DUSP8 Regulates Cardiac Ventricular Remodeling by Altering ERK1/2 Signaling

Circulation Research

Volumn 119, Issue 2, 2016, Pages 249-260

  Liu, Ruijie ^a   Van Berlo, Jop H ^a,c   York, Allen J ^a   Vagnozzi, Ronald J ^a   Maillet, Marjorie ^a   Molkentin, Jeffery D ^a,b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

dilated cardiomyopathy; disease susceptibility; dual specificity phosphatase; heart failure; myocardium

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE; DUAL SPECIFICITY PHOSPHATASE 8; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; DUSP8 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CARDIOMYOPATHY; CELL GROWTH; CELL STRUCTURE; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENZYME ACTIVATION; GENE SILENCING; HEART FAILURE; HEART MUSCLE CONTRACTILITY; HEART STRESS; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VASODILATATION; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; KNOCKOUT MOUSE; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; DUAL-SPECIFICITY PHOSPHATASES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYOCYTES, CARDIAC; RATS; VENTRICULAR REMODELING;

EID: 84973313895     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.308238     Document Type: Article

References (46)

1. Kyriakis JM, Avruch J, Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol Rev 2012 92 689 737. doi: 10.1152/physrev.00028.2011
2. Cargnello M, Roux PP, Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 2011 75 50 83. doi: 10.1128/MMBR.00031-10
3. Goldsmith ZG, Dhanasekaran DN, G protein regulation of MAPK networks. Oncogene 2007 26 3122 3142. doi: 10.1038/sj.onc.1210407
4. Hall A, Rho GTPases and the control of cell behaviour. Biochem Soc Trans 2005 33 891 895. doi: 10.1042/BST20050891
5. Goupil E, Wisehart V, Khoury E, Zimmerman B, Jaffal S, Hébert TE, Laporte SA, Biasing the prostaglandin F2α receptor responses toward EGFR-dependent transactivation of MAPK. Mol Endocrinol 2012 26 1189 1202. doi: 10.1210/me.2011-1245
6. Li L, Fan D, Wang C, Wang JY, Cui XB, Wu D, Zhou Y, Wu LL, Angiotensin II increases periostin expression via Ras/p38 MAPK/CREB and ERK1/2/TGF-β1 pathways in cardiac fibroblasts. Cardiovasc Res 2011 91 80 89. doi: 10.1093/cvr/cvr067
7. Braz JC, Bueno OF, Liang Q, Wilkins BJ, Dai YS, Parsons S, Braunwart J, Glascock BJ, Klevitsky R, Kimball TF, Hewett TE, Molkentin JD, Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling. J Clin Invest 2003 111 1475 1486. doi: 10.1172/JCI17295
8. Nishida K, Yamaguchi O, Hirotani S, p38alpha mitogen-activated protein kinase plays a critical role in cardiomyocyte survival but not in cardiac hypertrophic growth in response to pressure overload. Mol Cell Biol 2004 24 10611 10620. doi: 10.1128/MCB.24.24.10611-10620.2004
9. Liang Q, Bueno OF, Wilkins BJ, Kuan CY, Xia Y, Molkentin JD, c-Jun N-terminal kinases (JNK) antagonize cardiac growth through cross-talk with calcineurin-NFAT signaling. EMBO J 2003 22 5079 5089. doi: 10.1093/emboj/cdg474
10. Liu W, Zi M, Jin J, Prehar S, Oceandy D, Kimura TE, Lei M, Neyses L, Weston AH, Cartwright EJ, Wang X, Cardiac-specific deletion of mkk4 reveals its role in pathological hypertrophic remodeling but not in physiological cardiac growth. Circ Res 2009 104 905 914. doi: 10.1161/CIRCRESAHA.108.188292
11. Liu W, Zi M, Chi H, Jin J, Prehar S, Neyses L, Cartwright EJ, Flavell RA, Davis RJ, Wang X, Deprivation of MKK7 in cardiomyocytes provokes heart failure in mice when exposed to pressure overload. J Mol Cell Cardiol 2011 50 702 711. doi: 10.1016/j.yjmcc.2011.01.013
12. Bueno OF, De Windt LJ, Tymitz KM, Witt SA, Kimball TR, Klevitsky R, Hewett TE, Jones SP, Lefer DJ, Peng CF, Kitsis RN, Molkentin JD, The MEK1-ERK1/2 signaling pathway promotes compensated cardiac hypertrophy in transgenic mice. EMBO J 2000 19 6341 6350. doi: 10.1093/emboj/19.23.6341
