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UV irradiation inhibits initiation of DNA replication from oriC in Escherichia coli

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Summary

Irradiation of Escherichia coli with UV light causes a transient inhibition of DNA replication. This effect is generally thought to be accounted for by blockage of the elongation of DNA replication by UV-induced lesions in the DNA (a cis effect). However, by introducing an unirradiated E. coli origin (oriC)-dependent replicon into UV-irradiated cells, we have been able to show that the environment of a UV-irradiated cell inhibits initiation of replication from oriC on a dimer-free replicon. We therefore conclude that UV-irradiation of E. coli leads to a trans-acting inhibition of initiation of replication. The inhibition is transient and does not appear to be an SOS function.

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References

  • Appleyard RK (1954) Segregation of new lysogenic types during growth of a doubly lysogenic strain derived from Escherichia coli K12. Genetics 39:440–452

    Google Scholar 

  • Billen D (1969) Replication of the bacterial chromosome: Location of new initiation sites after irradiation. J Bacteriol 97:1169–1175

    Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkaline procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    Google Scholar 

  • Bowden DW, Twersky RS, Calender R (1975) Escherichia coli deoxyribonucleic acid synthesis mutants. Their effect upon bacteriophage P2 and satellite bacteriophage P4 deoxyribonucleic acid synthesis. J Bacteriol 124:167–275

    Google Scholar 

  • Caillet-Fauquet P, Defais M, Radman M (1977) Molecular mechanisms of induced mutagenesis. Replication in vivo of bacteriophage φX174 single-stranded, ultraviolet light-irradiated DNA in intact and irradiated host cells. J Mol Biol 117:95–112

    Google Scholar 

  • Casaregola S, Khidir M, Holland IB (1987) Effects of modulation of RnaseH production on the recovery of DNA synthesis following UV irradiation in Escherichia coli. Mol Gen Genet 209:494–498

    Google Scholar 

  • Castellazi M, Brachet P, Eisen H (1972) Isolation and characterisation of deletions in bacteriophage λ residing as a prophage in E. coli K12. Mol Gen Genet 117:211–218

    Google Scholar 

  • Denhardt DT (1966) A membrane filter technique for the detection of complementary DNA. Biochem Biophys Res Commun 23:641–646

    Google Scholar 

  • Doudney CO (1971) Deoxyribonucleic acid replication in UV damaged bacteria revisited. Mutat Res 12:121–128

    Google Scholar 

  • Doudney CO (1973) Rifampicin limitation of DNA synthesis in ultraviolet-damaged bacteria: Evidence for post irradiation replication syndrony. Biochim Biophys Acta 312:243–247

    Google Scholar 

  • Eberle H, Forrest N (1982) Regulation of DNA sythesis and capacity for initiation in DNA temperature sensitive mutants of Escherichia coli. II. Requirements for acquisition and expression of initiation capacity. Mol Gen Genet 186:66–70

    Google Scholar 

  • Eberle H, Forrest N, Hrynyszyn J, Van Knapp J (1982) Regulation of DNA synthesis and capacity for initiation in DNA temperature sensitive mutants of Escherichia coli. I. Reinitiation and chain elongation. Mol Gen Genet 186:57–65

    Google Scholar 

  • Eridle L, Inman RB (1984) The role of gene O protein in the replication of bacteriophage λ. Virology 139:97–108

    Google Scholar 

  • Friedberg EC (1984) DNA Repair. WH Freeman and Company, New York

    Google Scholar 

  • Furth ME, Wickner S (1983) λDNA replication. In: Hendrix RW, Roberts JW, Stahl FW, Weisberg RA (eds) Lambda II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 145–173

    Google Scholar 

  • Gill DS, Kumarasamy R, Symons RH (1981) Cucumber Mosaic Virus-induced RNA replicase: Solubilisation and partial purification of the particulate enzyme. Virology 113:1–8

    Google Scholar 

  • Gottesman S (1981) Genetic control of the SOS system. Cell 23:1–2

    Google Scholar 

  • Grossman AD, Straus DB, Walter WA, Gross CA (1987) 453-1 synthesis can regulate the synthesis of heat shock protein in E. coli. Genes Dev 1:179–184

    Google Scholar 

  • Hocking SM, Egan JB (1982) Genetic studies of Coliphage 186. J Virol 44:1068–1071

    Google Scholar 

  • Hooper I, Egan JB (1981) Coliphage 186 infection requires host initiation functions DnaA and DnaC. J Virol 40:599–601

    Google Scholar 

  • Hooper I, Woods WH, Egan JB (1981) Coliphage 186 replication is delayed when the host cell is UV irradiated before infection. J Virol 40:341–349

    Google Scholar 

  • Kafatos FC, Jones CW, Efstratidis A (1979) Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res 7:1541–1552

    Google Scholar 

  • Khidhir MA, Casaregola S, Holland IB (1985) Mechanism of transient inhibition of DNA synthesis in ultraviolet-irradiated E. coli: Inhibition is independent of recA whilst recovery requires RecA protein itself and an additional, inducible SOS function. Mol Gen Genet 199:133–140

    Google Scholar 

  • Kogoma T (1986) RNaseH-Defective mutants of Escherichia coli. J Bacteriol 166:361–363

