Skip to main content
Log in

An adaptive response of E. coli to low levels of alkylating agent: Comparison with previously characterised DNA repair pathways

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

Summary

We have described previously an inducible response in Escherichia coli which occurs during growth on low levels of the methylating agent, N-methyl-N′-nitro-N-nitrosoguanidine (MNNG), and which enables cells both to survive better and to be less mutated by a subsequent challenge dose of MNNG than control cultures (Samson and Cairns, 1977). We show here that this response is distinct from previously characterised pathways of DNA repair, and particularly from the SOS response, which is another inducible effect resulting from DNA damage. An examination of the cross-reactivity of this response with other mutagens has shown that it is a generalised mechanism affecting alkylation damage to DNA. It cannot, however, be induced by UV or the UV-mimetic mutagen, 4-nitroquinoline 1-oxide, nor act on lesions put into DNA by those mutagens.

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

Access this article

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

  • Braun, A., Grossman, L.: An endonuclease from Escherichia coli that acts preferentially on UV-irradiated DNA and is absent from the uvrA and uvrB mutants. Proc. nat. Acad. Sci. (Wash.) 71, 1838–1842 (1974)

    Google Scholar 

  • Bridges, B.A., Mottershead, R.P., Rothwell, A.M., Green, M.H.L.: Repair deficient bacterial strains suitable for mutagenicity screening: tests with the fungicide captan. Chem-biol. Interact. 5, 77–84 (1972)

    Google Scholar 

  • Boyce, R.P., Howard-Flanders, P.: Release of ultraviolet-light induced Thymine dimers from DNA in E. coli K12. Proc. nat. Acad. Sci. (Wash.) 51, 293–300 (1964)

    Google Scholar 

  • Brooks-Low, K.: Formation of merodiploids in matings with a class of rec-recipient strains of E. coli K12. Proc. nat. Acad. Sci. (Wash.) 60, 160–167 (1968)

    Google Scholar 

  • Clark, A.J., Margulies, A.D.: Isolation and characterisation of recombination deficient mutants of Escherichia coli. Proc. nat. Acad. Sci. (Wash.) 53, 451–459 (1965)

    Google Scholar 

  • Defais, M., Caillet-Fauquet, P., Fox, M.S., Radman, M.: Induction kinetics of mutagenic DNA repair activity in Escherichia coli following ultraviolet irradiation. Molec. gen. Genet. 148, 125–130 (1976)

    Google Scholar 

  • Defais, M., Fauquet, P., Radman, M., Errera, M.: Ultraviolet reactivation and ultraviolet mutagenesis of α different genetic systems. Virology 43, 495–503 (1971)

    Google Scholar 

  • Guerola, N., Cerdá-Olmedo, E.: Distribution of mutations by ethyl methanesulphonate and ultraviolet radiation in the Escherichia coli chromosome. Mutation Res. 29, 145–147 (1975)

    Google Scholar 

  • Guerola, N., Ingraham, J.L., Cerdá-Olmedo, E.: Induction of closely linked multiple mutations by nitrosoguanidine. Nature (Lond.) New Biol. 230, 122–125 (1971)

    Google Scholar 

  • Hill, R.F.: Ultraviolet-induced lethality and reversion to prototropy in Escherichia coli strains with normal and reduced dark repair ability. Photochem. and Photobiol. 4, 563–568 (1965)

    Google Scholar 

  • Hince, T.A., Neale, S.: A comparison of the mutagenic action of the methyl and ethyl derivatives of nitrosamides and nitrosamidines on Escherichia coli. Mutation Res. 24, 383–387 (1974)

    Google Scholar 

  • Howard-Flanders, P., Boyce, R.P., Theriot, L.: Three loci in Escherichia coli K12 that control the excision of pyrimidine dimers and certain other mutagen product from DNA. Genetics 53, 1119–1136 (1966a)

    Google Scholar 

  • Howard-Flanders, P., Theriot, L.: Mutants of Escherichia coli K12 defective in DNA repair and in genetic recombination. Genetics 53, 1137–1150 (1966b)

    Google Scholar 

  • Ishii, Y., Kondo, S.: Comparative analysis of deletion and base change mutabilities of Escherichia coli B strains differing in DNA repair capacity (wild-type, uvrA, polA, recA) by various mutagens. Mutation Res. 27, 27–44 (1975)

    Google Scholar 

  • Kirtikar, D.M., Cathcart, G.R., Goldthwait, D.A.: Endonuclease II, apurinic acid endonuclease and exonuclease III. Proc. nat. Acad. Sci. (Wash.) 73, 4324–4328 (1976)

    Google Scholar 

  • Kirtikar, D.M., Goldthwait, D.A.: The enzymatic release of 06 methyl guanine and 3-methyl adenine from DNA reacted with the carcinogen N-methyl-N-nitrosourea. Proc. nat. Acad. Sci. (Wash.) 71, 2022–2026 (1974)

