Neurohormonal regulation of cardiac histone deacetylase 5 nuclear localization by phosphorylation-dependent and phosphorylation-independent mechanisms

Circulation Research

Volumn 110, Issue 12, 2012, Pages 1585-1595

  Haworth, Robert S ^a   Stathopoulou, Konstantina ^a   Candasamy, Alexandra J ^a   Avkiran, Metin ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cardiac hypertrophy; Histone deacetylases; Myocyte enhancer factor 2; Protein kinases; Signal transduction

Indexed keywords

ATENOLOL; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENDOTHELIN 1; HEART ENZYME; HISTONE DEACETYLASE 5; ISOPRENALINE; MYOCYTE ENHANCER FACTOR 2; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; HEART FAILURE; HEART MUSCLE CELL; HORMONAL REGULATION; MUTANT; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CELLS, CULTURED; HISTONE DEACETYLASES; MYOCYTES, CARDIAC; NEUROTRANSMITTER AGENTS; PHOSPHORYLATION; RATS;

EID: 84862279509     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.263665     Document Type: Article

References (47)

1. Kim Y, Phan D, van Rooij E, Wang DZ, McAnally J, Qi X, Richardson JA, Hill JA, Bassel-Duby R, Olson EN. The MEF2D transcription factor mediates stress-dependent cardiac remodeling in mice. J Clin Invest. 2008;118:124-132.
2. Konno T, Chen D, Wang L, Wakimoto H, Teekakirikul P, Nayor M, Kawana M, Eminaga S, Gorham JM, Pandya K, Smithies O, Naya FJ, Olson EN, Seidman JG, Seidman CE. Heterogeneous myocyte enhancer factor-2 (Mef2) activation in myocytes predicts focal scarring in hypertrophic cardiomyopathy. Proc Natl Acad Sci USA. 2010;107: 18097-18102.
3. McKinsey TA, Olson EN. Cardiac histone acetylation: therapeutic opportunities abound. Trends Genet. 2004;20:206-213. (Pubitemid 38369192)
4. Backs J, Olson EN. Control of cardiac growth by histone acetylation/deacetylation. Circ Res. 2006;98:15-24. (Pubitemid 43977219)
5. Anderson ME, Brown JH, Bers DM. CaMKII in myocardial hypertrophy and heart failure. J Mol Cell Cardiol. 2011;51:468-473.
6. Avkiran M, Rowland AJ, Cuello F, Haworth RS. Protein kinase D in the cardiovascular system: emerging roles in health and disease Circ Res. 2008;102:157-163. (Pubitemid 351651119)
7. Vega RB, Harrison BC, Meadows E, Roberts CR, Papst PJ, Olson EN, McKinsey TA. Protein kinase C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol Cell Biol. 2004;24:8374-8385. (Pubitemid 39245060)
8. Backs J, Song K, Bezprozvannaya S, Chang S, Olson EN. CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J Clin Invest. 2006;116:1853-1864. (Pubitemid 44033310)
9. Harrison BC, Kim MS, van Rooij E, Plato CF, Papst PJ, Vega RB, McAnally JA, Richardson JA, Bassel-Duby R, Olson EN, McKinsey TA. Regulation of cardiac stress signaling by protein kinase D1. Mol Cell Biol. 2006;26:3875-3888. (Pubitemid 43726404)
10. Fielitz J, Kim MS, Shelton JM, Qi X, Hill JA, Richardson JA, Bassel-Duby R, Olson EN. Requirement for protein kinase D1 for pathological cardiac remodeling. Proc Natl Acad Sci USA. 2008;105: 3059-3063. (Pubitemid 351723667)
11. 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. The isoform of CaM kinase II is required for pathological cardiac hypertrophy and remodeling after pressure overload. Proc Natl Acad Sci USA. 2009;106:2342-2347.
12. Wu X, Zhang T, Bossuyt J, Li X, McKinsey TA, Dedman JR, Olson EN, Chen J, Brown JH, Bers DM. Local InsP3-dependent perinuclear Ca2 signaling in cardiac myocyte excitation-transcription coupling. J Clin Invest. 2006;116:675-682. (Pubitemid 43326876)
13. Ha CH, Kim JY, Zhao J, Wang W, Jhun BS, Wong C, Jin ZG. 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. 2010;107:15467-15472.
