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J. Biol. Chem., Vol. 279, Issue 23, 24852-24860, June 4, 2004

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Mitogen-activated Protein Kinases p38 and ERK 1/2 Mediate the Wall Stress-induced Activation of GATA-4 Binding in Adult Heart^*

Olli Tenhunen, Balázs Sármán, Risto Kerkelä, István Szokodi¶, Lajos Papp¶, Miklós Tóth, and Heikki Ruskoaho||

From the Department of Pharmacology and Toxicology, Biocenter Oulu, University of Oulu, P. O. Box 5000, FIN-90014 University of Oulu, Finland, First Department of Medicine, Semmelweis Medical University and Molecular Genetic Research Group of the Hungarian Academy of Sciences, Budapest H-1083, Hungary, and the ^¶Heart Institute, Faculty of Medicine, University of Pécs, H-7624, Hungary

The zinc finger transcription factor GATA-4 has been implicated as a critical regulator of inducible cardiac gene expression and as a potential mediator of the hypertrophic program. However, the precise intracellular mechanisms that regulate the DNA-binding activity of GATA-4 are not fully understood. The aim of the present study was to examine the role of mitogen-activated protein kinases (p38 kinase, extracellular signal-regulated protein kinase, and c-Jun N-terminal protein kinase) in the left ventricular wall stress-induced activation of GATA-4 DNA binding in adult heart. Isolated perfused rat hearts were subjected to increased left ventricular wall stress by inflating a balloon in the ventricle. Gel mobility shift assays were used to analyze the transacting factors that interact with the GATA motifs of the B-type natriuretic peptide promoter. The left ventricular wall stress rapidly activated GATA-4 DNA binding and significantly increased the levels of phosphorylated p38 kinase, extracellular signal-regulated protein kinase, and c-Jun N-terminal protein kinase. The wall stress-induced increase in the DNA-binding activity of GATA-4 was abolished both in the presence of the p38 inhibitor SB239063 and MEK1/2 inhibitor U0126. In contrast, the inhibition of c-Jun N-terminal protein kinase by CEP11004had no effect on the baseline or stretch-induced GATA-4 DNA binding. Moreover, GATA-4 DNA binding was up-regulated by mechanical stretch in the isolated rat atria via p38 and extracellular signal-regulated protein kinase. In conclusion, the present study demonstrates that both p38 and extracellular signal-regulated protein kinase are required for the stretch-induced GATA-4 binding in intact heart.

Received for publication, December 31, 2003 , and in revised form, March 26, 2004.

^* This work was supported by grants from the Academy of Finland (to H. R.), the Sigrid Juselius Foundation (to H. R.), the Finnish Foundation for Cardiovascular Research (to H. R.), The National Technology Foundation TEKES (to H. R.), Aarne Koskelo Foundation (to O. T. and R. K.), the Finnish Medical Foundation (to O. T. and R. K.), and the Hungarian Scientific Research Found (OTKA: F035213, TO43403) (to I. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| To whom correspondence should be addressed. Tel.: 358-8-537-5236; Fax: 358-8-537-5247; E-mail: heikki.ruskoaho{at}oulu.fi.

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