DNA repair and sequence context affect 1O2-induced mutagenesis in bacteria

Electronic excited molecular oxygen (singlet oxygen, (1)O(2)) is known to damage DNA, yielding mutations. In this work, the mutagenicity induced by (1)O(2) in a defined sequence of DNA was investigated after replication in Escherichia coli mutants deficient for nucleotide and base excision DNA repair pathways. For this purpose a plasmid containing a (1)O(2)-damaged 14 base oligonucleotide was introduced into E.coli by transfection and mutations were screened by hybridization with an oligonucleotide with the original sequence. Mutagenesis was observed in all strains tested, but it was especially high in the BH20 (fpg), AYM57 (fpg mutY) and AYM84 (fpg mutY uvrC) strains. The frequency of mutants in the fpg mutY strain was higher than in the triple mutant fpg mutY uvrC, suggesting that activity of the UvrABC excinuclease can favor the mutagenesis of these lesions. Additionally, most of the mutations were G-->T and G-->C transversions, but this was dependent on the position of the guanine in the sequence and on repair deficiency in the host bacteria. Thus, the kind of repair and the mutagenesis associated with (1)O(2)-induced DNA damage are linked to the context of the damaged sequence.

[1]  A. H. Wanamarta,et al.  Influence of nucleotide excision repair of Escherichia coli on radiation-induced mutagenesis of double-stranded M13 DNA. , 1997, Mutation research.

[2]  P. Koehl,et al.  Construction of plasmids containing a unique acetylaminofluorene adduct located within a mutation hot spot. A new probe for frameshift mutagenesis. , 1989, Journal of molecular biology.

[3]  C. Menck,et al.  Singlet oxygen induced DNA damage. , 1992, Mutation research.

[4]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[5]  C. Menck,et al.  Singlet oxygen induces predominantly G to T transversions on a single-stranded shuttle vector replicated in monkey cells. , 1994, Free radical research.

[6]  T. O'Connor,et al.  Homogeneous Escherichia coli FPG Protein , 2001 .

[7]  A. Sarasin,et al.  DNA synthesis blocking lesions induced by singlet oxygen are targeted to deoxyguanosines. , 1992, Nucleic acids research.

[8]  J. Piette,et al.  Singlet oxygen‐induced mutations in M13 lacZ phage DNA. , 1987, The EMBO journal.

[9]  C. Menck,et al.  Mutation Spectrum Induced by Singlet Oxygen in Escherichia coli Deficient in Exonuclease III , 1999, Photochemistry and photobiology.

[10]  J. Aubry,et al.  Naphthalene endoperoxides as generators of singlet oxygen in biological media. , 2000, Methods in enzymology.

[11]  C. Burrows,et al.  Insertion of dGMP and dAMP during in vitro DNA synthesis opposite an oxidized form of 7,8-dihydro-8-oxoguanine. , 1999, Nucleic acids research.

[12]  M. Moriya.  Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-oxoguanine in DNA induces targeted G.C-->T.A transversions in simian kidney cells. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[13]  B. Slotman,et al.  The influence of combined Fpg- and MutY-deficiency on the spontaneous and γ-radiation-induced mutation spectrum in the lacZα gene of M13mp10 , 2000 .

[14]  H. Sies,et al.  Quantification of Singlet Oxygen Generated by Thermolysis of 3,3′-(1,4-Naphthylidene)dipropionate. Monomol and Dimol Photoemission and the Effects of 1,4-Diazabicyclo(2.2.2)octane. , 1989 .

[15]  Q. -. Zhang,et al.  Escherichia coli MutY protein has a guanine-DNA glycosylase that acts on 7,8-dihydro-8-oxoguanine:guanine mispair to prevent spontaneous G:C-->C:G transversions. , 1998, Nucleic acids research.

[16]  J. Cadet,et al.  Reaction of singlet oxygen with 2'-deoxyguanosine and DNA. Isolation and characterization of the main oxidation products. , 1995, Chemical research in toxicology.

