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. 1986 Oct;168(1):276–282. doi: 10.1128/jb.168.1.276-282.1986

Effects of DNA gyrase inhibitors in Escherichia coli topoisomerase I mutants.

G J Pruss, R J Franco, S G Chevalier, S H Manes, K Drlica
PMCID: PMC213448  PMID: 3019999

Abstract

Relaxation of titratable supercoils in bacterial nucleoids was measured following treatment of topA mutants with coumermycin or oxolinic acid, inhibitors of DNA gyrase. Relaxation occurred after treatment of the mutants with either inhibitor. We detected no significant difference in relaxation between topA- and topA+ strains treated with coumermycin. This finding, together with previous observations, supports the idea that relaxation caused by coumermycin probably arises from the relaxing activity of gyrase itself. The source of DNA relaxation caused by oxolinic acid was not identified. Nucleoid supercoiling can be increased by adding oxolinic acid to a strain that carries three topoisomerase mutations: delta topA, gyrB225, and gyrA (Nalr) (S. H. Manes, G. J. Pruss, and K. Drlica, J. Bacteriol. 155:420-423, 1983). We found that this increase in supercoiling requires partial sensitivity to the drug and at the delta topA and gyrA mutations. Full resistance to oxolinic acid in the presence of the delta topA, gyrB225, and gyrA mutations was conferred by an additional mutation that maps at or near gyrB.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. CUMMINGS D. J. SEDIMENTATION AND BIOLOGICAL PROPERTIES OF T-PHAGES OF ESCHERICHIA COLI. Virology. 1964 Jul;23:408–418. doi: 10.1016/0042-6822(64)90264-8. [DOI] [PubMed] [Google Scholar]
  2. Cozzarelli N. R. DNA gyrase and the supercoiling of DNA. Science. 1980 Feb 29;207(4434):953–960. doi: 10.1126/science.6243420. [DOI] [PubMed] [Google Scholar]
  3. Dean F., Krasnow M. A., Otter R., Matzuk M. M., Spengler S. J., Cozzarelli N. R. Escherichia coli type-1 topoisomerases: identification, mechanism, and role in recombination. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):769–777. doi: 10.1101/sqb.1983.047.01.088. [DOI] [PubMed] [Google Scholar]
  4. DiNardo S., Voelkel K. A., Sternglanz R., Reynolds A. E., Wright A. Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell. 1982 Nov;31(1):43–51. doi: 10.1016/0092-8674(82)90403-2. [DOI] [PubMed] [Google Scholar]
  5. Drlica K. Biology of bacterial deoxyribonucleic acid topoisomerases. Microbiol Rev. 1984 Dec;48(4):273–289. doi: 10.1128/mr.48.4.273-289.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Drlica K., Snyder M. Superhelical Escherichia coli DNA: relaxation by coumermycin. J Mol Biol. 1978 Apr 5;120(2):145–154. doi: 10.1016/0022-2836(78)90061-x. [DOI] [PubMed] [Google Scholar]
  7. Gellert M. DNA topoisomerases. Annu Rev Biochem. 1981;50:879–910. doi: 10.1146/annurev.bi.50.070181.004311. [DOI] [PubMed] [Google Scholar]
  8. Gellert M., Menzel R., Mizuuchi K., O'Dea M. H., Friedman D. I. Regulation of DNA supercoiling in Escherichia coli. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):763–767. doi: 10.1101/sqb.1983.047.01.087. [DOI] [PubMed] [Google Scholar]
  9. Gellert M., Mizuuchi K., O'Dea M. H., Itoh T., Tomizawa J. I. Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4772–4776. doi: 10.1073/pnas.74.11.4772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gellert M., Mizuuchi K., O'Dea M. H., Nash H. A. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3872–3876. doi: 10.1073/pnas.73.11.3872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gellert M., O'Dea M. H., Itoh T., Tomizawa J. Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4474–4478. doi: 10.1073/pnas.73.12.4474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Manes S. H., Pruss G. J., Drlica K. Inhibition of RNA synthesis by oxolinic acid is unrelated to average DNA supercoiling. J Bacteriol. 1983 Jul;155(1):420–423. doi: 10.1128/jb.155.1.420-423.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McClure W. R. Mechanism and control of transcription initiation in prokaryotes. Annu Rev Biochem. 1985;54:171–204. doi: 10.1146/annurev.bi.54.070185.001131. [DOI] [PubMed] [Google Scholar]
