c-Jun N-terminal kinases (JNK) antagonize cardiac growth through cross-talk with calcineurin-NFAT signaling

EMBO Journal

Volumn 22, Issue 19, 2003, Pages 5079-5089

  Liang, Qiangrong ^a   Bueno, Orlando F ^a   Wilkins, Benjamin J ^a   Kuan, Chia Yi ^a   Xia, Ying ^a   Molkentin, Jeffery D ^a  

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

Author keywords

Calcineurin; Cardiac growth; Cross talk; JNK signaling; NFAT

Indexed keywords

CALCINEURIN; HYBRID PROTEIN; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

AGING; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CONTROLLED STUDY; EUKARYOTIC CELL; GENE TARGETING; HEART DEVELOPMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRESS;

ANIMALS; CALCINEURIN; DNA-BINDING PROTEINS; GENE TARGETING; HEART; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 7; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ANIMALIA; EUKARYOTA; MUS MUSCULUS;

EID: 0141642015     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg474     Document Type: Article

References (48)

1. Antos, C.L., McKinsey, T.A., Frey, N., Kutschke, W., McAnally, J., Shelton, J.M. Richardson, J.A. Hill, J.A. and Olson, E.N. (2002). Activated glycogen synthase-3 beta suppresses cardiac hypertrophy in vivo. Proc. Natl Acad. Sci. USA, 99, 907-912.
2. Braz, J.C., Bueno, O.F., Liang, Q., Wilkins, B.J., Dai, Y.-S., Braunwart, J., Glascock, B.J., Klevitsky, R., Kimball, T.F. et al. (2003). Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling, J. Clin. Invest., 111, 1475-1486
3. Bueno, O.F., Brandt, E.B., Rothenberg, M.E. and Molkentin, J.D. (2002a). Defective T cell development and function in Calcineurin A-deficient mice. Proc. Natl Acad. Sci. USA, 99, 9398-9403.
4. Bueno, O.F., Wilkins, B.J., Tymitz, K.M., Glascock, B.J., Kimball, T.F., Lorenz, J.N. and Molkentin, J.D. (2002b). Impaired cardiac hypertrophic response in Calcineurin A beta-deficient mice. Proc. Natl Acad. Sci, USA, 99, 4586-4591.
5. Choukroun, G., Hajjar, R., Kyriakis, J.M., Bonventre, J.V., Rosenzweig, A. and Force, T. (1998). Role of the stress-activated protein kinases in endothelin-induced cardiomyocyte hypertrophy. J. Clin. Invest., 102, 1311-1320.
6. 2terminal kinases. J. Clin. Invest., 104, 391-398.
7. Chow, C.W., Rincon, M., Cavanagh, J., Dickens, M. and Davis, R.J. (1997). Nuclear accumulation of NFAT4 opposed by the JNK signal transduction pathway. Science, 278, 1638-1641.
8. Claycomb, W.C. (1977). Cardiac-muscle hypertrophy. Differentiation and growth of the heart cell during development. Biochem. J., 168, 599-601.
9. 2+, calcineurin and NF-AT, Cell, 96, 611-614.
10. Crabtree, G.R. and Olson, E.N. (2002). NFAT signaling: choreographing the social lives of cells. Cell, 109, S67-S79.
11. Davis, R.J. (2000). Signal transduction by the JNK group of MAP kinases. Cell, 103, 239-252.
12. De Windt, L.J., Lim, H.W., Haq, S., Force, T. and Molkentin, J.D. (2000) 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., 275, 13571-13579.
13. Downward, J. and Goff, S.P. (2002). Update on the big C: complexity and cross-talk between pathways. Curr. Opin. Genet. Dev., 12, 11-13.
14. Esposito, G., Prasad, S.V., Rapacciulo, A., Mao, L., Koch, W.J. and Rockman, H.A. (2001). Cardiac overexpression of G(q) inhibitor blocks induction of extracellular signal-regulated kinase and c-Jun NH(2)-terminal kinase activity in in vivo pressure overload. Circulation, 103, 1453-1458.
