The AP-1 Transcription Factor c-Jun Prevents Stress-Imposed Maladaptive Remodeling of the Heart

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Windak, Renata ^a   Müller, Julius ^a   Felley, Allison ^b   Akhmedov, Alexander ^c   Wagner, Erwin F ^d   Pedrazzini, Thierry ^b   Sumara, Grzegorz ^a,e   Ricci, Romeo ^a,e,f  

^a ETH ZURICH   (Switzerland)

^b Laboratory of Cellular and Molecular Neurotherapies   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d BBVA University Institute for Economic and Social Analysis University of Alcalá   (Spain)

^e UNIVERSITÉ DE STRASBOURG   (France)

^f HÔPITAL CIVIL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN C FOS; PROTEIN C JUN; SCLEROPROTEIN; TRANSCRIPTION FACTOR AP 1;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARDIOVASCULAR RESPONSE; CELL COUNT; CONTROLLED STUDY; DOWN REGULATION; GENOTYPE; HEART FUNCTION; HEART MUSCLE CELL; HEART SIZE; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE OVERLOAD; HEART VENTRICLE PRESSURE; HEART VENTRICLE REMODELING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SARCOMERE; UPREGULATION;

ANIMALS; CARDIOMEGALY; GENE DELETION; HEART; MICE; MICE, INBRED C57BL; MYOCARDIUM; MYOCYTES, CARDIAC; PRESSURE; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; TRANSCRIPTION FACTOR AP-1;

EID: 84883775293     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073294     Document Type: Article

References (71)

