Tsunematsu S, Kumagai N, Ishii H. Down-regulation of matrix-invasive potential of human liver cancer cells by type I interferon and a histone deacetylase inhibitor sodium butyrate. Int J Oncol 2004; 24: 837-845.
33. Cortez DM, Feldman MD, Mummidi S, Valente AJ, Steffensen B, Vincenti M, Barnes JL, Chandrasekar B. IL-17 stimulates MMP-1 expression in primary human cardiac fibroblasts via p38 MAPK- and ERK1/2-dependent C/EBP-beta, NF-kappaB, and AP-1 activation. Am J Physiol Heart Circ Physiol 2007; 293: H3356-H3365.
34. Majumdar G, Johnson IM, Kale S, Raghow R. Epigenetic regulation of cardiac muscle-specific genes in H9c2 cells by Interleukin-18 and histone deacetylase inhibitor m-carboxycinnamic acid bis-hydroxamide. Mol Cell Biochem 2008; 312: 47-60.
35. Majumdar G, Rooney RJ, Johnson IM, Raghow R. Panhistone deacetylase inhibitors inhibit proinflammatory signaling pathways to ameliorate interleukin-18-induced cardiac hypertrophy. Physiol Genomics 2011; 43: 1319-1333.
36. Koyama N, Koschmieder S, Tyagi S, Nürnberger H, Wagner S, Böcker U, Hoelzer D, Gerhard Ottmann O, Kalina U. Differential effects of histone deacetylase inhibitors on interleukin-18 gene expression in myeloid cells. Biochem Biophys Res Commun 2002; 292: 937-943.
37. Chang HC, Liu LT, Hung WC. Involvement of histone deacetylation in ras-induced down-regulation of the metastasis suppressor RECK. Cell Signal 2004; 16: 675-679.
38. Fredj S, Bescond J, Louault C, Delwail A, Lecron JC, Potreau D. Role of interleukin-6 in cardiomyocyte/cardiac fibroblast interactions during myocyte hypertrophy and fibroblast proliferation. J Cell Physiol 2005; 204: 428-436.
39. Walsh LA, Roy DM, Reyngold M, Giri D, Snyder A, Turcan S, Badwe CR, Lyman J, Bromberg J, King TA, Chan TA. RECK controls breast cancer metastasis by modulating a convergent, STAT3-dependent neoangiogenic switch. Oncogene 2015; 34: 2189-2203.
40. Kitajima S, Miki T, Takegami Y, Kido Y, Noda M, Hara E, Shamma A, Takahashi C. Reversion-inducing cysteine-rich protein with Kazal motifs interferes with epidermal growth factor receptor signaling. Oncogene 2011; 30: 737-750.
41. Murasawa S, Mori Y, Nozawa Y, Gotoh N, Shibuya M, Masaki H, Maruyama K, Tsutsumi Y, Moriguchi Y, Shibazaki Y, Tanaka Y, Iwasaka T, Inada M, Matsubara H. Angiotensin II type 1 receptor-induced extracellular signal-regulated protein kinase activation is mediated by Ca2+/calmodulin-dependent transactivation of epidermal growth factor receptor. Circ Res 1998; 82: 1338-1348.