Histone deacetylase signaling in cardioprotection

Cellular and Molecular Life Sciences

Volumn 71, Issue 9, 2014, Pages 1673-1690

  Lehmann, Lorenz H ^a   Worst, Barbara C ^a   Stanmore, David A ^a   Backs, Johannes ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cardiovascular disease; Cardiovascular therapeutics; HDAC; HDAC inhibitors; Heart failure; Histone deacetylase

Indexed keywords

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CARDIOVASCULAR DISEASES; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VENTRICULAR REMODELING;

EID: 84899414153     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1516-9     Document Type: Review

References (163)

1. Scholte op Reimer WJM SM, Boersma E, Gitt AK (2006) Cardiovascular diseases in Europe 2006. Sophia Antipolis
2. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Soliman EZ, Sorlie PD, Sotoodehnia N, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics Committee and Stroke Statistics Subcommittee (2012) Executive summary: heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 125:188-197
3. Murphy SL, Xu J, Kochanek KD (2013) Deaths: Final Data for 2010. Natl Vital Stat Rep 61(4):1-118
4. Tarride JE, Lim M, DesMeules M, Luo W, Burke N, O'Reilly D, Bowen J, Goeree R (2009) A review of the cost of cardiovascular disease. Can J Cardiol 25(6):e195-e202
5. Leal J, Luengo-Fernandez R, Gray A, Petersen S, Rayner M (2006) Economic burden of cardiovascular diseases in the enlarged European Union. Eur Heart J 27(13):1610-1619. doi: 10.1093/eurheartj/ehi733 (Pubitemid 43954923)
6. Thom T, Haase N, Rosamond W, Howard VJ, Rumsfeld J, Manolio T, Zheng ZJ, Flegal K, O'Donnell C, Kittner S, Lloyd-Jones D, Goff DC Jr, Hong Y, Adams R, Friday G, Furie K, Gorelick P, Kissela B, Marler J, Meigs J, Roger V, Sidney S, Sorlie P, Steinberger J, Wasserthiel-Smoller S, Wilson M, Wolf P (2006) Heart disease and stroke statistics-2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 113(6):e85-e151. doi: 10.1161/CIRCULATIONAHA.105.171600
7. Heidenreich PA, Trogdon JG, Khavjou OA, Butler J, Dracup K, Ezekowitz MD, Finkelstein EA, Hong Y, Johnston SC, Khera A, Lloyd-Jones DM, Nelson SA, Nichol G, Orenstein D, Wilson PW, Woo YJ (2011) Forecasting the future of cardiovascular disease in the United States: a policy statement from the American Heart Association. Circulation 123(8):933-944. doi: 10.1161/CIR.0b013e31820a55f5
8. WHO-Regional Office for Europe (2012) Definition of cardiovascular diseases. http://www.euro.who.int/en/what-we-do/health-topics/noncommunicable- diseases/cardiovascular-diseases/definition. Accessed 28 May 2012
9. Topol EJ (2009) Past the wall in cardiovascular R&D. Nat Rev Drug Discov 8(4):259. doi: 10.1038/nrd2853
10. Suckling K (2012) The landscape of drug discovery in atherosclerosis and dyslipidaemia revisited: an update of patenting activity. Expert Opin Ther Pat 22(3):199-204. doi: 10.1517/13543776.2012.667402
11. Pazin MJ, Kadonaga JT (1997) What's up and down with histone deacetylation and transcription? Cell 89(3):325-328 pii: S0092-8674(00)80211-1 (Pubitemid 27220876)
12. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325(5942):834-840. doi: 10.1126/science. 1175371
13. Glozak MA, Sengupta N, Zhang X, Seto E (2005) Acetylation and deacetylation of non-histone proteins. Gene 363:15-23. doi: 10.1016/j.gene.2005. 09.010 (Pubitemid 41691888)
14. Trivedi CM, Zhu W, Wang Q, Jia C, Kee HJ, Li L, Hannenhalli S, Epstein JA (2010) Hopx and Hdac2 interact to modulate Gata4 acetylation and embryonic cardiac myocyte proliferation. Dev Cell 19(3):450-459. doi: 10.1016/j.devcel. 2010.08.012
15. Choi MC, Cohen TJ, Barrientos T, Wang B, Li M, Simmons BJ, Yang JS, Cox GA, Zhao Y, Yao TP (2012) A direct HDAC4-MAP kinase crosstalk activates muscle atrophy program. Mol Cell 47(1):122-132. doi: 10.1016/j.molcel.2012.04.025
16. Haberland M, Montgomery RL, Olson EN (2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10(1):32-42. doi: 10.1038/nrg2485
17. Fischle W, Dequiedt F, Hendzel MJ, Guenther MG, Lazar MA, Voelter W, Verdin E (2002) Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol Cell 9(1):45-57 (Pubitemid 34127770)
18. Doetzlhofer A, Rotheneder H, Lagger G, Koranda M, Kurtev V, Brosch G, Wintersberger E, Seiser C (1999) Histone deacetylase 1 can repress transcription by binding to Sp1. Mol Cell Biol 19(8):5504-5511 (Pubitemid 29339908)
19. Trivedi CM, Luo Y, Yin Z, Zhang M, Zhu W, Wang T, Floss T, Goettlicher M, Noppinger PR, Wurst W, Ferrari VA, Abrams CS, Gruber PJ, Epstein JA (2007) Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity. Nat Med 13(3):324-331. doi: 10.1038/nm1552 (Pubitemid 46376684)
20. Zhang CL, McKinsey TA, Chang S, Antos CL, Hill JA, Olson EN (2002) Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110(4):479-488 pii: S0092867402008619 (Pubitemid 35232291)