13. Kehat I, Davis J, Tiburcy M, Accornero F, Saba-El-Leil MK, Maillet M, York AJ, Lorenz JN, Zimmermann WH, Meloche S, Molkentin JD, Extracellular signal-regulated kinases 1 and 2 regulate the balance between eccentric and concentric cardiac growth. Circ Res 2011 108 176 183. doi: 10.1161/CIRCRESAHA.110.231514
14. Purcell NH, Wilkins BJ, York A, Saba-El-Leil MK, Meloche S, Robbins J, Molkentin JD, Genetic inhibition of cardiac ERK1/2 promotes stress-induced apoptosis and heart failure but has no effect on hypertrophy in vivo. Proc Natl Acad Sci USA 2007 104 14074 14079. doi: 10.1073/pnas.0610906104
15. Caunt CJ, Keyse SM, Dual-specificity MAP kinase phosphatases (MKPs): shaping the outcome of MAP kinase signalling. FEBS J 2013 280 489 504. doi: 10.1111/j.1742-4658.2012.08716.x
16. Salojin K, Oravecz T, Regulation of innate immunity by MAPK dual-specificity phosphatases: knockout models reveal new tricks of old genes. J Leukoc Biol 2007 81 860 869. doi: 10.1189/jlb.1006639
17. Li J, Gorospe M, Hutter D, Barnes J, Keyse SM, Liu Y, Transcriptional induction of MKP-1 in response to stress is associated with histone H3 phosphorylation-acetylation. Mol Cell Biol 2001 21 8213 8224. doi: 10.1128/MCB.21.23.8213-8224.2001
18. Mori Sequeiros García M, Gómez NV, Gorostizaga A, Acquier A, González-Calvar SI, Mendez CF, Paz C, MAP kinase phosphatase-3 (MKP-3) is transcriptionally and post-translationally up-regulated by hCG and modulates cAMP-induced p21 expression in MA-10 Leydig cells. Mol Cell Endocrinol 2013 371 174 181. doi: 10.1016/j.mce.2012.12.006
19. Yang D, Xie P, Liu Z, Ischemia/reperfusion-induced MKP-3 impairs endothelial NO formation via inactivation of ERK1/2 pathway. PLoS One 2012 7 e42076. doi: 10.1371/journal.pone.0042076
20. Auger-Messier M, Accornero F, Goonasekera SA, Bueno OF, Lorenz JN, van Berlo JH, Willette RN, Molkentin JD, Unrestrained p38 MAPK activation in Dusp1/4 double-null mice induces cardiomyopathy. Circ Res 2013 112 48 56. doi: 10.1161/CIRCRESAHA.112.272963
21. Maillet M, Purcell NH, Sargent MA, York AJ, Bueno OF, Molkentin JD, DUSP6 (MKP3) null mice show enhanced ERK1/2 phosphorylation at baseline and increased myocyte proliferation in the heart affecting disease susceptibility. J Biol Chem 2008 283 31246 31255. doi: 10.1074/jbc.M806085200
22. Ferguson BS, Harrison BC, Jeong MY, Reid BG, Wempe MF, Wagner FF, Holson EB, McKinsey TA, Signal-dependent repression of DUSP5 by class I HDACs controls nuclear ERK activity and cardiomyocyte hypertrophy. Proc Natl Acad Sci USA 2013 110 9806 9811. doi: 10.1073/pnas.1301509110
23. Molina G, Vogt A, Bakan A, Dai W, Queiroz de Oliveira P, Znosko W, Smithgall TE, Bahar I, Lazo JS, Day BW, Tsang M, Zebrafish chemical screening reveals an inhibitor of Dusp6 that expands cardiac cell lineages. Nat Chem Biol 2009 5 680 687. doi: 10.1038/nchembio.190
24. Huang CY, Tan TH, DUSPs, to MAP kinases and beyond. Cell Biosci 2012 2 24. doi: 10.1186/2045-3701-2-24
25. Martell KJ, Seasholtz AF, Kwak SP, Clemens KK, Dixon JE, hVH-5: a protein tyrosine phosphatase abundant in brain that inactivates mitogen-activated protein kinase. J Neurochem 1995 65 1823 1833
26. Chen YR, Shrivastava A, Tan TH, Down-regulation of the c-Jun N-terminal kinase (JNK) phosphatase M3/6 and activation of JNK by hydrogen peroxide and pyrrolidine dithiocarbamate. Oncogene 2001 20 367 374. doi: 10.1038/sj.onc.1204105
27. Theodosiou A, Ashworth A, Differential effects of stress stimuli on a JNK-inactivating phosphatase. Oncogene 2002 21 2387 2397. doi: 10.1038/sj.onc.1205309
28. Muda M, Theodosiou A, Rodrigues N, Boschert U, Camps M, Gillieron C, Davies K, Ashworth A, Arkinstall S, The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases. J Biol Chem 1996 271 27205 27208
29. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD, Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 2004 94 110 118. doi: 10.1161/01.RES.0000109415.17511.18
