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. 1992 May 25;20(10):2465–2469. doi: 10.1093/nar/20.10.2465

DNA synthesis blocking lesions induced by singlet oxygen are targeted to deoxyguanosines.

D T Ribeiro 1, F Bourre 1, A Sarasin 1, P Di Mascio 1, C F Menck 1
PMCID: PMC312380  PMID: 1375992

Abstract

In vitro DNA synthesis on single stranded templates damaged by singlet oxygen was investigated in the supF tRNA gene sequence, using several DNA polymerases. Singlet oxygen was generated by the thermal decomposition of the water soluble with the endoperoxide of disodium 3,3'-(1,4-naphthylidene) dipropionate (NDPO2). The data demonstrated that damage at deoxyguanosine residues interrupts DNA polymerization. Modified T7 phage and Thermus aquaticus DNA polymerases were found to synthesize DNA fragments which terminated opposite deoxyguanosine, while T4 phage DNA polymerase and avian myeloblast virus reverse transcriptase were blocked one nucleotide 3' to deoxyguanosine positions on the template. DNA polymerase I (Klenow fragment) from Escherichia coli was inhibited at both positions, before and at the putative damaged sites. The blocking lesions, induced by 5 mM NDPO2, were estimated to be approximately 1.5 per 260 nucleotides, corresponding to 2% of deoxyguanosines. The distribution of lesions in the supF gene did not reveal any specific sequence context which showed distinct susceptibility to the attack of singlet oxygen.