21. Haq S, Choukroun G, Kang ZB, Ranu H, Matsui T, Rosenzweig A, Molkentin JD, Alessandrini A, Woodgett J, Hajjar R, Michael A, Force T (2000) Glycogen synthase kinase-3beta is a negative regulator of cardiomyocyte hypertrophy. J Cell Biol 151(1):117-130
22. Hardt SE, Sadoshima J (2002) Glycogen synthase kinase-3beta: a novel regulator of cardiac hypertrophy and development. Circ Res 90(10):1055-1063 (Pubitemid 34627903)
23. Sugden PH, Fuller SJ, Weiss SC, Clerk A (2008) Glycogen synthase kinase 3 (GSK3) in the heart: a point of integration in hypertrophic signalling and a therapeutic target? A critical analysis. Br J Pharmacol 153(Suppl 1):S137-S153. doi: 10.1038/sj.bjp.0707659 (Pubitemid 351341012)
24. Montgomery RL, Davis CA, Potthoff MJ, Haberland M, Fielitz J, Qi X, Hill JA, Richardson JA, Olson EN (2007) Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 21(14):1790-1802. doi: 10.1101/gad.1563807 (Pubitemid 47076478)
25. Stanford WL, Cohn JB, Cordes SP (2001) Gene-trap mutagenesis: past, present and beyond. Nat Rev Genet 2(10):756-768. doi: 10.1038/35093548 (Pubitemid 33685573)
26. Cao DJ, Wang ZV, Battiprolu PK, Jiang N, Morales CR, Kong Y, Rothermel BA, Gillette TG, Hill JA (2011) Histone deacetylase (HDAC) inhibitors attenuate cardiac hypertrophy by suppressing autophagy. Proc Natl Acad Sci USA 108(10):4123-4128. doi: 10.1073/pnas.1015081108
27. Trivedi CM, Lu MM, Wang Q, Epstein JA (2008) Transgenic overexpression of Hdac3 in the heart produces increased postnatal cardiac myocyte proliferation but does not induce hypertrophy. J Biol Chem 283(39):26484-26489. doi: 10.1074/jbc.M803686200
28. Montgomery RL, Potthoff MJ, Haberland M, Qi X, Matsuzaki S, Humphries KM, Richardson JA, Bassel-Duby R, Olson EN (2008) Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J Clin Invest 118(11):3588-3597. doi: 10.1172/JCI35847
29. Sun Z, Singh N, Mullican SE, Everett LJ, Li L, Yuan L, Liu X, Epstein JA, Lazar MA (2011) Diet-induced lethality due to deletion of the Hdac3 gene in heart and skeletal muscle. J Biol Chem 286(38):33301-33309. doi: 10.1074/jbc.M111.277707
30. Haberland M, Mokalled MH, Montgomery RL, Olson EN (2009) Epigenetic control of skull morphogenesis by histone deacetylase 8. Genes Dev 23(14):1625-1630. doi: 10.1101/gad.1809209
31. Bradner JE, West N, Grachan ML, Greenberg EF, Haggarty SJ, Warnow T, Mazitschek R (2010) Chemical phylogenetics of histone deacetylases. Nat Chem Biol 6(3):238-243. doi: 10.1038/nchembio.313
32. Lahm A, Paolini C, Pallaoro M, Nardi MC, Jones P, Neddermann P, Sambucini S, Bottomley MJ, Lo Surdo P, Carfi A, Koch U, De Francesco R, Steinkuhler C, Gallinari P (2007) Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc Natl Acad Sci USA 104(44):17335-17340. doi: 10.1073/pnas.0706487104 (Pubitemid 350219843)
33. Granger A, Abdullah I, Huebner F, Stout A, Wang T, Huebner T, Epstein JA, Gruber PJ (2008) Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice. FASEB J 22(10):3549-3560. doi: 10.1096/fj.08-108548
34. Kee HJ, Sohn IS, Nam KI, Park JE, Qian YR, Yin Z, Ahn Y, Jeong MH, Bang YJ, Kim N, Kim JK, Kim KK, Epstein JA, Kook H (2006) Inhibition of histone deacetylation blocks cardiac hypertrophy induced by angiotensin II infusion and aortic banding. Circulation 113(1):51-59. doi: 10.1161/CIRCULATIONAHA.105.559724 (Pubitemid 43958488)
35. Kong Y, Tannous P, Lu G, Berenji K, Rothermel BA, Olson EN, Hill JA (2006) Suppression of class I and II histone deacetylases blunts pressure-overload cardiac hypertrophy. Circulation 113(22):2579-2588. doi: 10.1161/CIRCULATIONAHA.106.625467 (Pubitemid 43948006)
36. Kook H, Lepore JJ, Gitler AD, Lu MM, Wing-Man Yung W, Mackay J, Zhou R, Ferrari V, Gruber P, Epstein JA (2003) Cardiac hypertrophy and histone deacetylase-dependent transcriptional repression mediated by the atypical homeodomain protein Hop. J Clin Invest 112(6):863-871. doi: 10.1172/JCI19137 (Pubitemid 38063744)
37. Liu F, Levin MD, Petrenko NB, Lu MM, Wang T, Yuan LJ, Stout AL, Epstein JA, Patel VV (2008) Histone-deacetylase inhibition reverses atrial arrhythmia inducibility and fibrosis in cardiac hypertrophy independent of angiotensin. J Mol Cell Cardiol 45(6):715-723. doi: 10.1016/j.yjmcc.2008.08.015
38. Lee TM, Lin MS, Chang NC (2007) Inhibition of histone deacetylase on ventricular remodeling in infarcted rats. Am J Physiol Heart Circ Physiol 293(2):H968-H977. doi: 10.1152/ajpheart.00891.2006 (Pubitemid 47254195)
39. Duvic M, Talpur R, Ni X, Zhang C, Hazarika P, Kelly C, Chiao JH, Reilly JF, Ricker JL, Richon VM, Frankel SR (2007) Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 109(1):31-39. doi: 10.1182/blood-2006-06-025999 (Pubitemid 46053039)
40. Duvic M, Vu J (2007) Vorinostat: a new oral histone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert Opin Investig Drugs 16(7):1111-1120. doi: 10.1517/13543784.16.7.1111 (Pubitemid 47074165)
41. U.S. National Institutes of Health (2012) U.S. National Institutes of Health. http://clinicaltrials.gov/ct2/results?term=SAHA&recr=Open&no- unk=Y&pg=5. Accessed 08 June 2012
