Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1998 Aug 1;26(15):3599–3607. doi: 10.1093/nar/26.15.3599

Neighboring base damage induced by permanganate oxidation of 8-oxoguanine in DNA.

S Koizume 1, H Inoue 1, H Kamiya 1, E Ohtsuka 1
PMCID: PMC147747  PMID: 9671825

Abstract

We found that single-stranded DNA oligomers containing a 7, 8-dihydro-8-oxoguanine (8-oxo-G) residue have high reactivity toward KMnO4; the oxidation of 8-oxo-G induces damage to the neighboring nucleotide residues. This paper describes the novel reaction in detail, including experiments that demonstrate the mechanism involved in the induction of DNA damage. The results using DNAs of various base compositions indicated that damaged G, T and C (but not A) sites caused strand scissions after hot piperidine treatment and that the damage around the 8-oxo-G occurred at G sites in both single and double strands with high frequency. The latter substrates were less sensitive to damage. Further, kinetic studies of the KMnO4reaction of single-stranded oligomers suggested that thereactivity of the DNA bases at the site 5'-adjacent to the 8-oxo-G was in the order G >A >T, C. This preference correlates with the electron donating abilities of the bases. In addition, we found that the DNA damage at the G site, which was connected with the 8-oxo-G by a long abasic chain, was inhibited in the above order by the addition of dG, dA or dC. On the other hand, the damage reactions proceeded even after the addition of scavengers for active oxygen species. This study suggests the involvement of a redox process in the unique DNA damage initiated by the oxidation of the 8-oxo-G.