30. De Windt LJ, Lim HW, Haq S, Force T, Molkentin JD, Calcineurin promotes protein kinase C and c-Jun NH2-terminal kinase activation in the heart. Cross-talk between cardiac hypertrophic signaling pathways. J Biol Chem 2000 275 13571 13579
31. Liu R, Correll RN, Davis J, Vagnozzi RJ, York AJ, Sargent MA, Nairn AC, Molkentin JD, Cardiac-specific deletion of protein phosphatase 1β promotes increased myofilament protein phosphorylation and contractile alterations. J Mol Cell Cardiol 2015 87 204 213. doi: 10.1016/j.yjmcc.2015.08.018
32. Barth AS, Kuner R, Buness A, Ruschhaupt M, Merk S, Zwermann L, Kääb S, Kreuzer E, Steinbeck G, Mansmann U, Poustka A, Nabauer M, Sültmann H, Identification of a common gene expression signature in dilated cardiomyopathy across independent microarray studies. J Am Coll Cardiol 2006 48 1610 1617. doi: 10.1016/j.jacc.2006.07.026
33. Lim HW, New L, Han J, Molkentin JD, Calcineurin enhances MAPK phosphatase-1 expression and p38 MAPK inactivation in cardiac myocytes. J Biol Chem 2001 276 15913 15919. doi: 10.1074/jbc.M100452200
34. Tardiff JC, Hewett TE, Factor SM, Vikstrom KL, Robbins J, Leinwand LA, Expression of the beta (slow)-isoform of MHC in the adult mouse heart causes dominant-negative functional effects. Am J Physiol Heart Circ Physiol 2000 278 H412 H419
35. Liu S, Sun JP, Zhou B, Zhang ZY, Structural basis of docking interactions between ERK2 and MAP kinase phosphatase 3. Proc Natl Acad Sci USA 2006 103 5326 5331. doi: 10.1073/pnas.0510506103
36. Zhou B, Zhang J, Liu S, Reddy S, Wang F, Zhang ZY, Mapping ERK2-MKP3 binding interfaces by hydrogen/deuterium exchange mass spectrometry. J Biol Chem 2006 281 38834 38844. doi: 10.1074/jbc.M608916200
37. Lips DJ, Bueno OF, Wilkins BJ, Purcell NH, Kaiser RA, Lorenz JN, Voisin L, Saba-El-Leil MK, Meloche S, Pouysségur J, Pagès G, De Windt LJ, Doevendans PA, Molkentin JD, MEK1-ERK2 signaling pathway protects myocardium from ischemic injury in vivo. Circulation 2004 109 1938 1941. doi: 10.1161/01.CIR.0000127126.73759.23
38. Maejima Y, Galeotti J, Molkentin JD, Sadoshima J, Zhai P, Constitutively active MEK1 rescues cardiac dysfunction caused by overexpressed GSK-3α during aging and hemodynamic pressure overload. Am J Physiol Heart Circ Physiol 2012 303 H979 H988. doi: 10.1152/ajpheart.00415.2012
39. Palacios C, Collins MK, Perkins GR, The JNK phosphatase M3/6 is inhibited by protein-damaging stress. Curr Biol 2001 11 1439 1443
40. Cotsiki M, Oehrl W, Samiotaki M, Theodosiou A, Panayotou G, Phosphorylation of the M3/6 dual-specificity phosphatase enhances the activation of JNK by arsenite. Cell Signal 2012 24 664 676. doi: 10.1016/j.cellsig.2011.10.015
41. Bueno OF, De Windt LJ, Lim HW, Tymitz KM, Witt SA, Kimball TR, Molkentin JD, The dual-specificity phosphatase MKP-1 limits the cardiac hypertrophic response in vitro and in vivo. Circ Res 2001 88 88 96
42. Tanoue T, Adachi M, Moriguchi T, Nishida E, A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat Cell Biol 2000 2 110 116. doi: 10.1038/35000065
43. Kehat I, Molkentin JD, Extracellular signal-regulated kinase 1/2 (ERK1/2) signaling in cardiac hypertrophy. Ann N Y Acad Sci 2010 1188 96 102. doi: 10.1111/j.1749-6632.2009.05088.x
44. Kaiser RA, Liang Q, Bueno O, Huang Y, Lackey T, Klevitsky R, Hewett TE, Molkentin JD, Genetic inhibition or activation of JNK1/2 protects the myocardium from ischemia-reperfusion-induced cell death in vivo. J Biol Chem 2005 280 32602 32608. doi: 10.1074/jbc.M500684200
45. Liao P, Georgakopoulos D, Kovacs A, Zheng M, Lerner D, Pu H, Saffitz J, Chien K, Xiao RP, Kass DA, Wang Y, The in vivo role of p38 MAP kinases in cardiac remodeling and restrictive cardiomyopathy. Proc Natl Acad Sci USA 2001 98 12283 12288. doi: 10.1073/pnas.211086598
46. Rechsteiner M, Rogers SW, PEST sequences and regulation by proteolysis. Trends Biochem Sci 1996 21 267 271