42. Sweet MJ, Shakespear MR, Kamal NA, Fairlie DP (2011) HDAC inhibitors: modulating leukocyte differentiation, survival, proliferation and inflammation. Immunol Cell Biol 90(1):14-22. doi: 10.1038/icb.2011.88
43. Dinarello CA, Fossati G, Mascagni P (2011) Histone deacetylase inhibitors for treating a spectrum of diseases not related to cancer. Mol Med 17(5-6):333-352. doi: 10.2119/molmed.2011.00116
44. Wightman F, Ellenberg P, Churchill M, Lewin SR (2011) HDAC inhibitors in HIV. Immunol Cell Biol 90(1):47-54. doi: 10.1038/icb.2011.95
45. Antos CL, McKinsey TA, Dreitz M, Hollingsworth LM, Zhang CL, Schreiber K, Rindt H, Gorczynski RJ, Olson EN (2003) Dose-dependent blockade to cardiomyocyte hypertrophy by histone deacetylase inhibitors. J Biol Chem 278(31):28930-28937. doi: 10.1074/jbc.M303113200 (Pubitemid 36935803)
46. McKinsey TA, Kass DA (2007) Small-molecule therapies for cardiac hypertrophy: moving beneath the cell surface. Nat Rev Drug Discov 6(8):617-635. doi: 10.1038/nrd2193 (Pubitemid 47207749)
47. Kee HJ, Kook H (2009) Krüppel-like factor 4 mediates histone deacetylase inhibitor-induced prevention of cardiac hypertrophy. J Mol Cell Cardiol 47(6):770-780. doi: 10.1016/j.yjmcc.2009.08.022
48. Cantley MD, Bartold PM, Fairlie DP, Rainsford KD, Haynes DR (2012) Histone deacetylase inhibitors as suppressors of bone destruction in inflammatory diseases. J Pharm Pharmacol 64(6):763-774. doi: 10.1111/j.2042-7158.2011.01421.x
49. Kee HJ, Eom GH, Joung H, Shin S, Kim JR, Cho YK, Choe N, Sim BW, Jo D, Jeong MH, Kim KK, Seo JS, Kook H (2008) Activation of histone deacetylase 2 by inducible heat shock protein 70 in cardiac hypertrophy. Circ Res 103(11):1259-1269. doi: 10.1161/01.RES.0000338570.27156.84
50. Cardinale JP, Sriramula S, Pariaut R, Guggilam A, Mariappan N, Elks CM, Francis J (2010) HDAC inhibition attenuates inflammatory, hypertrophic, and hypertensive responses in spontaneously hypertensive rats. Hypertension 56(3):437-444. doi: 10.1161/HYPERTENSIONAHA.110.154567
51. Zhao TC, Cheng G, Zhang LX, Tseng YT, Padbury JF (2007) Inhibition of histone deacetylases triggers pharmacologic preconditioning effects against myocardial ischemic injury. Cardiovasc Res 76(3):473-481. doi: 10.1016/j.cardiores.2007.08.010 (Pubitemid 350007465)
52. Zhang L, Qin X, Zhao Y, Fast L, Zhuang S, Liu P, Cheng G, Zhao TC (2012) Inhibition of histone deacetylases preserves myocardial performance and prevents cardiac remodeling through stimulation of endogenous angiomyogenesis. J Pharmacol Exp Ther 341(1):285-293. doi: 10.1124/jpet.111.189910
53. Zhang LX, Zhao Y, Cheng G, Guo TL, Chin YE, Liu PY, Zhao TC (2010) Targeted deletion of NF-kappaB p50 diminishes the cardioprotection of histone deacetylase inhibition. Am J Physiol Heart Circ Physiol 298(6):H2154-H2163. doi: 10.1152/ajpheart.01015.2009
54. McKinsey TA (2012) Therapeutic potential for HDAC inhibitors in the heart. Annu Rev Pharmacol Toxicol 52:303-319. doi: 10.1146/annurev-pharmtox- 010611-134712
55. Liao X, Haldar SM, Lu Y, Jeyaraj D, Paruchuri K, Nahori M, Cui Y, Kaestner KH, Jain MK (2010) Krüppel-like factor 4 regulates pressure-induced cardiac hypertrophy. J Mol Cell Cardiol 49(2):334-338. doi: 10.1016/j.yjmcc.2010.04.008
56. Pang M, Zhuang S (2010) Histone deacetylase: a potential therapeutic target for fibrotic disorders. J Pharmacol Exp Ther 335(2):266-272. doi: 10.1124/jpet.110.168385
57. Guo W, Shan B, Klingsberg RC, Qin X, Lasky JA (2009) Abrogation of TGF-beta1-induced fibroblast-myofibroblast differentiation by histone deacetylase inhibition. Am J Physiol Lung Cell Mol Physiol 297(5):L864-L870. doi: 10.1152/ajplung.00128.2009
58. Lemon DD, Horn TR, Cavasin MA, Jeong MY, Haubold KW, Long CS, Irwin DC, McCune SA, Chung E, Leinwand LA, McKinsey TA (2011) Cardiac HDAC6 catalytic activity is induced in response to chronic hypertension. J Mol Cell Cardiol 51(1):41-50. doi: 10.1016/j.yjmcc.2011.04.005
59. Zhao TC, Taher MM, Valerie KC, Kukreja RC (2001) p38 Triggers late preconditioning elicited by anisomycin in heart: involvement of NF-kappaB and iNOS. Circ Res 89(10):915-922 (Pubitemid 34627897)
60. Shizukuda Y, Piekarz RL, Bates SE, Sachdev V, Finkel T, Rosing DR (2005) Effect of a histone deacetylase inhibitor on human cardiac mass. Cardiovasc Drugs Ther 19(1):89-90. doi: 10.1007/s10557-005-6901-7 (Pubitemid 40767776)
61. Shah MH, Binkley P, Chan K, Xiao J, Arbogast D, Collamore M, Farra Y, Young D, Grever M (2006) Cardiotoxicity of histone deacetylase inhibitor depsipeptide in patients with metastatic neuroendocrine tumors. Clin Cancer Res 12(13):3997-4003. doi: 10.1158/1078-0432.CCR-05-2689 (Pubitemid 44078086)
62. Subramanian S, Bates SE, Wright JJ, Espinoza-Delgado I, Piekarz RL (2010) Clinical toxicities of histone deacetylase inhibitors. Pharmaceuticals 3:2751-2767