1. Hill JA, Olson EN, (2008) Cardiac plasticity. N Engl J Med 358: 1370-1380.
2. Olson EN, (2004) A decade of discoveries in cardiac biology. Nat Med 10: 467-474.
3. Hoshijima M, Chien KR, (2002) Mixed signals in heart failure: cancer rules. J Clin Invest 109: 849-855.
4. Chien KR, (1999) Stress pathways and heart failure. Cell 98: 555-558.
5. Morita H, Seidman J, Seidman CE, (2005) Genetic causes of human heart failure. J Clin Invest 115: 518-526.
6. Liang Q, Molkentin JD, (2003) Redefining the roles of p38 and JNK signaling in cardiac hypertrophy: dichotomy between cultured myocytes and animal models. J Mol Cell Cardiol 35: 1385-1394.
7. Heineke J, Molkentin JD, (2006) Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 7: 589-600.
8. Chang L, Karin M, (2001) Mammalian MAP kinase signalling cascades. Nature 410: 37-40.
9. Bueno OF, De Windt LJ, Tymitz KM, Witt SA, Kimball TR, et al. (2000) The MEK1-ERK1/2 signaling pathway promotes compensated cardiac hypertrophy in transgenic mice. EMBO J 19: 6341-6350.
10. Sanna B, Bueno OF, Dai YS, Wilkins BJ, Molkentin JD, (2005) Direct and indirect interactions between calcineurin-NFAT and MEK1-extracellular signal-regulated kinase 1/2 signaling pathways regulate cardiac gene expression and cellular growth. Mol Cell Biol 25: 865-878.
11. Liao P, Georgakopoulos D, Kovacs A, Zheng M, Lerner D, et al. (2001) The in vivo role of p38 MAP kinases in cardiac remodeling and restrictive cardiomyopathy. Proc Natl Acad Sci U S A 98: 12283-12288.
12. Petrich BG, Molkentin JD, Wang Y, (2003) Temporal activation of c-Jun N-terminal kinase in adult transgenic heart via cre-loxP-mediated DNA recombination. FASEB J 17: 749-751.
13. Petrich BG, Gong X, Lerner DL, Wang X, Brown JH, et al. (2002) c-Jun N-terminal kinase activation mediates downregulation of connexin43 in cardiomyocytes. Circ Res 91: 640-647.
14. Liang Q, Bueno OF, Wilkins BJ, Kuan CY, Xia Y, et al. (2003) c-Jun N-terminal kinases (JNK) antagonize cardiac growth through cross-talk with calcineurin-NFAT signaling. EMBO J 22: 5079-5089.
15. Braz JC, Bueno OF, Liang Q, Wilkins BJ, Dai YS, et al. (2003) Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling. J Clin Invest 111: 1475-1486.
16. Tachibana H, Perrino C, Takaoka H, Davis RJ, Naga Prasad SV, et al. (2006) JNK1 is required to preserve cardiac function in the early response to pressure overload. Biochem Biophys Res Commun 343: 1060-1066.
17. Engel FB, Schebesta M, Duong MT, Lu G, Ren S, et al. (2005) p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev 19: 1175-1187.
18. Potthoff MJ, Olson EN, (2007) MEF2: a central regulator of diverse developmental programs. Development 134: 4131-4140.
19. Eferl R, Wagner EF, (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3: 859-868.
20. Parker TG, Schneider MD, (1991) Growth factors, proto-oncogenes, and plasticity of the cardiac phenotype. Annu Rev Physiol 53: 179-200.
21. Schneider MD, McLellan WR, Black FM, Parker TG, (1992) Growth factors, growth factor response elements, and the cardiac phenotype. Basic Res Cardiol 87Suppl 2: 33-48.
22. Komuro I, Kaida T, Shibazaki Y, Kurabayashi M, Katoh Y, et al. (1990) Stretching cardiac myocytes stimulates protooncogene expression. J Biol Chem 265: 3595-3598.
23. Sadoshima J, Izumo S, (1997) The cellular and molecular response of cardiac myocytes to mechanical stress. Annu Rev Physiol 59: 551-571.
24. Ricci R, Eriksson U, Oudit GY, Eferl R, Akhmedov A, et al. (2005) Distinct functions of junD in cardiac hypertrophy and heart failure. Genes Dev 19: 208-213.
25. Hilfiker-Kleiner D, Hilfiker A, Kaminski K, Schaefer A, Park JK, et al. (2005) Lack of JunD promotes pressure overload-induced apoptosis, hypertrophic growth, and angiogenesis in the heart. Circulation 112: 1470-1477.
26. Omura T, Yoshiyama M, Yoshida K, Nakamura Y, Kim S, et al. (2002) Dominant negative mutant of c-Jun inhibits cardiomyocyte hypertrophy induced by endothelin 1 and phenylephrine. Hypertension 39: 81-86.
