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Originally published In Press as doi:10.1074/jbc.M011766200 on February 27, 2001

J. Biol. Chem., Vol. 276, Issue 19, 16045-16050, May 11, 2001
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c-Jun N-terminal Kinase Activation by Hydrogen Peroxide in Endothelial Cells Involves Src-dependent Epidermal Growth Factor Receptor Transactivation*

Kai Chen, Joseph A. VitaDagger , Bradford C. Berk§, and John F. Keaney Jr.Dagger

From the Evans Memorial Department of Medicine and Whitaker Cardiovascular Institute, Boston University School of Medicine, Boston, Massachusetts 02118 and the § Center for Cardiovascular Research, University of Rochester Medical Center, Rochester, New York 14642

The phenotypic properties of the endothelium are subject to modulation by oxidative stress, and the c-Jun N-terminal kinase (JNK) pathway is important in mediating cellular responses to stress, although activation of this pathway in endothelial cells has not been fully characterized. Therefore, we exposed endothelial cells to hydrogen peroxide (H2O2) and observed rapid activation of JNK within 15 min that involved phosphorylation of JNK and c-Jun and induction of AP-1 DNA binding activity. Inhibition of protein kinase C and phosphoinositide 3-kinase did not effect JNK activation. In contrast, the tyrosine kinase inhibitors, genistein, herbimycin A, and 4-amino-5-(4-chlorophenyl)-7-(t-butyl)pyrazolo[3,4-D]pyrimidine (PP2) significantly attenuated H2O2-induced JNK activation as did endothelial cell adenoviral transfection with a dominant-negative form of Src, implicating Src as an upstream activator of JNK. Activation of JNK by H2O2 was also inhibited by AG1478 and antisense oligonucleotides directed against the epidermal growth factor receptor (EGFR), implicating the EGFR in this process. Consistent with this observation, H2O2 stimulated EGFR tyrosine phosphorylation and complex formation with Shc-Grb2 that was abolished by PP2, implicating Src in H2O2-induced EGFR activation. Tyrosine phosphorylation of the EGFR by H2O2 did not involve receptor autophosphorylation at Tyr1173 as assessed by an autophosphorylation-specific antibody. These data indicate that H2O2-induced JNK activation in endothelial cells involves the EGFR through an Src-dependent pathway that is distinct from EGFR ligand activation. These data represent one potential pathway for mediating oxidative stress-induced phenotypic changes in the endothelium.

* This work was supported by National Institute of Health Grants HL53398 and HL52936 (to J. A. V.); HL49192 and HL18645 (to B. C. B.); and HL59346, HL55854, and DK55656 (to J. F. K).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger Established Investigator of the American Heart Association.

To whom correspondence should be addressed: Boston University School of Medicine, Whitaker Cardiovascular Institute, 715 Albany St., Rm. W507, Boston, MA 02118. Tel.: 617-638-4894; Fax: 617-638-5437; E-mail: jkeaney@bu.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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