63. de Bono JS, Kristeleit R, Tolcher A, Fong P, Pacey S, Karavasilis V, Mita M, Shaw H, Workman P, Kaye S, Rowinsky EK, Aherne W, Atadja P, Scott JW, Patnaik A (2008) Phase I pharmacokinetic and pharmacodynamic study of LAQ824, a hydroxamate histone deacetylase inhibitor with a heat shock protein-90 inhibitory profile, in patients with advanced solid tumors. Clin Cancer Res 14(20):6663-6673. doi: 10.1158/1078-0432.CCR-08-0376
64. Rajan I, Savelieva KV, Ye GL, Wang CY, Malbari MM, Friddle C, Lanthorn TH, Zhang W (2009) Loss of the putative catalytic domain of HDAC4 leads to reduced thermal nociception and seizures while allowing normal bone development. PLoS ONE 4(8):e6612. doi: 10.1371/journal.pone.0006612
65. Vega RB, Matsuda K, Oh J, Barbosa AC, Yang X, Meadows E, McAnally J, Pomajzl C, Shelton JM, Richardson JA, Karsenty G, Olson EN (2004) Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119(4):555-566. doi: 10.1016/j.cell.2004.10.024 (Pubitemid 39482354)
66. Hohl M, Wagner M, Reil JC, Muller SA, Tauchnitz M, Zimmer AM, Lehmann LH, Thiel G, Bohm M, Backs J, Maack C (2013) HDAC4 controls histone methylation in response to elevated cardiac load. J Clin Invest 123(3):1359-1370. doi: 10.1172/JCI61084
67. Chang S, McKinsey TA, Zhang CL, Richardson JA, Hill JA, Olson EN (2004) Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol Cell Biol 24(19):8467-8476. doi: 10.1128/MCB.24.19.8467-8476.2004 (Pubitemid 39245069)
68. Chang S, Young BD, Li S, Qi X, Richardson JA, Olson EN (2006) Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 126(2):321-334. doi: 10.1016/j.cell.2006.05.040 (Pubitemid 44092958)
69. Czubryt MP, McAnally J, Fishman GI, Olson EN (2003) Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1 alpha) and mitochondrial function by MEF2 and HDAC5. Proc Natl Acad Sci USA 100(4):1711-1716. doi: 10.1073/pnas.0337639100 (Pubitemid 36254513)
70. McKinsey TA, Zhang CL, Lu J, Olson EN (2000) Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408(6808):106-111. doi: 10.1038/35040593
71. McKinsey TA, Zhang CL, Olson EN (2002) MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27(1):40-47 pii: S096800040102031X (Pubitemid 34131624)
72. Lu J, McKinsey TA, Nicol RL, Olson EN (2000) Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc Natl Acad Sci USA 97(8):4070-4075. doi: 10.1073/pnas.080064097 (Pubitemid 30226088)
73. Davis FJ, Gupta M, Camoretti-Mercado B, Schwartz RJ, Gupta MP (2003) Calcium/calmodulin-dependent protein kinase activates serum response factor transcription activity by its dissociation from histone deacetylase, HDAC4. Implications in cardiac muscle gene regulation during hypertrophy. J Biol Chem 278(22):20047-20058. doi: 10.1074/jbc.M209998200 (Pubitemid 36799198)
74. Dai YS, Xu J, Molkentin JD (2005) The DnaJ-related factor Mrj interacts with nuclear factor of activated T cells c3 and mediates transcriptional repression through class II histone deacetylase recruitment. Mol Cell Biol 25(22):9936-9948. doi: 10.1128/MCB.25.22.9936-9948.2005 (Pubitemid 41572741)
75. Song K, Backs J, McAnally J, Qi X, Gerard RD, Richardson JA, Hill JA, Bassel-Duby R, Olson EN (2006) The transcriptional coactivator CAMTA2 stimulates cardiac growth by opposing class II histone deacetylases. Cell 125(3):453-466. doi: 10.1016/j.cell.2006.02.048
76. Watamoto K, Towatari M, Ozawa Y, Miyata Y, Okamoto M, Abe A, Naoe T, Saito H (2003) Altered interaction of HDAC5 with GATA-1 during MEL cell differentiation. Oncogene 22(57):9176-9184. doi: 10.1038/sj.onc.1206902 (Pubitemid 38067993)
77. Lin Q, Schwarz J, Bucana C, Olson EN (1997) Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276(5317):1404-1407 (Pubitemid 27235406)
78. Charron F, Nemer M (1999) GATA transcription factors and cardiac development. Semin Cell Dev Biol 10(1):85-91. doi: 10.1006/scdb1998.0281 (Pubitemid 129505541)
79. Parlakian A, Tuil D, Hamard G, Tavernier G, Hentzen D, Concordet JP, Paulin D, Li Z, Daegelen D (2004) Targeted inactivation of serum response factor in the developing heart results in myocardial defects and embryonic lethality. Mol Cell Biol 24(12):5281-5289. doi: 10.1128/MCB.24.12.5281-5289.2004 (Pubitemid 38738163)
80. Bushdid PB, Osinska H, Waclaw RR, Molkentin JD, Yutzey KE (2003) NFATc3 and NFATc4 are required for cardiac development and mitochondrial function. Circ Res 92(12):1305-1313. doi: 10.1161/01.RES.0000077045.84609.9F (Pubitemid 36773472)
81. Backs J, Olson EN (2006) Control of cardiac growth by histone acetylation/deacetylation. Circ Res 98(1):15-24. doi: 10.1161/01.RES.0000197782. 21444.8f (Pubitemid 43977219)
82. Kehat I, Molkentin JD (2010) Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation 122(25):2727-2735. doi: 10.1161/CIRCULATIONAHA.110.942268
83. McKinsey TA (2011) The biology and therapeutic implications of HDACs in the heart. Handb Exp Pharmacol 206:57-78. doi: 10.1007/978-3-642-21631-2-4
84. Arsenian S, Weinhold B, Oelgeschlager M, Ruther U, Nordheim A (1998) Serum response factor is essential for mesoderm formation during mouse embryogenesis. EMBO J 17(21):6289-6299. doi: 10.1093/emboj/17.21.6289 (Pubitemid 28497801)