27. Taimor G, Schluter KD, Best P, Helmig S, Piper HM, (2004) Transcription activator protein 1 mediates alpha- but not beta-adrenergic hypertrophic growth responses in adult cardiomyocytes. Am J Physiol Heart Circ Physiol 286: H2369-2375.
28. Bishopric NH, Jayasena V, Webster KA, (1992) Positive regulation of the skeletal alpha-actin gene by Fos and Jun in cardiac myocytes. J Biol Chem 267: 25535-25540.
29. Kovacic-Milivojevic B, Gardner DG, (1992) Divergent regulation of the human atrial natriuretic peptide gene by c-jun and c-fos. Mol Cell Biol 12: 292-301.
30. Rosenzweig A, Halazonetis TD, Seidman JG, Seidman CE, (1991) Proximal regulatory domains of rat atrial natriuretic factor gene. Circulation 84: 1256-1265.
31. Paradis P, MacLellan WR, Belaguli NS, Schwartz RJ, Schneider MD, (1996) Serum response factor mediates AP-1-dependent induction of the skeletal alpha-actin promoter in ventricular myocytes. J Biol Chem 271: 10827-10833.
32. Behrens A, Sibilia M, David JP, Mohle-Steinlein U, Tronche F, et al. (2002) Impaired postnatal hepatocyte proliferation and liver regeneration in mice lacking c-jun in the liver. Embo J 21: 1782-1790.
33. Fleischmann A, Hvalby O, Jensen V, Strekalova T, Zacher C, et al. (2003) Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci 23: 9116-9122.
34. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, et al. (1998) A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 2: 559-569.
35. Kassiri Z, Oudit GY, Sanchez O, Dawood F, Mohammed FF, et al. (2005) Combination of tumor necrosis factor-alpha ablation and matrix metalloproteinase inhibition prevents heart failure after pressure overload in tissue inhibitor of metalloproteinase-3 knock-out mice. Circ Res 97: 380-390.
36. Krishnan J, Suter M, Windak R, Krebs T, Felley A, et al. (2009) Activation of a HIF1alpha-PPARgamma axis underlies the integration of glycolytic and lipid anabolic pathways in pathologic cardiac hypertrophy. Cell Metab 9: 512-524.
37. Eferl R, Ricci R, Kenner L, Zenz R, David JP, et al. (2003) Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell 112: 181-192.
38. Crackower MA, Oudit GY, Kozieradzki I, Sarao R, Sun H, et al. (2002) Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell 110: 737-749.
39. Li YY, Feldman AM, Sun Y, McTiernan CF, (1998) Differential expression of tissue inhibitors of metalloproteinases in the failing human heart. Circulation 98: 1728-1734.
40. Sugden PH, (2001) Signalling pathways in cardiac myocyte hypertrophy. Ann Med 33: 611-622.
41. Rockman HA, Ross RS, Harris AN, Knowlton KU, Steinhelper ME, et al. (1991) Segregation of atrial-specific and inducible expression of an atrial natriuretic factor transgene in an in vivo murine model of cardiac hypertrophy. Proc Natl Acad Sci U S A 88: 8277-8281.
42. Kang PM, Izumo S, (2003) Apoptosis in heart: basic mechanisms and implications in cardiovascular diseases. Trends Mol Med 9: 177-182.
43. Spinale FG, (2007) Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev 87: 1285-1342.
44. Seeland U, Haeuseler C, Hinrichs R, Rosenkranz S, Pfitzner T, et al. (2002) Myocardial fibrosis in transforming growth factor-beta(1) (TGF-beta(1)) transgenic mice is associated with inhibition of interstitial collagenase. Eur J Clin Invest 32: 295-303.
45. Brooks WW, Conrad CH, (2000) Myocardial fibrosis in transforming growth factor beta(1)heterozygous mice. J Mol Cell Cardiol 32: 187-195.
46. Villarreal FJ, Dillmann WH, (1992) Cardiac hypertrophy-induced changes in mRNA levels for TGF-beta 1, fibronectin, and collagen. Am J Physiol 262: H1861-1866.
47. Villarreal FJ, Lee AA, Dillmann WH, Giordano FJ, (1996) Adenovirus-mediated overexpression of human transforming growth factor-beta 1 in rat cardiac fibroblasts, myocytes and smooth muscle cells. J Mol Cell Cardiol 28: 735-742.
48. Lorts A, Schwanekamp JA, Elrod JW, Sargent MA, Molkentin JD, (2009) Genetic manipulation of periostin expression in the heart does not affect myocyte content, cell cycle activity, or cardiac repair. Circ Res 104: e1-7.
49. Duisters RF, Tijsen AJ, Schroen B, Leenders JJ, Lentink V, et al. (2009) miR-133 and miR-30 regulate connective tissue growth factor: implications for a role of microRNAs in myocardial matrix remodeling. Circ Res 104: 170-178, 176p following 178.
