Cell proliferation in liver of Mmh/Ogg1-deficient mice enhances mutation frequency because of the presence of 8-hydroxyguanine in DNA

Cancer Res. 2003 Jul 15;63(14):4287-92.

Abstract

The Mmh/Ogg1 gene product maintains the integrity of the genome by removing the damaged base 8-hydroxyguanine (8-OH-G), one of the major DNA lesions generated by reactive oxygen species. Using Ogg1-deficient mice, we sought to establish if cells having high amounts of 8-OH-G have the ability to proliferate and whether the mutation frequency increases after proliferation in vivo. When KBrO(3), a known renal carcinogen, at a dose of 2 grams/liter was administered to Ogg1 mutant mice for 12 weeks, the amount of 8-OH-G in liver DNA from treated Ogg1(-/-) mice increased 26.1 times that of treated Ogg1(+/+) mice. The accumulated 8-OH-G did not decrease 4 weeks after cessation of KBrO(3) treatment. Partial hepatectomy was performed on Ogg1(+/-) and Ogg1(-/-) mice after being treated with KBrO(3) for 12 weeks. The remnant liver from Ogg1(-/-) mice treated with KBrO(3) regenerated to the same extent as nontreated Ogg1(+/-) mice. In addition, 8-OH-G was not repaired during cell proliferation by partial hepatectomy, indicating that there is no replication coupled repair of preexisting 8-OH-G. The mutation frequency after the regeneration of liver from treated Ogg1(-/-) mice showed a 3.5-fold increase compared with before regeneration. This represents a mutation frequency 6.2 times that of normal levels. The proliferation of cells having accumulated amounts of 8-OH-G caused mainly GC-->TA transversions. These results showed that inactivation of the Ogg1 gene leads to a higher risk of cancer because cells with accumulated 8-OH-G still retain the ability to proliferate, leading to an increase in the mutation frequency.

MeSH terms

  • Animals
  • Bromates
  • Carcinogens
  • Cell Division / genetics
  • DNA / drug effects
  • DNA / genetics
  • DNA / metabolism*
  • DNA Damage / genetics*
  • DNA Repair
  • DNA-Formamidopyrimidine Glycosylase
  • Female
  • Guanine / analogs & derivatives*
  • Guanine / metabolism*
  • Hepatectomy
  • Liver / cytology
  • Liver / drug effects
  • Liver / enzymology
  • Liver / physiology*
  • Liver Regeneration / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mutation*
  • N-Glycosyl Hydrolases / deficiency*
  • N-Glycosyl Hydrolases / genetics

Substances

  • Bromates
  • Carcinogens
  • potassium bromate
  • 8-hydroxyguanine
  • Guanine
  • DNA
  • N-Glycosyl Hydrolases
  • DNA-Formamidopyrimidine Glycosylase