15. Fleming, Y., Armstrong, C.G., Morrice, N., Paterson, A., Goedert, M. and Cohen, P. (2000). Synergistic activation of stress-activated protein kingsel/ JNK isoforms by MAPKs MKK4 and MKK7 Biochem. J., 352, 145-154.
16. Garrington, T.P and Johnson, G.L. (1999). Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr. Opin. Cell. Biol., 11, 211-218
17. Gomez del Arco, P, Martinez-Martinez, S., Maldonado, J.L., Ortega-Perez, I. and Redondo, J.M. (2000). A role for the p38 MAP kinase pathway in the nuclear shuttling of NFATp. J. Biol. Chem., 275, 13872-13878.
18. 2+/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell, 105, 863-875.
19. Gupta, S., Campbell, D., Derijard,B. and Davis, R.J. (1995) Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science, 267, 389-393.
20. Gupta, S., Barrett, T., Whitmarsh, A.J., Cavanagh, J., Sluss, H.K., Derijard, B. and Davis, R.J. (1996). Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J., 15, 2760-2770.
21. He, H., Li, H.L., Lin, A. and Gottlieb, R.A. (1999). Activation of the JNK pathway is important for cardiomyocyte death in response to simulated ischemia. Cell Death Differ., 6, 987-991.
22. Hunton, D.L., Lucchesi, P.A., Pang, Y., Cheng, X., Dell'Italia, L.J. and Marchase, R.B. (2002). Capacitative calcium entry contributes to NFAT nuclear translocation and hypertrophy in cardiomyocytes. J. Biol. Chem., 277, 14266-14273
23. Ito, M., Yoshioka, K., Akechi, M., Yamashita, S., Takamatsu, N., Sugiyama, K., Hibi, M., Nakabeppu, Y., Shiba, T. et al. (1999). JSAP1, a novel jun N-terminal protein kinase (JNK)-binding protein that functions as a Scaffold factor in the JNK signaling pathway. Mol. Cell. Biol., 19, 7539-7548.
24. Karandikar, M., Xu, S. and Cobb, M.H. (2000). MEKK1 binds raf-1 and the ERK2 cascade components. J. Biol. Chem., 275, 40120-40127.
25. Kuan, C-Y., Yang, D.D., Samanta-Roy, D.R., Davis, R.J., Rakic, P. and Flavell, R.A. (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron, 22, 667-676.
26. Kyriakis, J.M. and Avruch, J. (1996). Sounding the alarm: protein kinase cascades activated by stress and inflammation. J. Biol. Chem., 271, 24313-24316.
27. Lei, K., Nimnual, A., Zong, W.X., Kennedy, N.J., Flavell, R.A., Thompson, C.B., Bar-Sagi, D. and Davis, R.J. (2002). The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by C-Jun NH2-terminal kinase. Mol. Cell. Biol., 22, 4929-4942.
28. Liang, Q., Wiese, R.J., Bueno, O.F., Dai, Y.S., Markham, B.E. and Molkentin, J.D. (2001). The transcription factor gata4 is activated by extracellular signal-regulated kinase 1 - and 2-mediated phosphorylation of serine 105 in cardiomyocytes. Mol. Cell. Biol., 21, 7460-7469.
29. Liao, P., Georgakopoulos, D., Kovacs, A., Zheng, M., Lerner, D., Pu, H., Saffitz, J., Chien, K., Xiao, R.P. et al. (2001). The in vivo role of p38 MAP kinases in cardiac remodeling and restrictive cardiomyopathy. Proc. Natl Acad. Sci. USA, 98, 12283-12288.
30. Lorell, B.H. and Carabello, B.A. (2000). Left ventricular hypertrophy: pathogenesis, detection and prognosis. Circulation, 102, 470-479.
31. Lu, Z., Xu, S., Joaseiro, C., Cobb, M.H. and Hunter, T. (2002). The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitination and degradation of ERK1/2. Mol. Cell., 9, 945-956.
