Skip to main content
SpringerLink
Log in

DNA lesions that block DNA replication are responsible for the dnaA induction caused by DNA damage

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

The initiation protein DnaA of Escherichia coli regulates its own expression autogenously by binding to a 9 by consensus sequence, the dnaA box, between the promoters dnaAP1 and dnaAP2. In this study, we analysed dnaA regulation in relation to DNA damage and found dnaA expression to be inducible by DNA lesions that inhibit DNA replication. On the other hand, coding DNA lesions were not able to induce dnaA expression. These results suggest that an additional regulatory mechanism is involved in dnaA gene expression and that DnaA protein may play a role in cellular responses to DNA damage. Furthermore, they strongly suggest that in response to DNA replication inhibition by DNA damage, and enhanced (re)initiation capacity is induced by oriC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Atlung T, Clausen E, Hansen F (1985) Autoregulation of the dnaA gene of E. coli. Mol Gen Genet 200:442–450

    Google Scholar 

  • Atlung T, Loebner-Olesen A, Hansen F (1987) Overproduction of DnaA protein stimulates initiation of chromosome and minichromosome replication in E. coli. Mol Gen Genet 206:51–59

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Bonner C, Hays S, McEntee K, Goodman M (1990) DNA polymerase II is encoded by the DNA damage-inducible dinA gene of E. coli. Proc Natl Acad Sci USA 87:7663–7667

    Google Scholar 

  • Bramhill D, Kornberg A (1988) A model for initiation at origins of replication. Cell 54:915–918

    Google Scholar 

  • Braun R, O'Day K, Wright A (1985) Autoregulation of the DNA replication gene dnaA in E. coli. Cell 40:159–169

    Google Scholar 

  • Casaregola S, Khidhir M, Holland B (1987) Effects of modulation of RNase H production on recovery of DNA synthesis following UV irradiation in E. coli. Mol Gen Genet 209:494–498

    Google Scholar 

  • Chiaramello A, Zyskind J (1989) Expression of the dnaA and mioC genes as a function of growth rate. J Bacteriol 171:4272–4280

    Google Scholar 

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

    Google Scholar 

  • Doudney C (1973) Rifampicin limitation of DNA synthesis in UV damaged bacteria. Biochim Biophys Acta 312:243–247

    Google Scholar 

  • Fuller R, Kaguni J, Kornberg A (1981) Enzymatic replication of the origin of the E. coli chromosome. Proc Natl Acad Sci USA 78:7370–7374

    Google Scholar 

  • Fuller R, Funell B, Kornberg A (1984) The dnaA protein complex with the E. coli chromosomal origin and other sites. Cell 38: 889–900

    Google Scholar 

  • Friedberg E (1985) DNA repair. WH Freemanand Company, New York

    Google Scholar 

  • Hansen E, Hansen F, von Meyenburg K (1982) The nucleotide sequence of the dnaA gene and the firt part of the dnaN gene of E. coli. Nucleic Acids Res 10:7373–7385

    Google Scholar 

  • Hansen F, Christensen B, Atlung T, Kohiyama M (1991) The initiator titration model: Computer simulation of chromosome and minichromosome control. Res Microbiol, in press

  • Hirota Y, Ryter A, Jacob F (1968) Thermosensitive mutants of E. coli in the process of DNA synthesis and cellular division. Cold Spring Harbor Symp Quant Biol 33:677–693

    Google Scholar 

  • Iwasaki H, Makata A, Walker G, Shimagawa H (1990) The E. coli polB gene, which encodes DNA polymerase II, is regulated by the SOS system. J Bacteriol 172:6268–6273

    Google Scholar 

  • Jonczyk P, Hines R, Smith D (1989) The E. coli dam gene is expressed as a distal gene of a new operon. Mol Gen Genet 217:86–96

    Google Scholar 

  • Kaasch M, Kaasch J, Quiñones A (1989) Expression of the dnaN and dnaQ genes of E. coli is inducible by mitomycin C. Mol Gen Genet 219:187–192