50. Shanmugam P, Valente AJ, Prabhu SD, Venkatesan B, Yoshida T, et al. (2011) Angiotensin-II type 1 receptor and NOX2 mediate TCF/LEF and CREB dependent WISP1 induction and cardiomyocyte hypertrophy. J Mol Cell Cardiol 50: 928-938.
51. Katsuragi N, Morishita R, Nakamura N, Ochiai T, Taniyama Y, et al. (2004) Periostin as a novel factor responsible for ventricular dilation. Circulation 110: 1806-1813.
52. Kuhn B, del Monte F, Hajjar RJ, Chang YS, Lebeche D, et al. (2007) Periostin induces proliferation of differentiated cardiomyocytes and promotes cardiac repair. Nat Med 13: 962-969.
53. Muthuchamy M, Grupp IL, Grupp G, O'Toole BA, Kier AB, et al. (1995) Molecular and physiological effects of overexpressing striated muscle beta-tropomyosin in the adult murine heart. J Biol Chem 270: 30593-30603.
54. Otey CA, Rachlin A, Moza M, Arneman D, Carpen O, (2005) The palladin/myotilin/myopalladin family of actin-associated scaffolds. Int Rev Cytol 246: 31-58.
55. Flashman E, Redwood C, Moolman-Smook J, Watkins H, (2004) Cardiac myosin binding protein C: its role in physiology and disease. Circ Res 94: 1279-1289.
56. Ferrari MB, Podugu S, Eskew JD, (2006) Assembling the myofibril: coordinating contractile cable construction with calcium. Cell Biochem Biophys 45: 317-337.
57. Aoki H, Sadoshima J, Izumo S, (2000) Myosin light chain kinase mediates sarcomere organization during cardiac hypertrophy in vitro. Nat Med 6: 183-188.
58. Chien KR, Zhu H, Knowlton KU, Miller-Hance W, van-Bilsen M, et al. (1993) Transcriptional regulation during cardiac growth and development. Annu Rev Physiol 55: 77-95.
59. Fleischmann A, Hafezi F, Elliott C, Reme CE, Ruther U, et al. (2000) Fra-1 replaces c-Fos-dependent functions in mice. Genes Dev 14: 2695-2700.
60. Sadoshima J, Montagne O, Wang Q, Yang G, Warden J, et al. (2002) The MEKK1-JNK pathway plays a protective role in pressure overload but does not mediate cardiac hypertrophy. J Clin Invest 110: 271-279.
61. Shimazaki M, Nakamura K, Kii I, Kashima T, Amizuka N, et al. (2008) Periostin is essential for cardiac healing after acute myocardial infarction. J Exp Med 205: 295-303.
62. Wisdom R, Johnson RS, Moore C, (1999) c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J 18: 188-197.
63. Eferl R, Sibilia M, Hilberg F, Fuchsbichler A, Kufferath I, et al. (1999) Functions of c-Jun in liver and heart development. J Cell Biol 145: 1049-1061.
64. Shaulian E, Karin M, (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4: E131-136.
65. Fujita T, Ishikawa Y, (2011) Apoptosis in heart failure.-The role of the beta-adrenergic receptor-mediated signaling pathway and p53-mediated signaling pathway in the apoptosis of cardiomyocytes. Circ J 75: 1811-1818.
66. Gravning J, Orn S, Kaasboll OJ, Martinov VN, Manhenke C, et al. (2012) Myocardial connective tissue growth factor (CCN2/CTGF) attenuates left ventricular remodeling after myocardial infarction. PLoS One 7: e52120.
67. Ahmed MS, Gravning J, Martinov VN, von Lueder TG, Edvardsen T, et al. (2011) Mechanisms of novel cardioprotective functions of CCN2/CTGF in myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 300: H1291-1302.
68. Moe IT, Pham TA, Hagelin EM, Ahmed MS, Attramadal H, (2013) CCN2 exerts direct cytoprotective actions in adult cardiac myocytes by activation of the PI3-kinase/Akt/GSK-3beta signaling pathway. J Cell Commun Signal 7: 31-47.
69. Venkatesan B, Prabhu SD, Venkatachalam K, Mummidi S, Valente AJ, et al. (2010) WNT1-inducible signaling pathway protein-1 activates diverse cell survival pathways and blocks doxorubicin-induced cardiomyocyte death. Cell Signal 22: 809-820.
70. Su F, Overholtzer M, Besser D, Levine AJ, (2002) WISP-1 attenuates p53-mediated apoptosis in response to DNA damage through activation of the Akt kinase. Genes Dev 16: 46-57.
71. Li B, Wang L, Chi B, (2013) Upregulation of periostin prevents P53-mediated apoptosis in SGC-7901 gastric cancer cells. Mol Biol Rep 40: 1677-1683.