Full Text

The Full Text of this article is available as a PDF (219.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adam W., Saha-Möller C. R., Schönberger A., Berger M., Cadet J. Formation of 7,8-dihydro-8-oxoguanine in the 1,2-dioxetane-induced oxidation of calf thymus DNA: evidence for photosensitized DNA damage by thermally generated triplet ketones in the dark. Photochem Photobiol. 1995 Aug;62(2):231–238. doi: 10.1111/j.1751-1097.1995.tb05263.x. [DOI] [PubMed] [Google Scholar]
  2. Chung M. H., Kiyosawa H., Ohtsuka E., Nishimura S., Kasai H. DNA strand cleavage at 8-hydroxyguanine residues by hot piperidine treatment. Biochem Biophys Res Commun. 1992 Oct 15;188(1):1–7. doi: 10.1016/0006-291x(92)92341-t. [DOI] [PubMed] [Google Scholar]
  3. Darby G. K., Jones A. S., Tittensor J. R., Walker R. T. Chemical degradation of DNA oxidized by permanganate. Nature. 1967 Nov 25;216(5117):793–794. doi: 10.1038/216793a0. [DOI] [PubMed] [Google Scholar]
  4. Degan P., Bonassi S., De Caterina M., Korkina L. G., Pinto L., Scopacasa F., Zatterale A., Calzone R., Pagano G. In vivo accumulation of 8-hydroxy-2'-deoxyguanosine in DNA correlates with release of reactive oxygen species in Fanconi's anaemia families. Carcinogenesis. 1995 Apr;16(4):735–741. doi: 10.1093/carcin/16.4.735. [DOI] [PubMed] [Google Scholar]
  5. Floyd R. A., Watson J. J., Wong P. K., Altmiller D. H., Rickard R. C. Hydroxyl free radical adduct of deoxyguanosine: sensitive detection and mechanisms of formation. Free Radic Res Commun. 1986;1(3):163–172. doi: 10.3109/10715768609083148. [DOI] [PubMed] [Google Scholar]
  6. Hayatsu H., Ukita T. The selective degradation of pyrimidines in nucleic acids by permanganate oxidation. Biochem Biophys Res Commun. 1967 Nov 30;29(4):556–561. doi: 10.1016/0006-291x(67)90521-9. [DOI] [PubMed] [Google Scholar]
  7. Hutchinson F. Chemical changes induced in DNA by ionizing radiation. Prog Nucleic Acid Res Mol Biol. 1985;32:115–154. doi: 10.1016/s0079-6603(08)60347-5. [DOI] [PubMed] [Google Scholar]
  8. Ito K., Inoue S., Yamamoto K., Kawanishi S. 8-Hydroxydeoxyguanosine formation at the 5' site of 5'-GG-3' sequences in double-stranded DNA by UV radiation with riboflavin. J Biol Chem. 1993 Jun 25;268(18):13221–13227. [PubMed] [Google Scholar]
  9. Kamiya H., Murata-Kamiya N., Koizume S., Inoue H., Nishimura S., Ohtsuka E. 8-Hydroxyguanine (7,8-dihydro-8-oxoguanine) in hot spots of the c-Ha-ras gene: effects of sequence contexts on mutation spectra. Carcinogenesis. 1995 Apr;16(4):883–889. doi: 10.1093/carcin/16.4.883. [DOI] [PubMed] [Google Scholar]
  10. Kido K., Inoue H., Ohtsuka E. Sequence-dependent cleavage of DNA by alkylation with antisense oligodeoxyribonucleotides containing a 2-(N-iodoacetylaminoethyl)thio-adenine. Nucleic Acids Res. 1992 Mar 25;20(6):1339–1344. doi: 10.1093/nar/20.6.1339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lewis F. D., Wu T., Zhang Y., Letsinger R. L., Greenfield S. R., Wasielewski M. R. Distance-dependent electron transfer in DNA hairpins. Science. 1997 Aug 1;277(5326):673–676. doi: 10.1126/science.277.5326.673. [DOI] [PubMed] [Google Scholar]
  12. McCarthy J. G. An improvement in thymine specific chemical DNA sequencing. Nucleic Acids Res. 1989 Sep 25;17(18):7541–7541. doi: 10.1093/nar/17.18.7541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Melvin T., Plumb M. A., Botchway S. W., O'Neill P., Parker A. W. 193 nm light induces single strand breakage of DNA predominantly at guanine. Photochem Photobiol. 1995 Jun;61(6):584–591. doi: 10.1111/j.1751-1097.1995.tb09873.x. [DOI] [PubMed] [Google Scholar]
  14. Shigenaga M. K., Hagen T. M., Ames B. N. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10771–10778. doi: 10.1073/pnas.91.23.10771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Smith S. S., Laayoun A., Lingeman R. G., Baker D. J., Riley J. Hypermethylation of telomere-like foldbacks at codon 12 of the human c-Ha-ras gene and the trinucleotide repeat of the FMR-1 gene of fragile X. J Mol Biol. 1994 Oct 21;243(2):143–151. doi: 10.1006/jmbi.1994.1640. [DOI] [PubMed] [Google Scholar]
  16. Spassky A., Angelov D. Influence of the local helical conformation on the guanine modifications generated from one-electron DNA oxidation. Biochemistry. 1997 Jun 3;36(22):6571–6576. doi: 10.1021/bi962761d. [DOI] [PubMed] [Google Scholar]
  17. Spencer J. P., Jenner A., Aruoma O. I., Evans P. J., Kaur H., Dexter D. T., Jenner P., Lees A. J., Marsden D. C., Halliwell B. Intense oxidative DNA damage promoted by L-dopa and its metabolites. Implications for neurodegenerative disease. FEBS Lett. 1994 Oct 24;353(3):246–250. doi: 10.1016/0014-5793(94)01056-0. [DOI] [PubMed] [Google Scholar]
  18. Yanagawa H., Ogawa Y., Ueno M. Redox ribonucleosides. Isolation and characterization of 5-hydroxyuridine, 8-hydroxyguanosine, and 8-hydroxyadenosine from Torula yeast RNA. J Biol Chem. 1992 Jul 5;267(19):13320–13326. [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES