Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling

Journal of Clinical Investigation

Volumn 111, Issue 10, 2003, Pages 1475-1486

  Braz, Julian C ^a,b   Bueno, Orlando F ^a   Liang, Qiangrong ^a   Wilkins, Benjamin J ^a   Dai, Yan Shan ^a   Parsons, Stephanie ^a   Braunwart, Joseph ^a   Glascock, Berry J ^a   Klevitsky, Raisa ^a   Kimball, Thomas F ^a   Hewett, Timothy E ^a   Molkentin, Jeffery D ^a,c  

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

^b UNIVERSITY OF CINCINNATI   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN; CALCINEURIN; ISOPRENALINE; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 6; MITOGEN ACTIVATED PROTEIN KINASE P38; MUTANT PROTEIN; NUCLEAR FACTOR; PHENYLEPHRINE; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; MAP2K3 PROTEIN, MOUSE; MAP2K6 PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NUCLEAR PROTEIN; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CONTROLLED STUDY; ENZYME INHIBITION; EUKARYOTIC CELL; GENE DISRUPTION; GENE REPRESSION; GENETIC TRANSCRIPTION; HYPERTROPHIC CARDIOMYOPATHY; MAMMAL; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; SIGNAL TRANSDUCTION; STRESS; T LYMPHOCYTE ACTIVATION; TRANSGENE; TRANSGENIC MOUSE; ANIMAL; CELL CULTURE; CYTOLOGY; DISEASE COURSE; DOMINANT GENE; DRUG ANTAGONISM; GENE TARGETING; GENETICS; HEART MUSCLE CELL; IN VITRO STUDY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; UPREGULATION;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCINEURIN; CARDIOMYOPATHY, HYPERTROPHIC; CELLS, CULTURED; DISEASE PROGRESSION; DNA-BINDING PROTEINS; GENE TARGETING; GENES, DOMINANT; GENES, REPORTER; MAP KINASE KINASE 3; MAP KINASE KINASE 6; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 14; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; MYOCYTES, CARDIAC; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PROTEIN-TYROSINE KINASES; RATS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSGENES; UP-REGULATION;

EID: 0038651918     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200317295     Document Type: Article

References (45)