14. Backs J, Worst BC, Lehmann LH, Patrick DM, Jebessa Z, Kreusser MM, Sun Q, Chen L, Heft C, Katus HA, Olson EN. Selective repression of MEF2 activity by PKA-dependent proteolysis of HDAC4. J Cell Biol. 2011;195:403-415.
15. Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD, Vatner SF, Sadoshima J. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell. 2008;133:978-993. (Pubitemid 351787743)
16. Haworth RS, Roberts NA, Cuello F, Avkiran M. Regulation of protein kinase D activity in adult myocardium: novel counter-regulatory roles for protein kinase C2 and protein kinase A. J Mol Cell Cardiol. 2007;43:686-695. (Pubitemid 350166389)
17. Haworth RS, Cuello F, Avkiran M. Regulation by phosphodiesterase isoforms of protein kinase A-mediated attenuation of myocardial protein kinase D activation. Basic Res Cardiol. 2011;106:51-63.
18. Haworth RS, Goss MW, Rozengurt E, Avkiran M. Expression and activity of protein kinase D/protein kinase C2 in myocardium: evidence for 1-adrenergic receptor-and protein kinase C-mediated regulation. J Mol Cell Cardiol. 2000;32:1013-1023. (Pubitemid 30663108)
19. Snabaitis AK, Cuello F, Avkiran M. Protein kinase B/Akt phosphorylates and inhibits the cardiac Naf/Hrexchanger NHE1. Circ Res. 2008;103: 881-890.
20. Cuello F, Bardswell SC, Haworth RS, Yin X, Lutz S, Wieland T, Mayr M, Kentish JC, Avkiran M. Protein kinase D selectively targets cardiac troponin I and regulates myofilament Ca2 sensitivity in ventricular myocytes. Circ Res. 2007;100:864-873. (Pubitemid 46555692)
21. Bain J, Plater L, Elliott M, Shpiro N, Hastie J, McLauchlan H, Klevernic I, Arthur S, Alessi D, Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochem J. 2007;408:297-315.
22. Haworth RS, Cuello F, Herron TJ, Franzen G, Kentish JC, Gautel M, Avkiran M. Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function. Circ Res. 2004;95: 1091-1099. (Pubitemid 39557896)
23. Peng Y, Lambert AA, Papst P, Pitts KR. Agonist-induced nuclear export of GFP-HDAC5 in isolated adult rat ventricular myocytes. J Pharmacol Toxicol Methods. 2009;59:135-140.
24. Nishikawa K, Toker A, Johannes F-J, Songyang Z, Cantley LC. Determination of the specific substrate sequence motifs of protein kinase C isozymes. J Biol Chem. 1997;272:952-960. (Pubitemid 27034586)
25. Hutti JE, Jarrell ET, Chang JD, Abbott DW, Storz P, Toker A, Cantley LC, Turk BE. A rapid method for determining protein kinase phosphorylation specificity. Nat Methods. 2004;1:27-29.
26. McKinsey TA, Olson EN. Toward transcriptional therapies for the failing heart: chemical screens to modulate genes. J Clin Invest. 2005;115: 538-546. (Pubitemid 40322223)
27. Meredith EL, Beattie K, Burgis R, et al. Identification of potent and selective amidobipyridyl inhibitors of protein kinase D. J Med Chem. 2010;53:5422-5438.
28. Monovich L, Vega RB, Meredith E, Miranda K, Rao C, Capparelli M, Lemon DD, Phan D, Koch KA, Chapo JA, Hood DB, McKinsey TA. A novel kinase inhibitor establishes a predominant role for protein kinase D as a cardiac class IIa histone deacetylase kinase. FEBS Lett. 2010;584: 631-637.
29. Roberts NA, Haworth RS, Avkiran M. Effects of bisindolylmaleimide PKC inhibitors on p90RSK activity in vitro and in adult ventricular myocytes. Br J Pharmacol. 2005;145:477-489. (Pubitemid 40966277)
30. Bossuyt J, Helmstadter K, Wu X, Clements-Jewery H, Haworth RS, Avkiran M, Martin JL, Pogwizd SM, Bers DM. Ca2f/calmodulindependent protein kinase II and protein kinase D overexpression reinforce the histone deacetylase 5 redistribution in heart failure. Circ Res. 2008;102:695-702. (Pubitemid 351457864)
