Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

DNA synthesis and degradation in UV-irradiated toluene treated cells of E. coli K12: The role of polynucleotide ligase

  • 26 Accesses

  • 8 Citations

Summary

Toluene treated cells have been used to study the processes of DNA synthesis and DNA degradation in ultra-violet irradiated Escherichia coli K12. Synthesis and degradation are both shown to occur extensively if polynucleotide ligase is inhibited, and to occur to a much lesser extent if ligase activity is optimal. Extensive UV-induced DNA synthesis in toluene-treated cells requires ATP for the initial incision step, and DNA polymerase I. Extensive degradation also depends on the early ATP-dependent incision step, and the subsequent degradation shows a partial requirement for ATP. Curtailment of degradation by ligase requires DNA polymerase activity, but is not dependent upon DNA polymerase I. Apparently this process can be carried out with equal facility by either DNA polymerase II or polymerase III. These observations suggest that extensive DNA polymerase I-dependent repair synthesis and extensive DNA degradation are facets of two divergent pathways of excision repair, both of which depend upon the early uvrABC determined ATP-dependent incision step.

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

References

  1. Billen, D., Hellerman, G.R.: Role of deoxyribonucleic acid polymerases and deoxyribonucleic acid ligase in X-ray-induced repair synthesis in toluene treated Escherichia coli K12. J. Bact. 126, 785–793 (1976)

  2. Billen, D., Hellerman, G.R., Stallions, D.R.: Role for deoxyribonucleic acid ligase in deoxyribonucleic acid polymerase-I dependent repair synthesis in toluene treated Escherichia coli. J. Bact. 124, 585–588 (1975)

  3. Boyle, J.M., Paterson, M.C., Setlow, R.B.: Excision repair properties of an Escherichia coli mutant deficient in DNA polymerase. Nature (Lond.) 226, 708–710 (1970)

  4. Campbell, J.L., Soll, L., Richardson, C.C.: Isolation and partial characterization of a mutant of Escherichia coli deficient in DNA polymerase II. Proc. nat. Acad. Sci. (Wash.) 69, 2090–2094 (1972)

  5. Cooper, P.: Excision repair in mutants of Escherichia coli deficient in DNA polymerase I and/or its associated 5′→3′ exonuclease. Molec. gen. Genet. 150, 1–12 (1977)

  6. Cooper, P.K., Hanawalt, P.C.: Role of DNA polymerase I and the rec system in excision repair in E. coli. Proc. nat. Acad. Sci. (Wash.) 69, 1156–1160 (1972a)

  7. Cooper, P.K., Hanawalt, P.C.: Heterogeneity of patch size in repair replicated DNA in Escherichia coli. J. molec. Biol. 67, 1–10 (1972b)

  8. De Lucia, P., Cairns, J.: Isolation of an Escherichia coli strain with a mutation affecting DNA polymerase. Nature (Lond.) 224, 1164–1166 (1969)

  9. Deutsch, W.A., Dorson, J.W., Moses, R.E.: Excision of pyrimidine dimers in toluene treated Escherichia coli. J. Bact. 125, 220–224 (1976)

  10. Glickman, B.W.: The role of DNA polymerase I in pyrimidine dimer excision and repair replication in Escherichia coli K12 following ultraviolet irradiation. Biochim. biophys. Acta (Amst.) 335, 115–122 (1974)

  11. Glickman, B.W.: The role of DNA polymerase I in excision repair. In: Molecular mechanisms of DNA repair (P.C. Hanawalt and R.B. Setlow, eds.), pp. 213–218. New York: Plenum Press 1975.

  12. Glickman, B.W., van Sluis, C.A., Heijneker, H.L., Rörsch, A.: A mutant of Escherichia coli K12 deficient in the 5′→3′ exonucleolytic activity of DNA polymerase I.I. General Characterization. Molec. gen. Genet. 124, 69–82 (1973)

  13. Goldmark, P.J., Linn, S.: Purification and properties of the recBC DNase of Escherichia coli K 12. J. biol. Chem. 247, 1849–1860 (1972)

  14. Gottesman, M.M., Hicks, M., Gellert, M.: Genetics and function of DNA ligase in Escherichia coli. J. molec. Biol. 77, 531–547 (1973)

  15. Grossman, L., Braun, A., Feldberg, R., Mahler, I.: Enzymatic repair of DNA. Ann. Rev. Biochem. 44, 19–43 (1975)

  16. Hamelin, C., Youngs, D.A., Smith K.C.: Role of deoxyribonucleic acid polymerase III in the repair of single-strand breaks produced in Escherichia coli deoxyribonucleic acid by gamma radiation. J. Bact. 127, 1307–1314 (1976)

  17. Hanawalt, P.C.: Molecular mechanisms involved in DNA repair. Genetics 79, 179–197 (1975)

  18. Hirota, Y., Gefter, M., Mindich, L.: A mutant of Escherichia coli defective in DNA polymerase II activity. Proc. nat. Acad. Sci. (Wash.) 69, 3238–3242 (1972)

  19. Howard-Flanders, P., Theriot, L.: Mutants of Escherichia coli K 12 defective in DNA repair and genetic recombination. Genetics 53, 1137–1150 (1966)

  20. Kelly, R.B., Atkinson, M.R., Huberman, J.A., Kornberg, A.: Excision of thymine dimers and other mismatched sequences by DNA polymerase of Escherichia coli. Nature (Lond.) 224, 495–501 (1969)