32. Minamino, T., Yujiri, T., Terada, N., Taffet, G.E., Michael, L.H., Johnson, G.L. and Schneider, M.D. (2002). MEKKI is essential for cardiac hypertrophy and dysfunction induced by Gq. Proc. Natl Acad. Sci. USA, 99, 3866-3871.
33. Molkentin, J.D., Lu, R.J., Antos, C.L., Markham, B.E., Richardson, J., Robbins, J., Grant, S.R. and Olson, E.N. (1998). A calcineur-independent transcriptional pathway for cardiac hypertrophy. Cell, 93, 215-228.
34. Muda, M., Theodosiou, A., Rodrigues, N., Boschert, U., Camps, M., Gillieron, C., Davies, K., Ashworth, A. and Arkinstall, S. (1996). The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases. J. Biol. Chem., 271, 27205-27208.
35. Nicol, R.L., Frey, N., Pearson, G., Cobb, M., Richardson, J. and Olson, E.N. (2001). Activated MEK5 induces serial assembly of sarcomeres and eccentric cardiac hypertrophy. EMBO J., 20, 2757-2767.
36. Petrich, B.G., Gong, X., Lerner,D.L., Wang, X., Brown, J.H., Saffitz, J.E. and Wang, Y. (2002). C-Jun N-terminal kinase activation mediates downregulation of connexin43 in cardiomyocytes. Circ. Res., 91, 640-647.
37. Porter, C.M., Havens, M.A. and Clipstone, N.A. (2000). Identification of amino acid residues and protein kinases involved in the regulation of NFATc subcellular localization. J. Biol. Chem., 275, 3543-3551.
38. Ramirez, M.T., Sah, V.P., Zhao, X.L., Hunter, J.J., Chien, K.R. and Brown, J.H. (1997). The MEKK-JNK pathway is stimulated by alpha 1-adrenergic receptor and ras activation and is associated with in vitro and in vivo cardiac hypertrophy. J. Biol. Chem., 272, 14057-14061.
39. Sabapathy, K., Jochum, W., Hochedlinger, K., Chang, L., Karin, M. and Wagner, E.F. (1999). Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2. Mech. Dev., 89, 115-124.
40. Sadoshima, 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.
41. Schreiber, E., Matthias, P., Muller, M.M. and Schaffner, W. (1989). Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res., 17, 6419.
42. Wang, Y., Su, B., Sah, V.P., Brown, J.H., Han, J. and Chien, K.R. (1998). Cardiac hypertrophy induced by mitogen-activated protein kinase kinase 7, a specific activator for c-Jun NH2-terminal kinase in ventricular muscle cells. J. Biol. Chem., 273, 5423-5426.
43. Weston, C.R. and Davis, R.J. (2002). The JNK signal transduction pathway. Curr. Opin. Genet. Dev., 12, 14-21.
44. Whitmarsh, A.J. and Davis, R.J. (2001). Analyzing JNK and p38 mitogen-activated protein kinase activity. Methods Enzymol., 332, 319-336.
45. Wilkins, B.J. and Molkentin, J.D. (2002). Calcineurin and cardiac hypertrophy: where have we been? Where are we going? J. Physiol., 541, 1-8.
46. Wilkins, B.J., De Windt, L.J., Bueno, O.F., Braz, J.C., Glascock, B.J., Kimball, T.F. and Molkentin, J.D. (2002). Targeted disruption of NFATc3, but not NFATc4 reveals an intrinsic defect in calcineurin-mediated cardiac hypertrophic growth. Mol. Cell. Biol., 22, 7603-7613.
47. Yang, D.D., Kuan, C.-Y., Whitmarsh, A.J., Rincon, M., Zheng, T.S., Davis, R.J., Rakic, P. and Flavell, R.A. (1997). Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature, 389, 865-870.
48. Yang, T.T.C., Xiong, Q., Enslen, H., Davis, R.J. and Chow, C.-W. (2002). Phosphorylation of NFATc4 by p38 mitogen-activated protein kinases. Mol. Cell. Biol., 22, 3892-3904.