Nitroxides scavenge myeloperoxidase-catalyzed thiyl radicals in model systems and in cells

J Am Chem Soc. 2004 Aug 4;126(30):9221-32. doi: 10.1021/ja0495157.

Abstract

Nitroxide radicals possess important antioxidant activity in live tissues because of their ability to scavenge reactive radicals. Despite the fact that, in cells, damaging free radicals are primarily quenched by glutathione (GSH) with subsequent formation of harmful glutathionyl radical (GS(*)), interactions of nitroxide radicals with GS(*) and thiols have not been studied in detail. In addition, intracellular metabolic pathways leading to the formation of secondary amines from nitroxides are unknown. Here we report that GS(*) radicals react efficiently and irreversibly with nitroxides to produce secondary amines. We developed a sensitive method for the detection of GS(*) based on their specific interaction with Ac-Tempo, a nonfluorescent conjugate of fluorogenic acridine with paramagnetic nitroxide Tempo, and used it to characterize interactions between nitroxide and thiyl radicals generated through phenoxyl radical recycling by peroxidase. During reaction of Ac-Tempo with GS(*), Tempo EPR signals decayed and acridine fluorescence concurrently increased. DMPO and PBN, spin traps for GS(*), inhibited this interaction. Using combined HPLC and mass spectrometry, we determined that 90% of the Ac-Tempo was converted into fluorescent acridine (Ac)-piperidine; GSH was primarily oxidized into sulfonic acid. In myeloperoxidase-rich HL-60 cells, Ac-piperidine fluorescence was observed upon stimulation of GS(*) generation by H(2)O(2) and phenol. Development of fluorescence was prevented by preincubation of cells with the thiol-blocking reagent N-ethylmaleimide as well as with peroxidase inhibitiors. Furthermore, Ac-Tempo preserved intracellular GSH and protected cells from phenol/GS(*) toxicity, suggesting a new mechanism for the free-radical scavenging activity of nitroxides in live cells.

Publication types

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

MeSH terms

  • Acridines / chemistry
  • Amines / chemistry
  • Amines / metabolism
  • Catalysis
  • Cyclic N-Oxides / chemistry
  • Cysteine / chemistry
  • Cysteine / metabolism
  • Electron Spin Resonance Spectroscopy
  • Free Radical Scavengers / chemistry
  • Free Radical Scavengers / metabolism
  • Free Radicals / chemistry
  • Free Radicals / metabolism
  • Glutathione / chemistry
  • Glutathione / metabolism*
  • HeLa Cells
  • Horseradish Peroxidase / chemistry
  • Horseradish Peroxidase / metabolism
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Nitrogen Oxides / chemistry
  • Nitrogen Oxides / metabolism*
  • Peroxidase / chemistry
  • Peroxidase / metabolism*
  • Spin Labels

Substances

  • Acridines
  • Amines
  • Cyclic N-Oxides
  • Free Radical Scavengers
  • Free Radicals
  • Nitrogen Oxides
  • Spin Labels
  • Hydrogen Peroxide
  • Horseradish Peroxidase
  • Peroxidase
  • Glutathione
  • nitroxyl
  • Cysteine
  • TEMPO