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The frequency of MMS-induced, umuDC-dependent, mutations declines during starvation in Escherichia coli

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Abstract

It has been found that the level of methyl methanesulfonate (MMS)-induced mutation in Escherichia coli is dependent on the level of UmuD(D′)C proteins. The frequency of argE(ochre)→Arg+ mutations (which occur predominantly by AT→TA transversions) and RifS→RifR mutations is much higher when UmuDC or UmuD'C are overproduced in the cell. When MMS-treated bacteria were starved for progressively longer times and hence the expression of mutations delayed, the level of mutations observed progressively declined. This same treatment had no effect on the degree of SOS induction. Examination of plasmid DNAs, isolated from MMS-treated cells, for their sensitivity to the specific endonucleases Fpg and Nth revealed that MMS causes formation of abasic sites, which are repaired during cell starvation. It is assumed that, in non-dividing cells, apurinic sites are mostly repaired by RecA-mediated recombinational repair. This pathway, which is error-free, is compared with the processing pathway in metabolically active cells, where translesion synthesis by the UmuD′2C-RecA-DNA polymerase III holoenzyme complex occurs; this latter pathway is error-prone.

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References

  • Asai T, Sommer S, Bailone A, Kogoma T (1993) Homologous recombination-dependent initiation of DNA replication from DNA damage-inducible origins in Escherichia coli. EMBO J 12:3287–3295

    Google Scholar 

  • Bachmann BJ (1987) Derivations and genotypes of some mutant derivatives of Escherichia coli K-12. In: Neidhardt FC, Ingraham J, Low KB, Magasanik B, Schaechler M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol 2. American Society for Microbiology, Washington, DC, pp 1190–1219

    Google Scholar 

  • Bachmann BJ (1990) Linkage map of Escherichia coli K-12, Edition 8. Microbiol Rev 54:130–197

    Google Scholar 

  • Beranek D (1990) Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat Res 231:11–30

    Google Scholar 

  • Bjelland S, Bjoras M, Seeberg E (1993) Ecxision of 3-methylguanine from alkylated DNA by 3-methyladenine DNA glycosylase I of Escherichia coli. Nucleic Acids Res 21:2045–2049

    Google Scholar 

  • Bockrath R, Kow YW Wallace SS (1993) Chemically altered apurinic sites in ΦX174 DNA give increased mutagenesis in SOS-induced E. coli. Mutat Res 288:207–214

    Google Scholar 

  • Boiteux S (1993) Properties and biological functions of the Nth and Fpg proteins of Escherichia coli: two DNA glycosylases that repair oxidative damage in DNA. J Photochem Photobiol [B Biol] 19:87–96

    Google Scholar 

  • Boiteux S, Huisman O, Laval J (1984) 3-Methyladenine residues in DNA induce the SOS function sfiA in Escherichia coli. EMBO J 3:2569–2573

    Google Scholar 

  • Cunningham RP, Weiss B (1985) Endonuclease III (nth) mutants of Escherichia coli. Proc Natl Acad Sci USA 85:474–478

    Google Scholar 

  • Doudney CO, Haas FL (1958) Modification of ultraviolet-induced mutation frequency and survival in bacteria by post-irradiation treatment. Proc Natl Acad Sci USA 44:390–401

    Google Scholar 

  • Epe B, Pflaum M, Boiteux S (1993) DNA damage induced by photosensitizers in cellular and cell-free systems. Mutat Res 299:135–145

    Google Scholar 

  • Foster PL, Eisenstadt E (1985) Induction of transversion mutations in Escherichia coli by N-methyl-N-nitro-N-nitrosoguanidine is SOS dependent. J Bacteriol 163:213–220

    Google Scholar 

  • George DL, Witkin EM (1974) Slow repair in an mfd mutant of Escherichia coli B/r. Mol Gen Genet 133:283–291

    Google Scholar 

  • Glickman BW, Radman M (1980) Escherichia coli mutator mutants deficient in methylation-instructed DNA mismatch correction. Proc Natl Acad Sci USA 77:1063–1067

