Peroxidase- and nitrite-dependent metabolism of the anthracycline anticancer agents daunorubicin and doxorubicin

Biochemistry. 2001 Dec 18;40(50):15349-61. doi: 10.1021/bi011869c.

Abstract

Oxidation of the anticancer anthracyclines doxorubicin (DXR) and daunorubicin (DNR) by lactoperoxidase(LPO)/H(2)O(2) and horseradish peroxidase(HRP)/H(2)O(2) systems in the presence and absence of nitrite (NO(2)(-)) has been investigated using spectrophotometric and EPR techniques. We report that LPO/H(2)O(2)/NO(2)(-) causes rapid and irreversible loss of anthracyclines' absorption bands, suggesting oxidative degradation of their chromophores. Both the initial rate and the extent of oxidation are dependent on both NO(2)(-) concentration and pH. The initial rate decreases when the pH is changed from 7 to 5, and the reaction virtually stops at pH 5. Oxidation of a model hydroquinone compound, 2,5-di-tert-butylhydroquinone, by LPO/H(2)O(2) is also dependent on NO(2)(-); however, in contrast to DNR and DXR, this oxidation is most efficient at pH 5, indicating that LPO/H(2)O(2)/NO(2)(-) is capable of efficiently oxidizing simple hydroquinones even in the neutral form. Oxidation of anthracyclines by HRP/H(2)O(2)/NO(2)(-) is substantially less efficient relative to that by LPO/H(2)O(2)/NO(2)(-) at either pH 5 or pH 7, most likely due to the lower rate of NO(2)(-) metabolism by HRP/H(2)O(2). EPR measurements show that interaction of anthracyclines and 2,5-di-tert-butylhydroquinone with LPO/H(2)O(2)/NO(2)(-) generates the corresponding semiquinone radicals presumably via one-electron oxidation of their hydroquinone moieties. The possible role of the (*)NO(2) radical, a putative LPO metabolite of NO(2)(-), in oxidation of these compounds is discussed. Because in vivo the anthracyclines may co-localize with peroxidases, H(2)O(2), and NO(2)(-) in tissues, their oxidation via the proposed mechanism is likely. These observations reveal a novel, peroxidase- and nitrite-dependent mechanism for the oxidative transformation of the anticancer anthracyclines, which may be pertinent to their biological activities in vivo.

Publication types

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

MeSH terms

  • Antibiotics, Antineoplastic / adverse effects
  • Antibiotics, Antineoplastic / chemistry
  • Antibiotics, Antineoplastic / metabolism*
  • Daunorubicin / adverse effects
  • Daunorubicin / chemistry
  • Daunorubicin / metabolism*
  • Doxorubicin / adverse effects
  • Doxorubicin / chemistry
  • Doxorubicin / metabolism*
  • Electron Spin Resonance Spectroscopy
  • Horseradish Peroxidase / metabolism
  • Humans
  • Hydrogen Peroxide / metabolism
  • Hydrogen-Ion Concentration
  • Lactoperoxidase / metabolism
  • Nitrites / metabolism
  • Oxidation-Reduction
  • Spectrophotometry

Substances

  • Antibiotics, Antineoplastic
  • Nitrites
  • Doxorubicin
  • Hydrogen Peroxide
  • Horseradish Peroxidase
  • Lactoperoxidase
  • Daunorubicin