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J. Biol. Chem., Vol. 279, Issue 28, 29857-29862, July 9, 2004
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From the
Vascular Biology Unit, the ¶Myocardial Biology Unit, and the **Diabetes and Metabolism Unit, Whitaker Cardiovascular Institute, Boston University Medical Center, Boston, Massachusetts 02118 and the ||Department of Surgery and Cancer Institute, Hillman Cancer Center, University of Pittsburg, Pittsburg, Pennsylvania 15260
Angiotensin II (AII) increases production of reactive oxygen species from NAD(P)H oxidase, a response that contributes to vascular hypertrophy. Here we show in cultured vascular smooth muscle cells that S-glutathiolation of the redox-sensitive Cys118 on the small GTPase, Ras, plays a critical role in AII-induced hypertrophic signaling. AII simultaneously increased the Ras activity and the S-glutathiolation of Ras (GSS-Ras) detected by biotin-labeled GSH or mass spectrometry. Both the increase in activity and GSS-Ras was labile under reducing conditions, suggesting the essential nature of this thiol modification to Ras activation. Overexpression of catalase, a dominant-negative p47phox, or glutaredoxin-1 decreased GSS-Ras, Ras activation, p38, and Akt phosphorylation and the induction of protein synthesis by AII. Furthermore, expression of a Cys118 mutant Ras decreased AII-mediated p38 and Akt phosphorylation as well as protein synthesis. These results show that H2O2 from NAD(P)H oxidase forms GSS-Ras on Cys118 and increases its activity leading to p38 and Akt phosphorylation, which contributes to the induction of protein synthesis. This study suggests that GSS-Ras is a redox-sensitive signaling switch that participates in the cellular response to AII.
Received for publication, December 5, 2003 , and in revised form, April 23, 2004.
* This work was supported by grants from the American Heart Association (to T. A. and D. R. P.), by National Institutes of Health Grant R01-HL55620, and by the University Cardiovascular Proteomics Center, which is funded by National Institutes of Health Contract HHSN268200248178C. 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.
The on-line version of this article (available at http://www.jbc.org) contains supplemental figures.
To whom correspondence should be addressed: Vascular Biology Unit, Boston University Medical Center X707, 650 Albany St., Boston, MA 02118-2393. Tel.: 617-638-7114; Fax: 617-638-7113; E-mail: tadachi{at}bumc.bu.edu.
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