    Google Scholar 

  • Grzesiuk E, Janion C (1993) Some aspects of EMS-induced mutagenesis in Escherichia coli. Mutat Res 297:313–321

    Google Scholar 

  • Janion C (1982) Effect of bacterial host repair systems on the viability of hydroxylamine and methyl methanesulfonate treated T4. Mol Gen Genet 186:419–426

    Google Scholar 

  • Jeggo P, Defais M, Samson L, Schnendel P (1978) The adaptive response of E. coli to low levels of alkylating agent: the role of polA in killing adaptation. Mol Gen Genet 162:299–305

    Google Scholar 

  • Kow YW (1989) Mechanism of action of Escherichia coli exonuclease III. Biochemistry 28:3280–3287

    Google Scholar 

  • Langer PJ, Perry KL, Walker GC (1985) Complementation of a pKM101 derivative that decreases resistance to UV killing but increases susceptibility to mutagenesis. Mutat Res 150:147–158

    Google Scholar 

  • Lin J-J, Sancar A (1989) A new mechanism for repairing oxidative damage to DNA: (A)BC excinuclease removes AP sites and thymine glycols from DNA. Biochemistry 28:7979–7984

    Google Scholar 

  • Lindahl T, Sedgwick B, Sekiguchi M, Nakabeppu Y (1988) Regulation and expression of the adaptive response to alkylating agents. Annu Rev Biochem 57:133–157

    Google Scholar 

  • Lloyd RS, Haidle W, Robertson DL (1978) Bleomycin-specific fragmentation of double-stranded DNA. Biochemistry 17:1890–1896

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory mannual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Marsh L, Walker GC (1985) Cold sensitivity induced by overproduction of UmuDC in Escherichia coli. J Bacteriol 162:155–161

    Google Scholar 

  • Marek F, Sedlakova M (1992) Inducible stable DNA replication in Escherichia coli uvr + cells, treated with genotoxic chemicals. Mutat Res 281:63–66

    Google Scholar 

  • McCarthy JG, Edington BV, Schendel PF (1983) Inducible repair of phosphotriesters in Escherichia coli. Proc Nat Acad Sci USA 80:7380–7384

    Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Modrich P (1991) Mechanism and biological effect of mismatch repair. Annu Rev Genet 25:229–253

    Google Scholar 

  • Nakabeppu Y, Sekiguchi (1986) Regulatory mechanism for induction of synthesis of repair enzymes in response to alkylation agents: Ada protein acts as a transcriptional regulator. Proc Natl Acad Sci USA 83:6297–6301

    Google Scholar 

  • Nohmi T, Battista JR, Dodson LA, Walker GC (1988) RecA mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation. Proc Natl Acad Sci USA 85:1816–1820

    Google Scholar 

  • de Oliveira RC, Laval J, Boiteux S (1986) Induction of SOS and adaptive responses by alkylating agents in Escherichia coli mutants deficient in 3-methyladenine-DNA glycosylase activities. Mutat Res 183:11–20

    Google Scholar 

  • Oller AR, Fijalkowska IJ, Dunn RL, Schaaper RM (1992) Transcription-repair coupling determines the strandedness of ultraviolet mutagenesis in Escherichia coli. Proc Natl Acad Sci USA 89:11036–11040

    Google Scholar 

  • Plachta A, Janion C (1992) Is the tRNA ochre suppressor supX derived from gltT? Acta Biochim Pol 39:265–269

    Google Scholar 

  • Radman M (1974) Phenomenology of an inducible mutagenis DNA repair pathway in Escherichia coli: SOS repair hypothesis. In: Prakash L, Sherman F, Miller M, Lawrence C, Tabor HW (eds) Molecular and environmental aspects of mutagenesis vol 3., Charles C. Thomas Publisher, Springfield, pp 128–142

    Google Scholar 

  • Rajagopalan M, Lu C, Woodgate R, O'Donell M, Goodman MF, Echols H (1992) Activity of the purified mutagenesis proteins UmuC, UmuD', and RecA in replicative bypass of an abasic DNA lesion by DNA polymerase III. Proc Natl Acad Sci USA 89:10777–10781

