S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells

J Biol Chem. 2004 Jul 9;279(28):29857-62. doi: 10.1074/jbc.M313320200. Epub 2004 Apr 27.

Abstract

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 Cys(118) 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 p47(phox), or glutaredoxin-1 decreased GSS-Ras, Ras activation, p38, and Akt phosphorylation and the induction of protein synthesis by AII. Furthermore, expression of a Cys(118) mutant Ras decreased AII-mediated p38 and Akt phosphorylation as well as protein synthesis. These results show that H(2)O(2) from NAD(P)H oxidase forms GSS-Ras on Cys(118) 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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Angiotensin II / metabolism*
  • Animals
  • Cells, Cultured
  • Enzyme Activation
  • ErbB Receptors / metabolism
  • Glutaredoxins
  • Glutathione / chemistry
  • Glutathione / metabolism*
  • Humans
  • Hydrogen Peroxide / metabolism
  • Mitogen-Activated Protein Kinases / metabolism
  • Muscle, Smooth, Vascular / cytology*
  • Myocytes, Smooth Muscle / cytology
  • Myocytes, Smooth Muscle / metabolism*
  • NADH, NADPH Oxidoreductases / metabolism
  • NADPH Oxidases
  • Oxidants / metabolism
  • Oxidation-Reduction
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Rats
  • Reactive Oxygen Species / metabolism
  • Signal Transduction / physiology*
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • p38 Mitogen-Activated Protein Kinases
  • ras Proteins / chemistry
  • ras Proteins / genetics
  • ras Proteins / metabolism*

Substances

  • Glrx protein, rat
  • Glrx2 protein, rat
  • Glutaredoxins
  • Oxidants
  • Proto-Oncogene Proteins
  • Reactive Oxygen Species
  • Angiotensin II
  • Hydrogen Peroxide
  • Oxidoreductases
  • NADH, NADPH Oxidoreductases
  • NADPH Oxidases
  • ErbB Receptors
  • AKT1 protein, human
  • Akt1 protein, rat
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • ras Proteins
  • Glutathione