Summary
Degradation products of restricted T4 DNA induced filamentation, mutagenesis, and to a lesser extent, synthesis of recA protein in wild type cells but not in recA, lexA or recBC mutants of Escherichia coli. We conclude that the structural damage to the DNA caused by restriction cleavage and exonuclease V degradation can induce SOS functions. Degradation of restricted nonglucosylated T4 DNA by exonuclease V delayed cell division and induced filament formation and mutagenesis in lexA + but not in lexA - cells. Delay of cell division was also dependent upon recA and recBC funtions. Such degradation of DNA also dramatically increased mutagenesis in tif - Sfi- cells at 42°C. The synthesis of recA protein continued in the restricting host after infection by the nonglucosylated T4 phage, but enhanced synthesis is not induced to the extent seen in SOS induced tif - cells grown at 42°. We also found that restriction of nonglucosylated T4 was alleviated in UV irradiated cells. The UV induced alleviation of rgl and r K restriction depended upon post irradiation protein synthesis and was not observed in recA, lexA or recBC mutants.
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References
Adams, M.H.: Bacteriophages. New York: John Wiley 1959
Barbour, S., Clark, A.J.: Biochemical and genetic studies of recombination proficiency in Eschrrichia coli. I. Enzymatic activity associated with recB + and recC + genes. Proc. Natl. Acad. Sci. U.S.A. 65, 955–961 (1970)
Bertani, G., Weigle, J.J.: Host controlled variation in bacterial viruses. J. Bacteriol. 65, 113–121 (1953)
Bridges, B.A., Rothwell, M.A., Green, M.H.L.: Repair process and dose response curves in ultraviolet mutagenesis of bacteria. An. Acad. Brasil. Ci. 45 Suppl, 203–208 (1973)
Castellazzi, M., George, J., Buttin, G.: Prophage induction and cell division in Escherichia coli. II. Linked (recA, zab) and unlinked (lex) suppressors of tif-1 mediated induction and filamentation. Mol. Gen. Genet. 119, 153–174 (1972)
Day, R.S.: UV-induced alleviation of K specific restriction of bacteriophage λ. J. Virol. 21, 1249–1251 (1977)
Dharmalingham, K., Goldberg, E.B.: Mechanism localization and control of restriction cleavage of phage T4 and λ chromosomes. Nature 260, 406–410 (1976)
Dharmalingam, K., Goldberg, E.B.: Restriction in vivo. III. General effects of glucosylation and restriction on phage T4 gene expression and replication. Virology 96, 393–403 (1979)
Doubleday, O.P., Green, M.H.L., Bridges, B.A.: Spontaneous and ultraviolet-induced mutations in Escherichia coli: Interaction between plasmid and tif-1 mutator effects. J. Gen. Microbiol. 101, 163–166 (1977)
Emmerson, P.T., West, S.C.: Identification of protein-X of E. coli as the recA + /tif + gene product. Mol. Gen. Genet. 155, 77–85 (1977)
George, J., Castellazzi, M., Buttin, G.: Prophage induction and cell division in E. coli. III. Mutations sfiA and sfiB restore division in tif and lon strains and permit the expression of mutator properties of tif. Mol. Gen. Genet. 140, 309–332 (1975)
George, J., Devoret, R., Radman, M.: Indirect ultraviolet reactivation of phage λ. Proc. Natl. Acad. Sci. U.S.A. 71, 144–147 (1974)
Georgopoulos, C.P.: Isolation and preliminary characterization of T4 mutants with non-glucosylated DNA. Biochem. Biophys. Res. Commun. 28, 179–184 (1967)
Green, M.H.L.: Appendix in Bridges, B.A.: Recent advances in basic mutation research. Mutat. Res. 44, 149–164 (1977)
Gudas, L.J., Pardee, A.B.: Model for the regulation of Escherichia coli DNA repair functions. Proc. Natl. Acad. Sci. U.S.A. 72, 2330–2334 (1975)
Gudas, L.J., Pardee, A.B.: DNA synthesis inhibition and the induction of protein-X in Escherichia coli. J. Mol. Biol. 101, 459–477 (1976)
Haberman, A., Heywood, M., Meselson, M.: DNA modification methylase activity of Escherichia coli restriction endonuclease K and P. Proc. Natl. Acad. Sci. U.S.A. 69, 3138–3141 (1972)
Kennel, D.: Inhibition of host protein synthesis during infection of Escherichia coli B by bacteriophage T4. I. Continued synthesis of host ribonucleic acid. J. Virol. 2, 1261–1271 (1968)