85. Kim Y, Phan D, van Rooij E, Wang DZ, McAnally J, Qi X, Richardson JA, Hill JA, Bassel-Duby R, Olson EN (2008) The MEF2D transcription factor mediates stress-dependent cardiac remodeling in mice. J Clin Investig 118(1):124-132. doi: 10.1172/JCI33255
86. Backs J, Worst BC, Lehmann LH, Patrick DM, Jebessa Z, Kreusser MM, Sun Q, Chen L, Heft C, Katus HA, Olson EN (2011) Selective repression of MEF2 activity by PKA-dependent proteolysis of HDAC4. J Cell Biol 195(3):403-415. doi: 10.1083/jcb.201105063
87. Grozinger CM, Schreiber SL (2000) Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Natl Acad Sci USA 97(14):7835-7840. doi: 10.1073/pnas.140199597 (Pubitemid 30460734)
88. McKinsey TA, Zhang CL, Olson EN (2000) Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc Natl Acad Sci USA 97(26):14400-14405. doi: 10.1073/pnas.260501497
89. Harrison BC, Roberts CR, Hood DB, Sweeney M, Gould JM, Bush EW, McKinsey TA (2004) The CRM1 nuclear export receptor controls pathological cardiac gene expression. Mol Cell Biol 24(24):10636-10649. doi: 10.1128/MCB.24.24.10636- 10649.2004 (Pubitemid 39603122)
90. Nishino TG, Miyazaki M, Hoshino H, Miwa Y, Horinouchi S, Yoshida M (2008) 14-3-3 regulates the nuclear import of class IIa histone deacetylases. Biochem Biophys Res Commun 377(3):852-856. doi: 10.1016/j.bbrc.2008.10.079
91. Bossuyt J, Helmstadter K, Wu X, Clements-Jewery H, Haworth RS, Avkiran M, Martin JL, Pogwizd SM, Bers DM (2008) Ca2+/calmodulin-dependent protein kinase IIdelta and protein kinase D overexpression reinforce the histone deacetylase 5 redistribution in heart failure. Circ Res 102(6):695-702. doi: 10.1161/CIRCRESAHA.107.169755 (Pubitemid 351457864)
92. McKinsey TA (2007) Derepression of pathological cardiac genes by members of the CaM kinase superfamily. Cardiovasc Res 73(4):667-677. doi: 10.1016/j.cardiores.2006.11.036 (Pubitemid 46227348)
93. Vega RB, Harrison BC, Meadows E, Roberts CR, Papst PJ, Olson EN, McKinsey TA (2004) Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol Cell Biol 24(19):8374-8385. doi: 10.1128/MCB.24.19.8374-8385.2004 (Pubitemid 39245060)
94. Avkiran M, Rowland AJ, Cuello F, Haworth RS (2008) Protein kinase D in the cardiovascular system: emerging roles in health and disease. Circ Res 102(2):157-163. doi: 10.1161/CIRCRESAHA.107.168211 (Pubitemid 351651119)
95. Haworth RS, Roberts NA, Cuello F, Avkiran M (2007) Regulation of protein kinase D activity in adult myocardium: novel counter-regulatory roles for protein kinase Cepsilon and protein kinase A. J Mol Cell Cardiol 43(6):686-695. doi: 10.1016/j.yjmcc.2007.09.013 (Pubitemid 350166389)
96. Haworth RS, Stathopoulou K, Candasamy AJ, Avkiran M (2012) Neurohormonal regulation of cardiac histone deacetylase 5 nuclear localization by phosphorylation-dependent and phosphorylation-independent mechanisms. Circ Res. doi: 10.1161/CIRCRESAHA.111.263665
97. Fielitz J, Kim MS, Shelton JM, Qi X, Hill JA, Richardson JA, Bassel-Duby R, Olson EN (2008) Requirement of protein kinase D1 for pathological cardiac remodeling. Proc Natl Acad Sci USA 105(8):3059-3063. doi: 10.1073/pnas. 0712265105 (Pubitemid 351723667)
98. Harrison BC, Kim MS, van Rooij E, Plato CF, Papst PJ, Vega RB, McAnally JA, Richardson JA, Bassel-Duby R, Olson EN, McKinsey TA (2006) Regulation of cardiac stress signaling by protein kinase d1. Mol Cell Biol 26(10):3875-3888. doi: 10.1128/MCB.26.10.3875-3888.2006 (Pubitemid 43726404)
99. Backs J, Song K, Bezprozvannaya S, Chang S, Olson EN (2006) CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J Clin Investig 116(7):1853-1864. doi: 10.1172/JCI27438 (Pubitemid 44033310)
100. Little GH, Bai Y, Williams T, Poizat C (2007) Nuclear calcium/calmodulin-dependent protein kinase IIdelta preferentially transmits signals to histone deacetylase 4 in cardiac cells. J Biol Chem 282(10):7219-7231. doi: 10.1074/jbc.M604281200 (Pubitemid 47093681)
101. Backs J, Backs T, Bezprozvannaya S, McKinsey TA, Olson EN (2008) Histone deacetylase 5 acquires calcium/calmodulin-dependent kinase II responsiveness by oligomerization with histone deacetylase 4. Mol Cell Biol 28(10):3437-3445. doi: 10.1128/MCB.01611-07 (Pubitemid 351657105)
102. Wu X, Zhang T, Bossuyt J, Li X, McKinsey TA, Dedman JR, Olson EN, Chen J, Brown JH, Bers DM (2006) Local InsP3-dependent perinuclear Ca2 + signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest 116(3):675-682. doi: 10.1172/JCI27374 (Pubitemid 43326876)
103. Anderson ME, Brown JH, Bers DM (2011) CaMKII in myocardial hypertrophy and heart failure. J Mol Cell Cardiol 51(4):468-473. doi: 10.1016/j.yjmcc.2011. 01.012
104. Zhang T, Johnson EN, Gu Y, Morissette MR, Sah VP, Gigena MS, Belke DD, Dillmann WH, Rogers TB, Schulman H, Ross J Jr, Brown JH (2002) The cardiac-specific nuclear delta(B) isoform of Ca2+/calmodulin-dependent protein kinase II induces hypertrophy and dilated cardiomyopathy associated with increased protein phosphatase 2A activity. J Biol Chem 277(2):1261-1267. doi: 10.1074/jbc.M108525200 (Pubitemid 34968878)
