Theoretical studies of chemical reactivity of metabolically activated forms of aromatic amines toward DNA

Chem Res Toxicol. 2012 Oct 15;25(10):2236-52. doi: 10.1021/tx300313b. Epub 2012 Sep 20.

Abstract

The metabolism of aromatic and heteroaromatic amines (ArNH₂) results in nitrenium ions (ArNH⁺) that modify nucleobases of DNA, primarily deoxyguanosine (dG), by forming dG-C8 adducts. The activated amine nitrogen in ArNH⁺ reacts with the C8 of dG, which gives rise to mutations in DNA. For the most mutagenic ArNH₂, including the majority of known genotoxic carcinogens, the stability of ArNH⁺ is of intermediate magnitude. To understand the origin of this observation as well as the specificity of reactions of ArNH⁺ with guanines in DNA, we investigated the chemical reactivity of the metabolically activated forms of ArNH₂, that is, ArNHOH and ArNHOAc, toward 9-methylguanine by DFT calculations. The chemical reactivity of these forms is determined by the rate constants of two consecutive reactions leading to cationic guanine intermediates. The formation of ArNH⁺ accelerates with resonance stabilization of ArNH⁺, whereas the formed ArNH⁺ reacts with guanine derivatives with the constant diffusion-limited rate until the reaction slows down when ArNH⁺ is about 20 kcal/mol more stable than PhNH⁺. At this point, ArNHOH and ArNHOAc show maximum reactivity. The lowest activation energy of the reaction of ArNH⁺ with 9-methylguanine corresponds to the charge-transfer π-stacked transition state (π-TS) that leads to the direct formation of the C8 intermediate. The predicted activation barriers of this reaction match the observed absolute rate constants for a number of ArNH⁺. We demonstrate that the mutagenic potency of ArNH₂ correlates with the rate of formation and the chemical reactivity of the metabolically activated forms toward the C8 atom of dG. On the basis of geometric consideration of the π-TS complex made of genotoxic compounds with long aromatic systems, we propose that precovalent intercalation in DNA is not an essential step in the genotoxicity pathway of ArNH₂. The mechanism-based reasoning suggests rational design strategies to avoid genotoxicity of ArNH₂ primarily by preventing N-hydroxylation of ArNH₂.

MeSH terms

  • Amines / chemistry
  • Amines / metabolism*
  • DNA / chemistry
  • DNA / metabolism*
  • DNA Adducts / chemistry
  • DNA Adducts / metabolism*
  • Guanine / analogs & derivatives*
  • Guanine / chemistry
  • Guanine / metabolism
  • Hydrocarbons, Aromatic / chemistry
  • Hydrocarbons, Aromatic / metabolism*
  • Models, Molecular
  • Mutagens / chemistry
  • Mutagens / metabolism*
  • Thermodynamics

Substances

  • Amines
  • DNA Adducts
  • Hydrocarbons, Aromatic
  • Mutagens
  • 9-methylguanine
  • Guanine
  • DNA