  21. Lakchaura, B.D., Fossum, T., Jagger, J.: Inactivation of adenosine 5′-triphosphate synthesis and reduced-form nicotinamide adenine dinucleotide dehydrogenase activity in Escherichia coli by near-ultraviolet and violet radiations. J. Bact. 125, 111–118 (1976)

  22. Lehman, I.R., Chien, J.R.: Persistence of deoxyribonucleic acid polymerase I and its 5′→3′ exonuclease activity in polA mutants of Escherichia coli K 12. J. biol. Chem. 248, 7717–7723 (1973)

  23. Little, J.W., Zimmerman, S.B., Oshinsky, C.K., Gellert, M.: Enzymatic joining of DNA strands. II. An enzyme-adenylate intermediate in the DPN-dependent DNA ligase reaction. Proc. nat. Acad. Sci. (Wash.) 58, 2004–2011 (1967)

  24. Masamune, Y., Richardson, C.C.: Strand displacement during deoxyribonucleic acid synthesis at single strand breaks. J. biol. Chem. 246, 2692–2701 (1971)

  25. Masker, W.E.: The ATP dependence of the incision and resynthesis steps of excision repair. Biochim. biophys. Acta (Amst.) 442, 162–173 (1976)

  26. Masker, W.E., Hanawalt, P.C.: Nucleoside triphosphate dependence of repair replication in toluenized Escherichia coli. J. molec. Biol. 88, 13–23 (1974)

  27. Masker, W.E., Simon, T.J., Hanawalt, P.C., Repair replication in permeablized Escherichia coli. In: Molecular mechanisms of DNA repair (P.C. Hanawalt and R.B. Setlow, eds.), pp. 245–254. New York: Plenum Press 1975

  28. Moses, R.E., Moody, E.E.M.: DNA repair synthesis dependent on the uvrA,B gene products in toluene treated cells. J. biol. Chem. 250, 8055–8061 (1975)

  29. Moses, R.E., Richardson, C.C.: Replication and reapair of DNA in cells of Escherichia coli treated with toluene. Proc. nat. Acad. Sci. (Wash.) 67, 674–681 (1970)

  30. Rama Reddy, G.V., Goulian, M., Hendler, S.S.: Inhibition of E. coli DNA polymerase II by Ara-CTP. Nature (Lond.) New Biol. 234, 286–288 (1971)

  31. Seeberg, E., Nissen-Meyer, J., Strike, P.: Incision of ultraviolet irradiated DNA by extracts of E. coli requires three different gene products. Nature (Lond.) 263, 524–526 (1976)

  32. Seeberg, E., Rupp, W.D.: Effect of mutations in lig and polA on UV-induced strand cutting in a uvrC strain of Escherichia coli. In: Molecular mechanisms of DNA repair (P.C. Hanawalt and R.B. Setlow, eds.), pp. 439–442. New York: Plenum Press 1975

  33. Seeberg, E., Strike, P.: Excision repair of ultraviolet-irradiated deoxyribonucleic acid in plasmolyzed cells of Escherichia coli. J. Bact. 125, 787–795 (1976)

  34. Sharon, R., Miller, C., Ben-Ishai, R.: Two modes of excision repair in toluene treated Escherichia coli. J. Bact. 123, 1107–1114 (1975)

  35. Strike, P., Emmerson, P.T.: Degradation of DNA following ultraviolet irradiation of Escherichia coli K 12 mutants lacking DNA polymerase I and Exonuclease V. Molec. gen. Genet. 130, 39–45 (1974)

  36. Swenson, P.A.: Physiological responses of Escherichia coli to farultraviolet radiation. Photochem. Photobiol. Rev. (K.C. Smith, ed.) 1, 269–387 (1976)

  37. Tait, R.C., Harris, A.L., Smith, D.W.: DNA repair in Escherichia coli mutants deficient in DNA polymerases I, II and/or III. Proc. nat. Acad. Sci. (Wash.) 71, 675–679 (1974)

  38. Thielmann, H.W.: Carcinogen induced DNA repair in nucleotide permeable Escherichia coli cells. Europ. J. Biochem. 61, 501–513 (1976)

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

  40. Youngs, D.A., Smith, K.C.: Evidence for control by exrA and polA genes of two branches of the uvr gene-dependent excision repair pathway in Escherichia coli K 12. J. Bact. 116, 175–182 (1973a)

  41. Youngs, D.A., Smith, K.C.: Involvement of DNA polymerase III in excision repair after ultraviolet irradiation. Nature (Lond.) New Biol. 244, 240–241 (1973b)

  42. Zimmerman, S.B., Little, J.W., Oshinsky, C.K., Gellert, M.: Enzymatic joining of DNA strands: a novel reaction of diphosphopyridine nucleotide. Proc. nat. Acad. Sci. (Wash.) 57, 1841–1848 (1967)

Download references

Author information

Additional information

Communicated by B.A. Bridges

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Strike, P. DNA synthesis and degradation in UV-irradiated toluene treated cells of E. coli K12: The role of polynucleotide ligase. Molec. Gen. Genet. 157, 99–107 (1977). https://doi.org/10.1007/BF00268692

Download citation

Keywords

  • Ligase
  • Excision Repair
  • Polymerase Activity
  • Polynucleotide
  • Subsequent Degradation