105. Zhang T, Kohlhaas M, Backs J, Mishra S, Phillips W, Dybkova N, Chang S, Ling H, Bers DM, Maier LS, Olson EN, Brown JH (2007) CaMKIIdelta isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses. J Biol Chem 282(48):35078-35087. doi: 10.1074/jbc.M707083200 (Pubitemid 350232479)
106. Backs J, Backs T, Neef S, Kreusser MM, Lehmann LH, Patrick DM, Grueter CE, Qi X, Richardson JA, Hill JA, Katus HA, Bassel-Duby R, Maier LS, Olson EN (2009) The delta isoform of CaM kinase II is required for pathological cardiac hypertrophy and remodeling after pressure overload. Proc Natl Acad Sci USA 106(7):2342-2347. doi: 10.1073/pnas.0813013106
107. Ling H, Zhang T, Pereira L, Means CK, Cheng H, Gu Y, Dalton ND, Peterson KL, Chen J, Bers D, Brown JH (2009) Requirement for Ca2+/calmodulin-dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. J Clin Investig 119(5):1230-1240. doi: 10.1172/JCI38022
108. Sorescu D, Griendling KK (2002) Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest Heart Fail 8(3):132-140 (Pubitemid 34669892)
109. Sadoshima J (2006) Redox regulation of growth and death in cardiac myocytes. Antioxid Redox Signal 8(9-10):1621-1624. doi: 10.1089/ars.2006.8.1621 (Pubitemid 44726336)
110. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O'Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME (2008) A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133(3):462-474. doi: 10.1016/j.cell.2008.02.048 (Pubitemid 351608692)
111. Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD, Vatner SF, Sadoshima J (2008) A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell 133(6):978-993. doi: 10.1016/j.cell.2008.04.041 (Pubitemid 351787743)
112. Oka S, Ago T, Kitazono T, Zablocki D, Sadoshima J (2009) The role of redox modulation of class II histone deacetylases in mediating pathological cardiac hypertrophy. J Mol Med (Berl) 87(8):785-791. doi: 10.1007/s00109-009- 0471-2
113. Fischer T, Herting J, Tirilomis T, Renner A, Neef S, Toischer K, Ellenberger D, Forster A, Schmitto J, Gummert J, Schondube F, Hasenfuss G, Maier L, Sossalla S (2013) CaMKII and PKA Differentially Regulate SR Ca2+ - Leak in human cardiac pathology. Circulation. doi: 10.1161/CIRCULATIONAHA.113.001746
114. Haworth RS, Cuello F, Avkiran M (2011) Regulation by phosphodiesterase isoforms of protein kinase A-mediated attenuation of myocardial protein kinase D activation. Basic Res Cardiol 106(1):51-63. doi: 10.1007/s00395-010-0116-1
115. Ha CH, Kim JY, Zhao J, Wang W, Jhun BS, Wong C, Jin ZG (2010) PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy. Proc Natl Acad Sci USA 107(35):15467-15472. doi: 10.1073/pnas.1000462107
116. Du M, Perry RL, Nowacki NB, Gordon JW, Salma J, Zhao J, Aziz A, Chan J, Siu KW, McDermott JC (2008) Protein kinase A represses skeletal myogenesis by targeting myocyte enhancer factor 2D. Mol Cell Biol 28(9):2952-2970. doi: 10.1128/MCB.00248-08 (Pubitemid 351556528)
117. Paroni G, Mizzau M, Henderson C, Del Sal G, Schneider C, Brancolini C (2004) Caspase-dependent regulation of histone deacetylase 4 nuclear-cytoplasmic shuttling promotes apoptosis. Mol Biol Cell 15(6):2804-2818. doi: 10.1091/mbc.E03-08-0624 (Pubitemid 38691869)
118. Paroni G, Fontanini A, Cernotta N, Foti C, Gupta MP, Yang XJ, Fasino D, Brancolini C (2007) Dephosphorylation and caspase processing generate distinct nuclear pools of histone deacetylase 4. Mol Cell Biol 27(19):6718-6732. doi: 10.1128/MCB.00853-07 (Pubitemid 47483624)
119. Engelhardt S, Hein L, Wiesmann F, Lohse MJ (1999) Progressive hypertrophy and heart failure in beta1-adrenergic receptor transgenic mice. Proc Natl Acad Sci USA 96(12):7059-7064 (Pubitemid 29275009)
120. Bisognano JD, Weinberger HD, Bohlmeyer TJ, Pende A, Raynolds MV, Sastravaha A, Roden R, Asano K, Blaxall BC, Wu SC, Communal C, Singh K, Colucci W, Bristow MR, Port DJ (2000) Myocardial-directed overexpression of the human beta(1)-adrenergic receptor in transgenic mice. J Mol Cell Cardiol 32(5):817-830. doi: 10.1006/jmcc.2000.1123 (Pubitemid 30658918)
121. Bristow MR, Ginsburg R, Minobe W, Cubicciotti RS, Sageman WS, Lurie K, Billingham ME, Harrison DC, Stinson EB (1982) Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. N Engl J Med 307(4):205-211. doi: 10.1056/NEJM198207223070401 (Pubitemid 12079105)
122. Bristow MR, Minobe WA, Raynolds MV, Port JD, Rasmussen R, Ray PE, Feldman AM (1993) Reduced beta 1 receptor messenger RNA abundance in the failing human heart. J Clin Invest 92(6):2737-2745. doi: 10.1172/JCI116891
123. Summers RJ, Kompa A, Roberts SJ (1997) Beta-adrenoceptor subtypes and their desensitization mechanisms. J Auton Pharmacol 17(6):331-343 (Pubitemid 28177411)
124. Wang W, Zhu W, Wang S, Yang D, Crow MT, Xiao RP, Cheng H (2004) Sustained beta1-adrenergic stimulation modulates cardiac contractility by Ca2+/calmodulin kinase signaling pathway. Circ Res 95(8):798-806. doi: 10.1161/01.RES. 0000145361.50017.aa (Pubitemid 39390582)
