Oxidative-stress-driven mutagenesis in the small intestine of the gpt delta mouse induced by oral administration of potassium bromate

Mutat Res Genet Toxicol Environ Mutagen. 2020 Feb-Mar:850-851:503136. doi: 10.1016/j.mrgentox.2020.503136. Epub 2020 Jan 15.

Abstract

Tumorigenesis induced by oxidative stress is thought to be initiated by mutagenesis, but via an indirect mechanism. The dose-response curves for agents that act by this route usually show a threshold, for unknown reasons. To gain insight into these phenomena, we have analyzed the dose response for mutagenesis induced by the oral administration of potassium bromate, a typical oxidative-stress-generating agent, to gpt delta mice. The agent was given orally for 90 d to either Nrf2+ or Nrf2-knockout (KO) mice and mutants induced in the small intestine were analyzed. In Nrf2+mice, the mutant frequency was significantly greater than in the vehicle controls at a dose of 0.6 g/L but not at 0.2 g/L, indicating that a practical threshold for mutagenesis lies between these doses. At 0.6 g/L, the frequencies of G-to-T transversions (landmark mutations for oxidative stress) and G-to-A transitions were significantly elevated. In Nrf2-KO mice, too, the total mutant frequency was increased only at 0.6 g/L. G-to-T transversions are likely to have driven tumorigenesis in the small intestine. A site-specific G-to-T transversion at guanine (nucleotide 406) in a 5'-TGAA-3' sequence in gpt, and our primer extension reaction showed that formation of the oxidative DNA base modification 8-oxo-deoxyguanosine (8-oxo-dG) at nucleotide 406 was significantly increased at doses of 0.6 and 2 g/L in the gpt delta mice. In the Apc oncogene, guanine residues in the same or similar sequences (TGAA or AGAA) are highly substituted by thymine (G-to-T transversions) in potassium bromate-induced tumors. We propose that formation of 8-oxo-dG in the T(A)GAA sequence is an initiating event in tumor formation in the small intestine in response to oxidative stress.

Keywords: In vivo mutation; Nrf2-knockout; Site-specific mutation; Threshold; Transgenic mouse assay.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 8-Hydroxy-2'-Deoxyguanosine / genetics
  • Administration, Oral
  • Animals
  • Bromates / pharmacology
  • Bromates / toxicity*
  • Carcinogenesis / drug effects
  • Carcinogenesis / genetics
  • DNA / drug effects
  • DNA / genetics
  • Dose-Response Relationship, Drug
  • Intestine, Small / drug effects
  • Intestine, Small / pathology
  • Mice
  • Mice, Knockout
  • Mutagenesis / drug effects
  • Mutagenesis / genetics*
  • Mutation
  • NF-E2-Related Factor 2 / genetics
  • Oxidative Stress / drug effects
  • Oxidative Stress / genetics*
  • Pentosyltransferases / genetics*

Substances

  • Bromates
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, mouse
  • potassium bromate
  • 8-Hydroxy-2'-Deoxyguanosine
  • DNA
  • Pentosyltransferases