    Google Scholar 

  • Kondo, S., Ichikawa, H., Kazuhiro, I., Kato, T.: Base-change mutagenesis and prophage induction in strains of Escherichia coli with different DNA repair capacities. Genetics 66, 187–217 (1970)

    Google Scholar 

  • Lawley, P.D.: Some chemical aspects of dose response relationships in alkylation mutagenesis. Mutation Res. 23, 283–295 (1974)

    Google Scholar 

  • Ljungquist, S., Lindahl, L., Howard-Flanders, P., Methyl methane sulphonate sensitive mutant of Escherichia coli deficient in an endonuclease specific for apurinic site in deoxyribonucleic acid. J. Bact. 126, 646–653 (1976)

    Google Scholar 

  • Miller, J.H.: Experiments in Molecular Genetics. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press, 1972

    Google Scholar 

  • Moreau, P., Devoret, R.: Potential carcinogens tested by induction and mutagenesis of prophage λ in Escherichia coli K12. In: Origins of human cancer (J.P. Watson and H. Hiatt, eds.). New York: Cold Spring Harbor Laboratory 1977 (in press)

    Google Scholar 

  • Mount, D.L.: Isolation and genetic analysis of a strain of Escherichia coli K12 with an amber recA mutation. J. Bact. 107, 388–389 (1971)

    Google Scholar 

  • Nestmann, E.R.: Mutagenesis by nitrosoguanidine, ethyl methane sulphonate and mutator gene mutH in continuous cultures of Escherichia coli. Mutation Res. 28, 323–330 (1975)

    Google Scholar 

  • Radman, M.: SOS repair hypothesis: Phenomenology of an inducible DNA repair which is accompanied by mutagenesis. In: Molecular mechanism for repair of DNA (P. Hanawalt and R.B. Setlow, eds.), Part A, pp 355–367. New York: Plenum Press, 1975

    Google Scholar 

  • Radman, M., Villani, G., Boiteux, S., Defais, M., Caillet-Fauquet, P., Spadari, S.: On the mechanism and control of mutagenesis due to carcinogenic mutagens. In: Origins of human cancer (J.P. Watson and H. Hiatt, eds.), New York: Cold Spring Harbor Laboratory 1977. In press.

    Google Scholar 

  • Samson, L., Cairns, J.: A New Pathway for DNA Repair in Escherichia coli. Nature (Lond.) 267, 281–283 (1977)

    Google Scholar 

  • Singer, B.: All oxygens in nucleic acids react with carcinogenic ethylating agents. Nature (Lond.) 264, 333–339 (1976)

    Google Scholar 

  • Strauss, B., Scudiero, D., Henderson, E.: The nature of the alkylation lesions in mammalian cells. In: Molecular mechanisms for repair of DNA (P. Hanawalt and R.B. Setlow, eds.). Part A, pp. 13–24, New York: Plenum Press 1975

    Google Scholar 

  • Weigle, J.J.: Induction of mutation in a bacterial virus. Proc. nat. Acad. Sci. (Wash.) 39 628–636 (1953)

    Google Scholar 

  • Willetts, N.S., Clark, A.J.: Characteristics of some multiply recombination-deficient strains of Escherichia coli. J. Bact. 100, 231–239 (1969)

    Google Scholar 

  • Witkin, E.M.: Thermal enhancement of ultraviolet mutability in a tif uvrA derivative of Escherichia coli B/r: Evidence that ultraviolet mutagenesis depends upon an inducible function. Proc. natl. Acad. Sci. (Wash.) 71, 1930–1934 (1974)

    Google Scholar 

  • Witkin, E.M.: Persistance and decay of thermoinducible errorprone repair activity in non-filamentous derivatives of tif1 Escherichia coli B/r: The timing of some critical events in ultraviolet mutagenesis. Molec. gen. Genet. 142, 87–103 (1975)

    Google Scholar 

  • Witkin, E.M.: Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bact. Rev. 40, 869–907 (1976)

    Google Scholar 

  • Witkin, E.M., George, D.L.: Ultraviolet mutagenesis in polA and uvrA derivatives of E. coli B/r: evidence for an inducible errorprone repair system. Genetics. Suppl. 73, 91–108 (1973)

    Google Scholar 

  • Yajko, D.M., Weiss, B.: Mutation simultaneously affecting endonuclease II and exonuclease III in Escherichia coli. Proc. nat. Acad. Sci. (Wash.) 72, 688–692 (1975)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by B.A. Bridges

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jeggo, P., Defais, M., Samson, L. et al. An adaptive response of E. coli to low levels of alkylating agent: Comparison with previously characterised DNA repair pathways. Molec. Gen. Genet. 157, 1–9 (1977). https://doi.org/10.1007/BF00268680

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00268680

Keywords

Navigation