Modification of protein by disulfide S-monoxide and disulfide S-dioxide: distinctive effects on PKC

Biochemistry. 2007 Feb 20;46(7):1961-71. doi: 10.1021/bi061955i. Epub 2007 Jan 24.

Abstract

Disulfide S-monoxide (DSMO) and disulfide S-dioxide (DSDO) have been proposed as proximal mediators for the oxidant-mediated modification of proteins. These disulfide S-oxides (DSOs) derived from glutathione (GSH) and captopril (CPSH) were synthesized by iron- or methyltrioxorhenium (VII)-catalyzed oxidation of the thiols with H2O2. Treatment of mouse hippocampal extracts with [35S]GS-DSOs revealed that a large number of proteins were susceptible to thionylation; however, only a limited number of the them were detectable by the commonly used antibody against GS-associated proteins. Using protein kinase C (PKC) as a model, we found that DSOs derived from different thiols modified this kinase with different efficacy and specificity; for example, the inhibitory potency of the kinase was glutathione disulfide S-dioxide (GS-DSDO) (IC50, approximately 30 microM) > captopril disulfide S-dioxide (CPS-DSDO) (IC50, approximately 450 microM) > glutathione disulfide S-monoxide (GS-DSMO) and captopril disulfide S-monoxide (CPS-DSMO). The stoichiometries of thionylation of PKC beta mediated by [35S]GS-DSMO and [35S]GS-DSDO were approximately 1 and 5 mol/mol, respectively, and at least four glutathionylation sites were identified in the GS-DSDO-treated kinase. Modification of PKC by GS-DSDO and CPS-DSDO rendered the kinase very susceptible to limited proteolysis; the former preferentially caused the degradation of the catalytic and the latter the regulatory domain of the kinase. Furthermore, CPS-DSDO-mediated modification of PKC increased the autonomous kinase activity; this was not the case for GS-DSDO-mediated modification. Since DSOs of different oxidative states as well as those derived from different thiols exert different effects on a target protein, these molecules could cause distinct cellular responses if derived from endogenous cellular reactions or even if they arise from exogenous sources.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Angiotensin-Converting Enzyme Inhibitors / chemistry
  • Animals
  • Captopril / chemistry
  • Catalysis
  • Disulfides / chemical synthesis
  • Disulfides / metabolism
  • Disulfides / pharmacology*
  • Ferric Compounds
  • Glutathione / chemistry
  • Hippocampus / metabolism
  • Hydrogen Peroxide / chemistry
  • Hydrolysis
  • In Vitro Techniques
  • Mice
  • Organometallic Compounds
  • Oxidation-Reduction
  • Protein Kinase C / metabolism*
  • Protein Kinase C beta
  • Structure-Activity Relationship
  • Sulfones / chemical synthesis
  • Sulfones / metabolism
  • Sulfones / pharmacology*
  • Tissue Extracts / metabolism

Substances

  • Angiotensin-Converting Enzyme Inhibitors
  • Disulfides
  • Ferric Compounds
  • Organometallic Compounds
  • Sulfones
  • Tissue Extracts
  • methyltrioxorhenium VII
  • Captopril
  • Hydrogen Peroxide
  • Protein Kinase C
  • Protein Kinase C beta
  • Glutathione