[17]  J. Miller,et al.  Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[18]  H. Joenje,et al.  Mutational specificity of oxidative DNA damage. , 1993, Mutation research.

[19]  C. Menck,et al.  Involvement of Escherichia coli exonuclease III and endonuclease IV in the repair of singlet oxygen-induced DNA damage. , 1996, Carcinogenesis.

[20]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[21]  A. Sarasin,et al.  SINGLET OXYGEN INDUCED DNA DAMAGE AND MUTAGENICITY IN A SINGLE‐STRANDED SV40‐BASED SHUTTLE VECTOR , 1992, Photochemistry and photobiology.

[22]  Irwin D. J. Bross,et al.  A Confidence Interval for a Percentage Increase , 1954 .

[23]  P. Di Mascio,et al.  Singlet molecular oxygen causes loss of biological activity in plasmid and bacteriophage DNA and induces single-strand breaks. , 1989, Biochimica et biophysica acta.

[24]  E. Gajewski,et al.  Substrate specificity of the Escherichia coli Fpg protein (formamidopyrimidine-DNA glycosylase): excision of purine lesions in DNA produced by ionizing radiation or photosensitization. , 1992, Biochemistry.

[25]  S. Boiteux,et al.  Escherichia coli Fpg protein and UvrABC endonuclease repair DNA damage induced by methylene blue plus visible light in vivo and in vitro , 1991, Journal of bacteriology.

[26]  R. Floyd,et al.  Methylene blue plus light mediates 8-hydroxyguanine formation in DNA. , 1989, Archives of biochemistry and biophysics.

[27]  H. Birnboim,et al.  A rapid alkaline extraction procedure for screening recombinant plasmid DNA. , 1979, Nucleic acids research.

[28]  L. Klotz,et al.  Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. , 1997, Biological chemistry.

[29]  J. Cadet,et al.  Effects of UV and visible radiation on DNA-final base damage. , 1997, Biological chemistry.

[30]  C. Menck,et al.  Singlet oxygen induced mutation spectrum in mammalian cells. , 1992, Nucleic acids research.

[31]  I. Lambert,et al.  Carcinogen-induced frameshift mutagenesis in repetitive sequences. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[32]  W. Schulz,et al.  Formation of 8-hydroxy(deoxy)guanosine and generation of strand breaks at guanine residues in DNA by singlet oxygen. , 1991, Biochemistry.

[33]  J. Miller,et al.  Substrate specificity of Escherichia coli MutY protein. , 1996, Biochemistry.

[34]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[35]  B. Epe,et al.  Oxidative DNA base damage induced by singlet oxygen and photosensitization: recognition by repair endonucleases and mutagenicity. , 2000, Mutation research.

[36]  A. Grollman,et al.  Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG , 1991, Nature.

[37]  R. Floyd,et al.  Methylene blue plus light mediates 8-hydroxy 2'-deoxyguanosine formation in DNA preferentially over strand breakage. , 1990, Nucleic acids research.

[38]  F. Lederer,et al.  Homogeneous Escherichia coli FPG protein. A DNA glycosylase which excises imidazole ring-opened purines and nicks DNA at apurinic/apyrimidinic sites. , 1990, The Journal of biological chemistry.

[39]  E. Ohtsuka,et al.  8-Hydroxyguanine (7,8-dihydro-8-oxoguanine) in hot spots of the c-Ha-ras gene: effects of sequence contexts on mutation spectra. , 1995, Carcinogenesis.

[40]  L. Loeb,et al.  Mutations induced by methylene blue plus light in single-stranded M13mp2. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[41]  H. Kasai,et al.  Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues , 1987, Nature.

[42]  J. Essigmann,et al.  Mechanistic studies of ionizing radiation and oxidative mutagenesis: genetic effects of a single 8-hydroxyguanine (7-hydro-8-oxoguanine) residue inserted at a unique site in a viral genome. , 1990, Biochemistry.