    Google Scholar 

  • Krueger JH, Walker GC (1984) GroEL and dnaK genes of Escherichia coli are induced by UV-irradiation and naladixic acid in an htpR +-dependent fashion. Proc Natl Acad Sci USA 81:1499–1503

    Google Scholar 

  • Kuempel PL (1972) Deoxyribonucleic acid-Deoxyribonucleic Acid hybridisation assay for replication origin Deoxyribonucleic acid of Escherichia coli. J Bacteriol 110:917–925

    Google Scholar 

  • Laskey RA, Mills AD (1975) Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem 56:335–341

    Google Scholar 

  • Livneh Z (1986) Replication of UV-irradiated single-stranded DNA by DNA polymerase III Holoenzyme of Escherichia coli: Evidence for bypass of pyrimidine photodimers. Proc Natl Acad Sci 83:4599–4603

    Google Scholar 

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

    Google Scholar 

  • Meyenberg K von, Hansen FG, Neilson LD, Jorgensen P (1977) Origin of replication, oriC, of the Escherichia coli chromosome: Mapping of genes relative to R. EcoRI cleavage sites in the oriC region. Mol Gen Genet 158:101–109

    Google Scholar 

  • Meyenberg K von, Hansen FG, Riise E, Bergmans HEN, Meijer M, Meser W (1979) Origin of replication, oriC, of the Escherichia coli K12 chromosome: Genetic mapping and minichromosome replication. Cold Spring Harbor Symp Quant Biol 43:121–138

    Google Scholar 

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

    Google Scholar 

  • Moore PD, Bose KK, Rabkin SD, Strauss BS (1981) Sites of termination of in vitro DNA synthesis of ultraviolet and N-acetyl-aminofluorene-treated φX174 templates by prokaryotic and cukaryotic DNA polymerases. Proc Natl Acad Sci USA 78:110–114

    Google Scholar 

  • Quiñones A, Kücherer C, Piechocki R, Messer W (1987) Reduced transcription of the rnh gene in Escherichia coli mutants expressing the SOS regulon constitutively. Mol Gen Genet 206:95–100

    Google Scholar 

  • Roberts JW, Devoret R (1983) Lysogenic Induction. In: Hendrix RW, Roberts JW, Stahl FW, Weisberg RA (eds) Lambda II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 123–144

    Google Scholar 

  • Rupp WD, Howard-Flanders P (1968) Discontinuities in the DNA synthesised in an excision-defective strain of E. coli following ultraviolet irradiation. J Mol Biol 31:291–304

    Google Scholar 

  • Salles B, Paoletti C (1983) Control of UV induction of recA protein. Proc Natl Acad Sci USA 80:65–69

    Google Scholar 

  • Skarstad K, Boyle E (1988) Perturbed chromosomal replication in recA Mutants of Escherichia coli. J Bacteriol 170:2549–2554

    Google Scholar 

  • Smith KC (1969) DNA synthesis in sensitive and resistant mutants of Escherichia coli B after ultraviolet irradiation. Mutat Res 8:481–495

    Google Scholar 

  • Smith KC, O'Leary M (1968) The pitfalls of measuring DNA synthesis kinetics as exemplified in ultraviolet radiation studies. Biochim Biophys Acta 169:430–438

    Google Scholar 

  • Soll L (1980) Isolation and characterisation of λb221poriC asnA, a plaque-forming specialised transducing phage carrying the origin of replication of the Escherichia coli chromosome. Mol Gen Genet 178:381–389

    Google Scholar 

  • Sussman R, Jacob F (1962) Genetique physiologigue — Sur un systeme de repression thermosensible chez le bacteriophage λ d'Escherichia coli. C R Acad Sci (Paris) 254:1517–1519

    Google Scholar 

  • Verma M, Egan JB (1985) Phenotypic variations in strain AB1157 cultivars of Escherichia coli from different sources. J Bacteriol 164:1381–1382

    Google Scholar 

  • Villani G, Boiteux S, Radman M (1978) Mechanism of ultraviolet-induced mutagenesis: Extent and fidelity of in vitro DNA synthesis on irradiated templates. Proc Natl Acad Sci USA 75:3037–3041

    Google Scholar 

  • Walker GC (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev 48:60–93

    Google Scholar 

  • Witken EM, Roegner-Maniscalio V, Sweasy JB, Sweasy JB, McCall JO (1987) Recovery from ultraviolet light-induced inhibition of DNA synthesis requires umuDC gene products in recA718 mutant strains but not in recA+ strains of Escherichia coli. Proc Natl Acad Sci USA 84:6805–6809

    Google Scholar 

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Author notes

  1. Meera Verma

    Present address: Bresatec ltd., Adelaide, South Australia

Authors and Affiliations

  1. Department of Biochemistry, University of Adelaide, 5000, Adelaide, S.A., Australia

    Meera Verma, Kevin G. Moffat & J. Barry Egan

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  1. Meera Verma
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  2. Kevin G. Moffat
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  3. J. Barry Egan
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Communicated by R. Devoret

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Verma, M., Moffat, K.G. & Egan, J.B. UV irradiation inhibits initiation of DNA replication from oriC in Escherichia coli . Mol Gen Genet 216, 446–454 (1989). https://doi.org/10.1007/BF00334389

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  • DOI: https://doi.org/10.1007/BF00334389

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