Reduction of phenoxyl radicals by thioredoxin results in selective oxidation of its SH-groups to disulfides. An antioxidant function of thioredoxin

Biochemistry. 1995 Apr 11;34(14):4765-72. doi: 10.1021/bi00014a034.

Abstract

Thioredoxin is an important cellular redox buffer. In this report, we describe the reaction of thioredoxin with phenoxyl radicals. The vicinal sulfhydryls of the bis(cysteinyl) active site sequence reduced phenoxyl radicals released in horseradish peroxidase-catalyzed oxidation of phenol. Redox cycling of phenol was accompanied by selective oxidation of thioredoxin sulfhydryls to disulfides. HPLC/UV-vis measurements showed that the SH:phenol oxidation ratio was 15:1 under the conditions used. At the end of the reaction, oxidized thioredoxin was quantitatively recovered in the reduced form with dithiothreitol. Oxidation of sulfhydryls to sulfoxy derivatives, oxidation of other amino acid residues, and formation of covalent adducts with phenolic metabolites (quinones) were not detected by LC-MS. While the thiyl radical of glutathione was readily detected with the spin trap 5,5-dimethyl-1-pyrroline N-oxide, no ESR-detectable DMPO-thiyl adducts formed during the oxidation of thioredoxin. Similarly, oxidation of vicinal sulfhydryls of dihydrolipoic acid did not produce DMPO-thiyl spin adducts, indicating that fast intramolecular cyclization to disulfide occurred with thioredoxin. Measurements of the superoxide dismutase-sensitive chemiluminescence response of lucigenin demonstrated that thioredoxin oxidation was accompanied by release of superoxide, most likely via disulfide radical anion-mediated one-electron reduction of oxygen. We propose that formation of disulfides is characteristic of the phenoxyl radical-catalyzed oxidation of vicinal sulfhydryls in both small thiols and disulfide-forming oxidoreductases. Reversibility of the phenoxyl radical-catalyzed modification of thioredoxin may be responsible for its function as an efficient cytosolic antioxidant.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acridines
  • Antioxidants / chemistry*
  • Catalysis
  • Cyclic N-Oxides
  • Disulfides / chemistry*
  • Electron Spin Resonance Spectroscopy
  • Escherichia coli / chemistry
  • Free Radicals
  • Mass Spectrometry
  • Oxidation-Reduction
  • Phenols / chemistry*
  • Spin Labels
  • Sulfhydryl Compounds / chemistry*
  • Superoxides / analysis
  • Thioredoxins / chemistry*

Substances

  • Acridines
  • Antioxidants
  • Cyclic N-Oxides
  • Disulfides
  • Free Radicals
  • Phenols
  • Spin Labels
  • Sulfhydryl Compounds
  • Superoxides
  • 10,10'-dimethyl-9,9'-biacridinium
  • phenoxy radical
  • Thioredoxins
  • 5,5-dimethyl-1-pyrroline-1-oxide