    Google Scholar 

  • Kaguni J, Kornberg A (1984) Replication initiated at the origin (oriC) of the E. coli chromosome reconstituted with purified enzymes. Cell 38:183–190

    Google Scholar 

  • Kenyon C, Walker G (1980) DNA damaging agents stimulate gene expression at specific loci in E. coli. Proc Natl Acad Sci USA 77:2819–2823

    Google Scholar 

  • Khidhir M, Casaregola S, Holland B (1985) Mechanism of transient inhibition of DNA synthesis in UV 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 

  • Kornberg A (1988) DNA replication. J Biol Chem 263:1–4

    Google Scholar 

  • Kücherer C, Lother H, Schauzu M, Messer W (1986) Regulation of transcription of the chromosomal dnaA gene of E. coli. Mol Gen Genet 205:115–121

    Google Scholar 

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

    Google Scholar 

  • Loebner-Olesen A, Skarstad K, Jansen F, von Meyenburg K, Boye E (1989) The DnaA protein determines the initiation mass of E. coli. Cell 57:881–889

    Google Scholar 

  • Lother H, Kölling R, Kücherer C, Schauzu M (1985) Initiation of replication in E. coli involves dnaA protein regulated transcription within the replication origin. EMBO J 4:555–560

    Google Scholar 

  • Mahaffy J, Zyskind J (1989) A model for the initiation of replication in E. coli. J Theor Biol 140:453–477

    Google Scholar 

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

    Google Scholar 

  • Masters M, Paterson T, Popplewell A, Owen T, Pringle J, Begg K (1989) Effect of DnaA protein levels and the rate of initiation at oriC on transcription originating in the ftsQ and ftsA genes: In vivo experiments. Mol Gen Genet 216:475–483

    Google Scholar 

  • Messer W, Seufert W, Schaefer C, Gielow A, Hartmann H, Wende M (1988) Functions of the DnaA protein of E. coli in replication and transcription. Biochim Biophys Acta 951:351–358

    Google Scholar 

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

    Google Scholar 

  • Pierucci O, Helmstetter C, Rickert M, Weinberger M, Leonard A (1987) Overexpression of the dnaA gene in E. coli B/r: Chromosome and minichromosome replication in the presence of rifampicin. J Bacteriol 169:1871–1877

    Google Scholar 

  • Polaczek P, Wright A (1990) Regulation of expression of the dnaA gene in E. coli: Role of the two promoters and the DnaA box. New Biologist 2:574–582

    Google Scholar 

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

    Google Scholar 

  • Quiñones A, Kaasch J, Kaasch M, Messer W (1989) Induction of dnaN and dnaQ gene expression in E. coli by alkylation damage to DNA. EMBO J 8:587–593

    Google Scholar 

  • Quiñones A, Jütterbock WR, Messer W (1991) Expression of the dnaA gene of E. coli is inducible by DNA damage. Mol Gen Genet 227:9–16

    Google Scholar 

  • Rokeach L, Chiaramello A, Junker D, Crain K, Nourani A, Jannatipour M, Zyskind J (1986) Effects of DnaA protein on replication and transcription events at the E. coli origin of replication. UCLA Symp Mol Cell Biol 47:415–217

    Google Scholar 

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

    Google Scholar 

  • Sakakibara Y, Yuasa S (1982) Continuous synthesis of the dnaA gene product of E. coli in the cell cycle. Mol Gen Genet 186:87–94

    Google Scholar 

  • Sassanfar M, Roberts J (1990) Nature of the SOS-inducing signal in E. coli. The involvement of DNA replication. J Mol Biol 212:79–96

    Google Scholar 

  • Schaefer C, Messer W (1988) Termination of the E. coli asnC transcript. The DnaA protein/dnaA box complex blocks transcribing RNA polymerase. Gene 73:347–354