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Selected References

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

  1. Blazek E. R., Peak J. G., Peak M. J. Singlet oxygen induces frank strand breaks as well as alkali- and piperidine-labile sites in supercoiled plasmid DNA. Photochem Photobiol. 1989 May;49(5):607–613. doi: 10.1111/j.1751-1097.1989.tb08431.x. [DOI] [PubMed] [Google Scholar]
  2. Cadet J., Berger M., Decarroz C., Wagner J. R., van Lier J. E., Ginot Y. M., Vigny P. Photosensitized reactions of nucleic acids. Biochimie. 1986 Jun;68(6):813–834. doi: 10.1016/s0300-9084(86)80097-9. [DOI] [PubMed] [Google Scholar]
  3. Decuyper-Debergh D., Piette J., Van de Vorst A. Singlet oxygen-induced mutations in M13 lacZ phage DNA. EMBO J. 1987 Oct;6(10):3155–3161. doi: 10.1002/j.1460-2075.1987.tb02626.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Devasagayam T. P., Steenken S., Obendorf M. S., Schulz W. A., Sies H. Formation of 8-hydroxy(deoxy)guanosine and generation of strand breaks at guanine residues in DNA by singlet oxygen. Biochemistry. 1991 Jun 25;30(25):6283–6289. doi: 10.1021/bi00239a029. [DOI] [PubMed] [Google Scholar]
  5. Di Mascio P., Menck C. F., Nigro R. G., Sarasin A., Sies H. Singlet molecular oxygen induced mutagenicity in a mammalian SV40-based shuttle vector. Photochem Photobiol. 1990 Mar;51(3):293–298. doi: 10.1111/j.1751-1097.1990.tb01713.x. [DOI] [PubMed] [Google Scholar]
  6. Di Mascio P., Wefers H., Do-Thi H. P., Lafleur M. V., Sies H. Singlet molecular oxygen causes loss of biological activity in plasmid and bacteriophage DNA and induces single-strand breaks. Biochim Biophys Acta. 1989 Mar 1;1007(2):151–157. doi: 10.1016/0167-4781(89)90033-x. [DOI] [PubMed] [Google Scholar]
  7. Fiel R. J., Datta-Gupta N., Mark E. H., Howard J. C. Induction of DNA damage by porphyrin photosensitizers. Cancer Res. 1981 Sep;41(9 Pt 1):3543–3545. [PubMed] [Google Scholar]
  8. Floyd R. A., West M. S., Eneff K. L., Schneider J. E. Methylene blue plus light mediates 8-hydroxyguanine formation in DNA. Arch Biochem Biophys. 1989 Aug 15;273(1):106–111. doi: 10.1016/0003-9861(89)90167-7. [DOI] [PubMed] [Google Scholar]
  9. Friedmann T., Brown D. M. Base-specific reactions useful for DNA sequencing: methylene blue--sensitized photooxidation of guanine and osmium tetraoxide modification of thymine. Nucleic Acids Res. 1978 Feb;5(2):615–622. doi: 10.1093/nar/5.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kawanishi S., Inoue S., Sano S., Aiba H. Photodynamic guanine modification by hematoporphyrin is specific for single-stranded DNA with singlet oxygen as a mediator. J Biol Chem. 1986 May 5;261(13):6090–6095. [PubMed] [Google Scholar]
  11. Kuchino Y., Mori F., Kasai H., Inoue H., Iwai S., Miura K., Ohtsuka E., Nishimura S. Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature. 1987 May 7;327(6117):77–79. doi: 10.1038/327077a0. [DOI] [PubMed] [Google Scholar]
  12. Larson K. L., Strauss B. S. Influence of template strandedness on in vitro replication of mutagen-damaged DNA. Biochemistry. 1987 May 5;26(9):2471–2479. doi: 10.1021/bi00383a011. [DOI] [PubMed] [Google Scholar]
  13. Lee P. C., Rodgers M. A. Laser flash photokinetic studies of rose bengal sensitized photodynamic interactions of nucleotides and DNA. Photochem Photobiol. 1987 Jan;45(1):79–86. doi: 10.1111/j.1751-1097.1987.tb08407.x. [DOI] [PubMed] [Google Scholar]
  14. Moore P. D., Bose K. K., Rabkin S. D., Strauss B. S. Sites of termination of in vitro DNA synthesis on ultraviolet- and N-acetylaminofluorene-treated phi X174 templates by prokaryotic and eukaryotic DNA polymerases. Proc Natl Acad Sci U S A. 1981 Jan;78(1):110–114. doi: 10.1073/pnas.78.1.110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Moore P., Strauss B. S. Sites of inhibition of in vitro DNA synthesis in carcinogen- and UV-treated phi X174 DNA. Nature. 1979 Apr 12;278(5705):664–666. doi: 10.1038/278664a0. [DOI] [PubMed] [Google Scholar]
  16. OhUigin C., McConnell D. J., Kelly J. M., van der Putten W. J. Methylene blue photosensitised strand cleavage of DNA: effects of dye binding and oxygen. Nucleic Acids Res. 1987 Sep 25;15(18):7411–7427. doi: 10.1093/nar/15.18.7411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Piette J., Calberg-Bacq C. M., Lopez M., van de Vorst A. Terminations of DNA synthesis on 'proflavine and light'-treated phi X174 single-stranded DNA. Biochim Biophys Acta. 1984 Apr 5;781(3):257–264. doi: 10.1016/0167-4781(84)90091-5. [DOI] [PubMed] [Google Scholar]
  18. Piette J., Moore P. D. DNA synthesis on phi X174 template damaged by proflavine and light treatment. Photochem Photobiol. 1982 May;35(5):705–708. doi: 10.1111/j.1751-1097.1982.tb02633.x. [DOI] [PubMed] [Google Scholar]
  19. Piette J. Mutagenic and genotoxic properties of singlet oxygen. J Photochem Photobiol B. 1990 Jan;4(3):335–339. doi: 10.1016/1011-1344(90)85039-y. [DOI] [PubMed] [Google Scholar]
  20. Ribeiro D. T., Madzak C., Sarasin A., Di Mascio P., Sies H., Menck C. F. Singlet oxygen induced DNA damage and mutagenicity in a single-stranded SV40-based shuttle vector. Photochem Photobiol. 1992 Jan;55(1):39–45. doi: 10.1111/j.1751-1097.1992.tb04207.x. [DOI] [PubMed] [Google Scholar]
  21. Schneider J. E., Price S., Maidt L., Gutteridge J. M., Floyd R. A. Methylene blue plus light mediates 8-hydroxy 2'-deoxyguanosine formation in DNA preferentially over strand breakage. Nucleic Acids Res. 1990 Feb 11;18(3):631–635. doi: 10.1093/nar/18.3.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Shibutani S., Takeshita M., Grollman A. P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature. 1991 Jan 31;349(6308):431–434. doi: 10.1038/349431a0. [DOI] [PubMed] [Google Scholar]
  23. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]

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