31. Vinogradova TM, Lyashkov AE, Zhu W, et al. High basal protein kinase A-dependent phosphorylation drives rhythmic internal Ca2 store oscillations and spontaneous beating of cardiac pacemaker cells. Circ Res. 2006;98:505-514.
32. Grimm M, Brown JH.-Adrenergic receptor signaling in the heart: role of CaMKII. J Mol Cell Cardiol. 2010;48:322-330.
33. Greco TM, Yu F, Guise AJ, Cristea IM. Nuclear import of histone deacetylase 5 by requisite nuclear localization signal phosphorylation. Mol Cell Proteomics. 2011;10:M110.004317.
34. Sossalla S, Fluschnik N, Schotola H, Ort KR, Neef S, Schulte T, Wittkopper K, Renner A, Schmitto JD, Gummert J, El-Armouche A, Hasenfuss G, Maier LS. Inhibition of elevated Ca2f/calmodulindependent protein kinase II improves contractility in human failing myocardium. Circ Res. 2010;107:1150-1161.
35. Kinoshita E, Kinoshita-Kikuta E, Koike T. Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat Protoc. 2009;4: 1513-1521.
36. Andersson DC, Fauconnier J, Yamada T, Lacampagne A, Zhang SJ, Katz A, Westerblad H. Mitochondrial production of reactive oxygen species contributes to the-adrenergic stimulation of mouse cardiomyocytes. J Physiol. 2011;589:1791-1801.
37. Sucharov CC, Mariner PD, Nunley KR, Long C, Leinwand L, Bristow MR. A2 1-adrenergic receptor CaM kinase II-dependent pathway mediates cardiac myocyte fetal gene induction. Am J Physiol Heart Circ Physiol. 2006;291:H1299-H1308. (Pubitemid 44343675)
38. Zhang R, Khoo MS, Wu Y, et al. Calmodulin kinase II inhibition protects against structural heart disease. Nat Med. 2005;11:409-417. (Pubitemid 40562331)
39. Sucharov CC, Dockstader K, Nunley K, McKinsey TA, Bristow M. Adrenergic receptor stimulation and activation of protein kinase A protect against 1-adrenergic-mediated phosphorylation of protein kinase D and histone deacetylase 5. J Card Fail. 2011;17:592-600.
40. Ke Y, Wang L, Pyle WG, de Tombe PP, Solaro RJ. Intracellular localization and functional effects of P21-activated kinase-1 (Pak1) in cardiac myocytes. Circ Res. 2004;94:194-200. (Pubitemid 38197451)
41. Yin X, Cuello F, Mayr U, Hao Z, Hornshaw M, Ehler E, Avkiran M, Mayr M. Proteomics analysis of the cardiac myofilament subproteome reveals dynamic alterations in phosphatase subunit distribution. Mol Cell Proteomics. 2010;9:497-509.
42. Zhao M, New L, Kravchenko VV, Kato Y, Gram H, di Padova F, Olson EN, Ulevitch RJ, Han J. Regulation of the MEF2 family of transcription factors by p38. Mol Cell Biol. 1999;19:21-30. (Pubitemid 29018406)
43. Wei JQ, Shehadeh LA, Mitrani JM, Pessanha M, Slepak TI, Webster KA, Bishopric NH. Quantitative control of adaptive cardiac hypertrophy by acetyltransferase p300. Circulation. 2008;118:934-946.
44. Backs J, Backs T, Bezprozvannaya S, McKinsey TA, Olson EN. Histone deacetylase 5 acquires calcium/calmodulin-dependent kinase II responsiveness by oligomerization with histone deacetylase 4. Mol Cell Biol. 2008;28:3437-3445. (Pubitemid 351657105)
45. Meredith EL, Ardayfio O, Beattie K, et al. Identification of orally available naphthyridine protein kinase D inhibitors. J Med Chem. 2010; 53:5400-5421.
46. Bristow MR. Treatment of chronic heart failure with-adrenergic receptor antagonists: a convergence of receptor pharmacology and clinical cardiology. Circ Res. 2011;109:1176-1194.
47. Lowes BD, Gilbert EM, Abraham WT, Minobe WA, Larrabee P, Ferguson D, Wolfel EE, Lindenfeld J, Tsvetkova T, Robertson AD, Quaife RA, Bristow MR. Myocardial gene expression in dilated cardiomyopathy treated with beta-blocking agents. N Engl J Med. 2002;346:1357-1365. (Pubitemid 34754608)