    Google Scholar 

  • Samson L, Cairns J (1977) A new pathway for DNA repair in Escherichia coli. Nature 267:281–282

    Google Scholar 

  • Schendel PF, Defais M (1980) The role of umuC gene product in mutagenesis by simple alkylating agents. Mol Gen Genet 177:661–665

    Google Scholar 

  • Sedgwick B, Vaughan P (1991) Widespread adaptive response against environmental methylating agents in microorganisms. Mutat Res 250:211–221

    Google Scholar 

  • Selby CP, Sancar A (1993) Molecular mechanism of transcription-repair coupling. Science 260:53–58

    Google Scholar 

  • Shevell DE, Bradford M, Friedman M, Walker GC (1990) Resistance to alkylation damage in Escherichia coli: role of the Ada protein in induction of the adaptive response. Mutat Res 233:53–72

    Google Scholar 

  • Shinagawa H, Kato T, Ise T, Makino K, Nakata A (1983) Cloning and characterisation of the umu gene responsible for inducible mutagenesis in Escherichia coli. Gene 23:167–174

    Google Scholar 

  • Sledziewska-Gójska E, Janion C (1989) Alternative pathways of methyl methanesulfonate-induced mutagenesis in Escherichia coli. Mol Gen Genet 216:126–131

    Google Scholar 

  • Sledziewska-Gójska E, Grzesiuk E, Plachta A, Janion C (1992) Mutagenesis of Escherichia coli: a method for determining mutagenic specificity by analysis of tRNA suppressors. Mutagenesis 7:41–46

    Google Scholar 

  • Sommer S, Bailone A, Devoret R (1994) The appearance of the UmuD′C protein complex in Escherichia coli switches repair from homologous recombination to SOS mutagenesis. Mol Microbiol (in press)

  • Strauss BS (1991) The “A rule” of mutagen specificity: a consequence of DNA polymerase bypass of non-instructional lessions? Bioessays 13:79–84

    Google Scholar 

  • Takahashi K, Kawazoe Y, Sakumi K, Nakabeppu Y, Sekiguchi M (1988) Activation of Ada protein as a transcriptional regulator by direct alkylation with methylating agents. J Biol Chem 263:13490–13492

    Google Scholar 

  • Teo I, Sedwick B, Kilpatrick MW, McCarthy TV, Lindahl T (1986) The intracellular signal for induction of resistance to alkylating agents in E. coli. Cell 45:315–324

    Google Scholar 

  • Volkert MR, Gately FH, Hajec LI (1989) Expression of DNA damage-inducible genes of Escherichia coli upon treatment with methylating, ethylating and propylating agents. Mutat Res 217:109–1115

    Google Scholar 

  • Walker GC (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in E. coli. Microbiol Rev 48:60–83

    Google Scholar 

  • Williams PH, Clarke CH (1971) Pre- and post-irradiation effects upon lethality and reversion in Salmonella typhimurium. J Gen Microbiol 68:199–205

    Google Scholar 

  • Witkin EM (1969) Ultraviolet-induced mutations and DNA repair. Annu Rev Microbiol 23:487–514

    Google Scholar 

  • Witkin EM (1976) Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol Rev 40:869–907

    Google Scholar 

  • Woodgate R (1992) Construction of a umuDC operon substitution mutation in Escherichia coli. Mutat Res 281:221–225

    Google Scholar 

  • Zhou W, Doetsch W (1993) Effects of abasic and DNA single-strand breaks on prokaryotic RNA polymerases. Proc Natl Acad Sci USA 90:6601–6605

    Google Scholar 

Download references

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Authors and Affiliations

  1. Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawinskiego 5a, 02-106, Warsaw, Poland

    Elzbieta Grzesiuk & Celina Janion

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  1. Elzbieta Grzesiuk
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  2. Celina Janion
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Communicated by R. Devoret

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Grzesiuk, E., Janion, C. The frequency of MMS-induced, umuDC-dependent, mutations declines during starvation in Escherichia coli . Molec. Gen. Genet. 245, 486–492 (1994). https://doi.org/10.1007/BF00302261

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  • DOI: https://doi.org/10.1007/BF00302261

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