125. Kirchhefer U, Schmitz W, Scholz H, Neumann J (1999) Activity of cAMP-dependent protein kinase and Ca2+/calmodulin-dependent protein kinase in failing and nonfailing human hearts. Cardiovasc Res 42(1):254-261 pii: S0008-6363(98)00296-X (Pubitemid 29167092)
126. Danielsen W, v der Leyen H, Meyer W, Neumann J, Schmitz W, Scholz H, Starbatty J, Stein B, Doring V, Kalmar P (1989) Basal and isoprenaline- stimulated cAMP content in failing versus nonfailing human cardiac preparations. J Cardiovasc Pharmacol 14(1):171-173 (Pubitemid 19158089)
127. Antos CL, Frey N, Marx SO, Reiken S, Gaburjakova M, Richardson JA, Marks AR, Olson EN (2001) Dilated cardiomyopathy and sudden death resulting from constitutive activation of protein kinase a. Circ Res 89(11):997-1004 (Pubitemid 34640866)
128. Marks AR (2000) Cardiac intracellular calcium release channels: role in heart failure. Circ Res 87(1):8-11 (Pubitemid 30456928)
129. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101(4):365-376 pii: S0092-8674(00)80847-8
130. Reiken S, Gaburjakova M, Gaburjakova J, He Kl KL, Prieto A, Becker E, Yi Gh GH, Wang J, Burkhoff D, Marks AR (2001) beta-adrenergic receptor blockers restore cardiac calcium release channel (ryanodine receptor) structure and function in heart failure. Circulation 104(23):2843-2848 (Pubitemid 33126661)
131. Reiken S, Wehrens XH, Vest JA, Barbone A, Klotz S, Mancini D, Burkhoff D, Marks AR (2003) Beta-blockers restore calcium release channel function and improve cardiac muscle performance in human heart failure. Circulation 107(19):2459-2466. doi: 10.1161/01.CIR.0000068316.53218.49 (Pubitemid 36605229)
132. Carnegie GK, Burmeister BT (2011) A-kinase anchoring proteins that regulate cardiac remodeling. J Cardiovasc Pharmacol 58(5):451-458. doi: 10.1097/FJC.0b013e31821c0220
133. Shan J, Betzenhauser MJ, Kushnir A, Reiken S, Meli AC, Wronska A, Dura M, Chen BX, Marks AR (2010) Role of chronic ryanodine receptor phosphorylation in heart failure and beta-adrenergic receptor blockade in mice. J Clin Invest 120(12):4375-4387. doi: 10.1172/JCI37649
134. Monovich L, Koch KA, Burgis R, Osimboni E, Mann T, Wall D, Gao J, Feng Y, Vega RB, Turner BA, Hood DB, Law A, Papst PJ, Koditek D, Chapo JA, Reid BG, Melvin LS, Pagratis NC, McKinsey TA (2009) Suppression of HDAC nuclear export and cardiomyocyte hypertrophy by novel irreversible inhibitors of CRM1. Biochim Biophys Acta 1789(5):422-431. doi: 10.1016/j.bbagrm.2009.04.001
135. Monovich L, Vega RB, Meredith E, Miranda K, Rao C, Capparelli M, Lemon DD, Phan D, Koch KA, Chapo JA, Hood DB, McKinsey TA (2010) A novel kinase inhibitor establishes a predominant role for protein kinase D as a cardiac class IIa histone deacetylase kinase. FEBS Lett 584(3):631-637. doi: 10.1016/j.febslet.2009.12.014
136. Meredith EL, Ardayfio O, Beattie K, Dobler MR, Enyedy I, Gaul C, Hosagrahara V, Jewell C, Koch K, Lee W, Lehmann H, McKinsey TA, Miranda K, Pagratis N, Pancost M, Patnaik A, Phan D, Plato C, Qian M, Rajaraman V, Rao C, Rozhitskaya O, Ruppen T, Shi J, Siska SJ, Springer C, van Eis M, Vega RB, von Matt A, Yang L, Yoon T, Zhang JH, Zhu N, Monovich LG (2010) Identification of orally available naphthyridine protein kinase D inhibitors. J Med Chem 53(15):5400-5421. doi: 10.1021/jm100075z
137. Meredith EL, Beattie K, Burgis R, Capparelli M, Chapo J, Dipietro L, Gamber G, Enyedy I, Hood DB, Hosagrahara V, Jewell C, Koch KA, Lee W, Lemon DD, McKinsey TA, Miranda K, Pagratis N, Phan D, Plato C, Rao C, Rozhitskaya O, Soldermann N, Springer C, van Eis M, Vega RB, Yan W, Zhu Q, Monovich LG (2010) Identification of potent and selective amidobipyridyl inhibitors of protein kinase D. J Med Chem 53(15):5422-5438. doi: 10.1021/jm100076w
138. Zhang R, Khoo MS, Wu Y, Yang Y, Grueter CE, Ni G, Price EE Jr, Thiel W, Guatimosim S, Song LS, Madu EC, Shah AN, Vishnivetskaya TA, Atkinson JB, Gurevich VV, Salama G, Lederer WJ, Colbran RJ, Anderson ME (2005) Calmodulin kinase II inhibition protects against structural heart disease. Nat Med 11(4):409-417. doi: 10.1038/nm1215 (Pubitemid 40562331)
139. Swaminathan PD, Purohit A, Hund TJ, Anderson ME (2012) Calmodulin-dependent protein Kinase II: linking heart failure and arrhythmias. Circ Res 110(12):1661-1677. doi: 10.1161/CIRCRESAHA.111.243956
140. Tsuji Y, Hojo M, Voigt N, El-Armouche A, Inden Y, Murohara T, Dobrev D, Nattel S, Kodama I, Kamiya K (2011) Ca(2+)-related signaling and protein phosphorylation abnormalities play central roles in a new experimental model of electrical storm. Circulation 123(20):2192-2203. doi: 10.1161/CIRCULATIONAHA. 110.016683
141. Matsushima S, Zablocki D, Sadoshima J (2011) Application of recombinant thioredoxin1 for treatment of heart disease. J Mol Cell Cardiol 51(4):570-573. doi: 10.1016/j.yjmcc.2010.09.020
142. Tao L, Gao E, Bryan NS, Qu Y, Liu HR, Hu A, Christopher TA, Lopez BL, Yodoi J, Koch WJ, Feelisch M, Ma XL (2004) Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion: role of S-nitrosation [corrected]. Proc Natl Acad Sci USA 101(31):11471-11476. doi: 10.1073/pnas.0402941101 (Pubitemid 39038371)