1. Lorell, B.H., and Carabello, B.A. 2000. Left ventricular hypertrophy: pathogenesis, detection, and prognosis. Circulation. 102:470-479.
2. Ho, K.K., Levy, D., Kannel, W.B., and Pinsky, J.L. 1993. The epidemiology of heart failure: The Framingham Study. J. Am. Coll. Cardiol. 22:6-13.
3. Levy, D., Garrison, R.J., Savage, D.D., Kannel, W.B., and Castelli, W.P. 1990. Prognostic implications of echocardiographically determined left ventricular mass in the Framingham heart study. N. Engl. J. Med. 322:1561-1566.
4. van Zwieten, P.A. 2000. The influence of antihypertensive drug treatment on the prevention and regression of left ventricular hypertrophy. Cardiovasc. Res. 45:82-91.
5. Molkentin, J.D., and Dorn, G.W. 2001. Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu. Rev. Physiol. 63:391-426.
6. Sugden, P.H., and Clerk, A. 1998. "Stress-responsive" mitogen-activated protein kinases (c-Jun N-terminal kinases and p38 mitogen-activated protein kinases) in the myocardium. Circ. Res. 24:345-352.
7. Nemoto, S., Sheng, S., and Lin, A. 1998. Opposing effects of Jun kinase and p38 mitogen-activated protein kinases on cardiomyocyte hypertrophy. Mol. Cell. Biol. 18:3518-3526.
8. Zechner, D., Thuerauf, D.J., Hanford, D.J., McDonough, P.M., and Glembotski, C.C. 1997. A role for the p38 mitogen-activated protein kinase pathway in myocardial cell growth, sarcomeric organization, and cardiac-specific gene expression. J. Cell. Biol. 139:115-127.
9. Wang, Y., et al. 1998. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J. Biol. Chem. 273:2161-2168.
10. Liang, F., Lu, S., and Gardner, D.G. 2000. Endothelin-dependent and -independent components of strain-activated brain natriuretic peptide gene transcription require extracellular signal regulated kinase and p38 mitogen-activated protein kinase. Hypertension. 35:188-192.
11. Liang, F., and Gardner, D.G. 1999. Mechanical strain activates BNP gene transcription through a p38/NF-kappaB-dependent mechanism. J. Clin. Invest. 104:1603-1612.
12. Choukroun, G., et al. 1998. Role of the stress-activated protein kinases in endothelin-induced cardiomyocyte hypertrophy. J. Clin. Invest. 102:1311-1320.
13. Clerk, A., Michael, A., and Sugden, P.H. 1998. Stimulation of the p38 mitogen-activated protein kinase pathway in neonatal rat ventricular myocytes by the G protein-coupled receptor agonists, endothelin-1 and phenylephrine: a role in cardiac myocyte hypertrophy? J. Cell. Biol. 142:523-535.
14. Ng, D.C., Long, C.S., and Bogoyevitch, M.A. 2000. A role for the extracellular signal-regulated kinase and p38 mitogen-activated protein kinases in interleukin-1 beta-stimulated delayed signal tranducer and activator of transcription 3 activation, atrial natriuretic factor expression, and cardiac myocyte morphology. J. Biol. Chem. 276:29490-29498.
15. Liao, P., 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.
16. Bueno, O.F., Brandt, E.B., Rothenberg, M.E., and Molkentin, J.D. 2002. Defective T cell development and function in calcineurin A beta-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 99:9398-9403
17. Bueno, O.F., et al. 2002. Impaired cardiac hypertrophic response in Calcineurin Abeta-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 99:4586-4591.
18. Gulick, J., et al. 1997. Transgenic remodeling of the regulatory myosin light chains in the mammalian heart. Circ. Res. 80:655-664.
19. Taigen, T., De Windt, L.J., Lim, H.W., and Molkentin, J.D. 2000. Targeted inhibition of calcineurin prevents agonist-induced cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 97:1196-1201.
20. 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.
21. Hunton, D.L., et al. 2002. Capacitative calcium entry contributes to NFAT nuclear translocation and hypertrophy in cardiomyocytes. J. Biol. Chem. 277:14266-14273.
22. Liu, Y., Cseresnyes, Z., Randall, W.R., and Schneider, M.F. 2001. Activity-dependent nuclear translocation and intranuclear distribution of NFATc in adult skeletal muscle fibers. J. Cell Biol. 155:27-39.
23. Lim, H.W., et al. 2000. Calcineurin expression, activation, and function in cardiac pressure-overload hypertrophy. Circulation. 101:2431-2437.
24. Jones, W.K., et al. 1996. Ablation of the murine α myosin heavy, chain gene leads to dosage effects and functional deficits in the heart. J. Clin. Invest. 98:1906-1917.
25. Raingeaud, J., Whitmarsh, A.J., Barrett, T., Derijard, B., and Davis, R.J. 1996. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell. Biol. 16:1247-1255.
26. 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.
27. 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.
28. 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.
29. Molkentin, J.D., et al. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 93:215-228.
30. Enslen, H., Raingeaud, J., and Davis, R.J. 1998. Selective activation of p38 mitogen-activated protein (MAP) kinase isoforms by the MAP kinase kinases MKK3 and MKK6. J. Biol. Chem. 273:1741-1748.
31. 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.
32. Adams, R.H., et al. 2000. Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol. Cell. 6:109-116.
33. Mudgett, J.S., et al. 2000. Essential role for p38alpha mitogen-activated protein kinase in placental angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 97:10454-10459.
34. Jiang, Y., et al. 1997. Characterization of the structure and function of the fourth member of p38 group mitogen-activated protein kinases, p38delta. J. Biol. Chem. 272:30122-30128.
35. Zanke, B.W., et al. 1996. Mammalian mitogen-activated protein kinase pathways are regulated through formation of specific kinase-activator complexes. J. Biol. Chem. 271:29876-29881.
36. Court, N.W., dos Remedios, C.G., Cordell, J., and Bogoyevitch, M.A. 2002. Cardiac expression and subcellular localization of the p38 mitogen-activated protein kinase member, stress-activated protein kinase-3 (SAPK3). J. Mol. Cell. Cardiol. 34:413-426.
37. Kumar, S., et al. 1997. Novel homologues of CSBP/p38 MAP kinase: activation, substrate specificity and sensitivity to inhibition by pyridinyl imidazoles. Biochem. Biophys. Res. Commun. 235:533-538.
38. Lemke, L.E., et al. 2001. Decreased p38 MAPK activity in end-stage failing human myocardium: p38 MAPK alpha is the predominant isoform expressed in human heart. J. Mol. Cell. Cardiol. 33:1527-1540.
39. Huang, W.Y., Aramburu, J., Douglas, P.S., and Izumo, S. 2000. Transgenic expression of green fluorescence protein can cause dilated cardiomyopathy. Nat. Med. 6:482-483.
40. Antos, C.L., et al. 2002. Activated glycogen synthase-3 beta suppresses cardiac hypertrophy in vivo. Proc. Natl. Acad. Sci. U. S. A. 99:907-912.
41. Wilkins, B.J., et al. 2002. Targeted disruption of NFATc3, but not NFATc4 reveals an intrinsic defect in calcineurin-mediated cardiac hypertrophic growth. Mol. Cell. Biol. 22:7603-7613
42. Zhang, D., et al. 2000. TAK1 is activated in the myocardium after pressure overload and is sufficient to provoke heart failure in transgenic mice. Nat. Med. 6:556-563.
43. Bueno, O.F., et al. 2001. The dual-specificity phosphatase MKP-1 limits the cardiac hypertrophic response in vitro and in vivo. Circ. Res. 88:88-96.
44. Wang, C., et al. 2001. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature. 412:346-351.
45. Purcell, N.H., et al. 2001. Activation of NFkappa B is required for hypertrophic growth of primary rat neonatal ventricular cardiomyocytes. Proc. Natl. Acad. Sci. U. S. A. 98:6668-6673.