    Google Scholar 

  • Schaefer C, Messer W (1989) Directionalty of DnaA protein DNA interaction. Active orientation of the DnaA protein/DnaA box complex in transcription termination. EMBO J 8:1609–1613

    Google Scholar 

  • Schaefer C, Holz A, Messer W (1991) DnaA protein mediated transcription termination in the gua operon of E. coli. Bull Inst Pasteur, in press

  • Schauzu MA, Kücherer C, Kölling R, Messer W, Lother H (1987) Transcripts within the replication origin, oriC, of Escherichia coli. Nucleic Acids Res 15:2479–2497

    Google Scholar 

  • Sekimizu K, Bramhill D, Kornberg A (1988a) Sequential early stages in the in vivo initiation of replication at the origin of the E. coli chromosome. J Biol Chem 263:7124–7130

    Google Scholar 

  • Sekimizu K, Yung B, Kornberg A (1988b) The DnaA protein of E. coli. Abundance, improved purification and membrane binding. J Biol Chem 263:7136–7140

    Google Scholar 

  • Singer B, Kusmierek T (1982) Chemical mutagenesis. Annu Rev Biochem 52:655–693

    Google Scholar 

  • Skarstad K, Loebner-Olesen A, Atlund T, von Meyenburg K, Boye E (1989) Initiation of DNA replication in E. coli after overproduction of the DnaA protein. Mol Gen Genet 218:50–56

    Google Scholar 

  • Verma M, Moffat K, Egan B (1989) UV irradiation inhibits initiation of DNA replication from oriC in E. coli. Mol Gen Genet 216:446–454

    Google Scholar 

  • von Meyenburg K, Hansen F, Riise E, Bergmans H, Meijer M, Messer W (1979) Origin of replication, oriC, of the E. coli chromosome: Genetic mapping and minichromosome replication. Cold Spring Harbor Symp Quant Biol 43:121–128

    Google Scholar 

  • Walker G (1984) Mutagenesis and inducible responses to DNA damage in E. coli. Microbiol Rev 48:60–93

    Google Scholar 

  • Wang Q, Kagumi J (1987) Transcriptional repression of the dnaA gene of E. coli by DnaA protein. Mol Gen Genet 209:518–525

    Google Scholar 

  • Wang Q, Kaguni J (1989) DnaA protein regulates transcription of the rpoH gene of E. coli. J Biol Chem 264:7338–7344

    Google Scholar 

  • Witkin E, Kogoma T (1984) Involvement of the activated form of RecA protein in SOS mutagenesis and stable replication in E. coli. Proc Natl Acad Sci USA 81:7539–7543

    Google Scholar 

  • Witkin E, Roegner-Maniscalco V, Sweasy J, McCall O (1987) Recovery from UV induced inhibition of DNA synthesis requires umuDC gene products in recA718 mutant strains but not in recA+ strains of E. coli. Proc Natl Acad Sci USA 84:6805–6809

    Google Scholar 

  • Xu Y, Bremer H (1988) Chromosome replication in E. coli induced by oversupply of DnaA. Mol Gen Genet 211:138–142

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Genetik, Martin-Luther-Universität, Domplatz 1, O-4020, Halle/S., Germany

    Ariel Quiñones

  2. Max-Planck-Institut für Molekulare Genetik, Ihnestrasse 73, W-1000, Berlin 33, Germany

    Wolf-Rainer Jueterbock & Walter Messer

Authors
  1. Ariel Quiñones
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wolf-Rainer Jueterbock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Walter Messer
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by R. Devoret

Rights and permissions

Reprints and permissions

About this article

Cite this article

Quiñones, A., Jueterbock, WR. & Messer, W. DNA lesions that block DNA replication are responsible for the dnaA induction caused by DNA damage. Molec. Gen. Genet. 231, 81–87 (1991). https://doi.org/10.1007/BF00293825

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00293825

Key words

Search

Navigation