143. Greco TM, Yu F, Guise AJ, Cristea IM (2011) Nuclear import of histone deacetylase 5 by requisite nuclear localization signal phosphorylation. Mol Cell Proteomics 10(2):M110004317. doi: 10.1074/mcp.M110.004317
144. Sucharov CC, Langer S, Bristow M, Leinwand L (2006) Shuttling of HDAC5 in H9C2 cells regulates YY1 function through CaMKIV/PKD and PP2A. Am J Physiol Cell Physiol 291(5):C1029-C1037. doi: 10.1152/ajpcell.00059.2006 (Pubitemid 44771821)
145. Varma A, Shah KB, Hess ML (2012) Phosphodiesterase inhibitors, congestive heart failure, and sudden death: time for re-evaluation. Congest Heart Fail. doi: 10.1111/j.1751-7133.2012.00293.x
146. Miska EA, Karlsson C, Langley E, Nielsen SJ, Pines J, Kouzarides T (1999) HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J 18(18):5099-5107. doi: 10.1093/emboj/18.18.5099 (Pubitemid 29443811)
147. Kao HY, Verdel A, Tsai CC, Simon C, Juguilon H, Khochbin S (2001) Mechanism for nucleocytoplasmic shuttling of histone deacetylase 7. J Biol Chem 276(50):47496-47507. doi: 10.1074/jbc.M107631200
148. Xu J, Gong NL, Bodi I, Aronow BJ, Backx PH, Molkentin JD (2006) Myocyte enhancer factors 2A and 2C induce dilated cardiomyopathy in transgenic mice. J Biol Chem 281(14):9152-9162. doi: 10.1074/jbc.M510217200 (Pubitemid 43864629)
149. Wilkins BJ, De Windt LJ, Bueno OF, Braz JC, Glascock BJ, Kimball TF, Molkentin JD (2002) Targeted disruption of NFATc3, but not NFATc4, reveals an intrinsic defect in calcineurin-mediated cardiac hypertrophic growth. Mol Cell Biol 22(21):7603-7613
150. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93(2):215-228 (Pubitemid 28180855)
151. Xing W, Zhang TC, Cao D, Wang Z, Antos CL, Li S, Wang Y, Olson EN, Wang DZ (2006) Myocardin induces cardiomyocyte hypertrophy. Circ Res 98(8):1089-1097. doi: 10.1161/01.RES.0000218781.23144.3e
152. Zhang X, Azhar G, Chai J, Sheridan P, Nagano K, Brown T, Yang J, Khrapko K, Borras AM, Lawitts J, Misra RP, Wei JY (2001) Cardiomyopathy in transgenic mice with cardiac-specific overexpression of serum response factor. Am J Physiol Heart Circ Physiol 280(4):H1782-H1792
153. Zhang X, Chai J, Azhar G, Sheridan P, Borras AM, Furr MC, Khrapko K, Lawitts J, Misra RP, Wei JY (2001) Early postnatal cardiac changes and premature death in transgenic mice overexpressing a mutant form of serum response factor. J Biol Chem 276(43):40033-40040. doi: 10.1074/jbc.M104934200
154. Parlakian A, Charvet C, Escoubet B, Mericskay M, Molkentin JD, Gary-Bobo G, De Windt LJ, Ludosky MA, Paulin D, Daegelen D, Tuil D, Li Z (2005) Temporally controlled onset of dilated cardiomyopathy through disruption of the SRF gene in adult heart. Circulation 112(19):2930-2939. doi: 10.1161/CIRCULATIONAHA.105. 533778 (Pubitemid 41612294)
155. Kuo CT, Morrisey EE, Anandappa R, Sigrist K, Lu MM, Parmacek MS, Soudais C, Leiden JM (1997) GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev 11(8):1048-1060 (Pubitemid 27199883)
156. Molkentin JD, Lin Q, Duncan SA, Olson EN (1997) Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev 11(8):1061-1072 (Pubitemid 27199884)
157. Oka T, Maillet M, Watt AJ, Schwartz RJ, Aronow BJ, Duncan SA, Molkentin JD (2006) Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ Res 98(6):837-845. doi: 10.1161/01.RES.0000215985.18538.c4
158. van Berlo JH, Elrod JW, van den Hoogenhof MM, York AJ, Aronow BJ, Duncan SA, Molkentin JD (2010) The transcription factor GATA-6 regulates pathological cardiac hypertrophy. Circ Res 107(8):1032-1040. doi: 10.1161/CIRCRESAHA.110. 220764
159. Liang Q, De Windt LJ, Witt SA, Kimball TR, Markham BE, Molkentin JD (2001) The transcription factors GATA4 and GATA6 regulate cardiomyocyte hypertrophy in vitro and in vivo. J Biol Chem 276(32):30245-30253. doi: 10.1074/jbc.M102174200
160. Nakagawa Y, Kuwahara K, Harada M, Takahashi N, Yasuno S, Adachi Y, Kawakami R, Nakanishi M, Tanimoto K, Usami S, Kinoshita H, Saito Y, Nakao K (2006) Class II HDACs mediate CaMK-dependent signaling to NRSF in ventricular myocytes. J Mol Cell Cardiol 41(6):1010-1022. doi: 10.1016/j.yjmcc.2006.08.010 (Pubitemid 44802867)
161. Chen ZF, Paquette AJ, Anderson DJ (1998) NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis. Nat Genet 20(2):136-142. doi: 10.1038/2431 (Pubitemid 28455445)
162. Kuwahara K, Saito Y, Takano M, Arai Y, Yasuno S, Nakagawa Y, Takahashi N, Adachi Y, Takemura G, Horie M, Miyamoto Y, Morisaki T, Kuratomi S, Noma A, Fujiwara H, Yoshimasa Y, Kinoshita H, Kawakami R, Kishimoto I, Nakanishi M, Usami S, Harada M, Nakao K (2003) NRSF regulates the fetal cardiac gene program and maintains normal cardiac structure and function. EMBO J 22(23):6310-6321. doi: 10.1093/emboj/cdg601 (Pubitemid 37522588)
163. Sucharov CC, Dockstader K, McKinsey TA (2008) YY1 protects cardiac myocytes from pathologic hypertrophy by interacting with HDAC5. Mol Biol Cell 19(10):4141-4153. doi: 10.1091/mbc.E07-12-1217