Lehmann, A.R., Bridges, B.A.: DNA repair. In: Essays in biochemistry (P.N. Campbell and W.N. Aldridge, eds.), Vol. 13, pp. 71–119. New York: Academic Press, Inc. 1977
Luria, S.E.: Host-induced modifications of viruses. Cold Spring Harbor Symp. Quant. Biol. 18, 237–244 (1953)
Malamy, M.H., Fiandt, M., Szybalsky, W.: Electron microscopy of polar insertions in the lac operon of Escherichia coli. Mol. Gen. Genet. 119, 207–222 (1972)
Marsden, H.S., Pollard, E.C., Ginoza, W., Randal, E.P.: Involvement of recA and exr genes in the in vivo inhibition of recBC nuclease. J. Bacteriol. 118, 465–470 (1974)
McGarva, D., Doubleday, O.P., Lehmann, A.R., Bridges, B.A.: Assays for the fidelity of DNA polymerase in cell free extracts of Escherichia coli are complicated by contaminating nucleotide triphosphatases. Biochem. Biophys. Acta 563:356–364 (1979)
Meyn, S., Rossman, T., Troll, W.: A protease inhibitor blocks SOS functions in Escherichia coli. Antipain prevents λ repressor inactivation ultraviolet mutagenesis and filamentous growth. Proc. Natl. Acad. Sci. U.S.A. 74, 1152–1156 (1977)
Oishi, M., Smith, C.L.: Inactivation of phage repressor in a permeable cell system: Role of recBC DNAse in induction. Proc. Natl. Acad. Sci. U.S.A. 75, 3569–3573 (1978)
Oliver, D.B., Goldberg, E.B.: Protection of parental T4 DNA from a restriction exonuclease by the product of gene 2. J. Mol. Biol. 116, 877–881 (1977)
Pollard, E., Randal, E.P.: Studies on the inducible inhibitor of radiation induced DNA degradation of Escherichia coli. Radiat. Res. 55, 265–279 (1973)
Radman, M.: Phenomenology of an inducible DNA repair which is accompanied by mutagenesis. In: Molecular and evironmental aspects of mutagenesis (L. Prakash, F. Sherman, M.W. Miller and H.W. Taber, eds.), pp. 128–148, Springfield: C.C. Thomas 1974
Radman, M., Villani, G., Boiteaux, S., Defais, M., Cailett-Fauquet, P., Spadari, S.: On the mechanism and genetic control of mutagenesis induced by carcinogenic mutagens. In: Origins of human cancer (H.H. Hiatt, J.D. Watson and J.A. Winstin, eds.) (Cold Spring Harbor) Book B 903–922 (1977)
Roberts, J., Roberts, C.: Proteolytic cleavage of bacteriophage λ repressor in induction. Proc. Natl. Acad. Sci. U.S.A. 72, 147–151 (1975)
Sauerbier, W.: Ultraviolet sensitivity and thymine dimerization in mutants of bacteriophage T4. Biochem. Biophys. Acta 87, 356–358 (1964)
Silverstein, J.L., Goldberg, E.B.: T4 DNA injection. II. Protection of entering DNA from host exonuclease V. Virol. 72, 212–233 (1976)
Smith, C.L., Oishi, M.: Early events and mechanisms in the induction of bacterial SOS functions: Analysis of the phage repressor inactivation process in vivo. Proc. Natl. Acad. Sci. U.S.A. 75, 1657–1661 (1978)
Sussman, R., BenZeev, H.: Proposed mechanism of bacteriophage lambda induction: Acquisition of binding sites for lambda repressor by DNA of the host. Proc. Natl. Acad. Sci. U.S.A. 72, 1973–1976 (1975)
Sussman, R., Resnick, J., Calame, K., Baluch, J.: Interaction of bacteriophage λ repressor with non operator DNA containing single-stranded gaps. Proc. Natl. Acad. Sci. U.S.A. 75, 5817–5821 (1978)
Villani, G., Boiteux, S., Radman, M.: Mechanism of ultraviolet induced mutagenesis: Extent and fidelity of in vitro DNA synthesis on irradiated templates. Proc. Natl. Acad. Sci. U.S.A. 75, 3037–3041 (1978)
Witkin, E.M.: Thermal enhancement of ultraviolet mutability in a tif-1 uvrA derivative of Escherichia coli B/r: evidence that ultraviolet mutagenesis depends upon an inducible function. Proc. Natl. Acad. Sci. U.S.A. 71, 1930–1934 (1974)
Witkin, E.M.: Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol. Rev. 40, 869–907 (1976)
Witkin, E.M.: Targetted and untargetted mutagenesis by various inducers of SOS functions in E. coli. Cold Spring Harbor Symp. Quant. Biol. 43, 881–886 (1978)
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Communicated by B.A. Bridges
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Dharmalingam, K., Goldberg, E.B. Restriction in vivo. Molec. Gen. Genet. 178, 51–58 (1980). https://doi.org/10.1007/BF00267212
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DOI: https://doi.org/10.1007/BF00267212