  14. Menzel R., Gellert M. Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell. 1983 Aug;34(1):105–113. doi: 10.1016/0092-8674(83)90140-x. [DOI] [PubMed] [Google Scholar]
  15. Mirkin S. M., Zaitsev E. N., Panyutin I. G., Lyamichev V. I. Native supercoiling of DNA: the effects of DNA gyrase and omega protein in E. coli. Mol Gen Genet. 1984;196(3):508–512. doi: 10.1007/BF00436200. [DOI] [PubMed] [Google Scholar]
  16. Pruss G. J. DNA topoisomerase I mutants. Increased heterogeneity in linking number and other replicon-dependent changes in DNA supercoiling. J Mol Biol. 1985 Sep 5;185(1):51–63. doi: 10.1016/0022-2836(85)90182-2. [DOI] [PubMed] [Google Scholar]
  17. Pruss G. J., Manes S. H., Drlica K. Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell. 1982 Nov;31(1):35–42. doi: 10.1016/0092-8674(82)90402-0. [DOI] [PubMed] [Google Scholar]
  18. Raji A., Zabel D. J., Laufer C. S., Depew R. E. Genetic analysis of mutations that compensate for loss of Escherichia coli DNA topoisomerase I. J Bacteriol. 1985 Jun;162(3):1173–1179. doi: 10.1128/jb.162.3.1173-1179.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Richardson S. M., Higgins C. F., Lilley D. M. The genetic control of DNA supercoiling in Salmonella typhimurium. EMBO J. 1984 Aug;3(8):1745–1752. doi: 10.1002/j.1460-2075.1984.tb02041.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sinden R. R., Carlson J. O., Pettijohn D. E. Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: analogous measurements in insect and human cells. Cell. 1980 Oct;21(3):773–783. doi: 10.1016/0092-8674(80)90440-7. [DOI] [PubMed] [Google Scholar]
  21. Steck T. R., Pruss G. J., Manes S. H., Burg L., Drlica K. DNA supercoiling in gyrase mutants. J Bacteriol. 1984 May;158(2):397–403. doi: 10.1128/jb.158.2.397-403.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sternglanz R., DiNardo S., Voelkel K. A., Nishimura Y., Hirota Y., Becherer K., Zumstein L., Wang J. C. Mutations in the gene coding for Escherichia coli DNA topoisomerase I affect transcription and transposition. Proc Natl Acad Sci U S A. 1981 May;78(5):2747–2751. doi: 10.1073/pnas.78.5.2747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stonington O. G., Pettijohn D. E. The folded genome of Escherichia coli isolated in a protein-DNA-RNA complex. Proc Natl Acad Sci U S A. 1971 Jan;68(1):6–9. doi: 10.1073/pnas.68.1.6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sugino A., Peebles C. L., Kreuzer K. N., Cozzarelli N. R. Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4767–4771. doi: 10.1073/pnas.74.11.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Trucksis M., Depew R. E. Identification and localization of a gene that specifies production of Escherichia coli DNA topoisomerase I. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2164–2168. doi: 10.1073/pnas.78.4.2164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tse-Dinh Y. C. Regulation of the Escherichia coli DNA topoisomerase I gene by DNA supercoiling. Nucleic Acids Res. 1985 Jul 11;13(13):4751–4763. doi: 10.1093/nar/13.13.4751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wall J. D., Harriman P. D. Phage P1 mutants with altered transducing abilities for Escherichia coli. Virology. 1974 Jun;59(2):532–544. doi: 10.1016/0042-6822(74)90463-2. [DOI] [PubMed] [Google Scholar]
  28. Wang J. C. Interaction between DNA and an Escherichia coli protein omega. J Mol Biol. 1971 Feb 14;55(3):523–533. doi: 10.1016/0022-2836(71)90334-2. [DOI] [PubMed] [Google Scholar]
  29. Worcel A., Burgi E. On the structure of the folded chromosome of Escherichia coli. J Mol Biol. 1972 Nov 14;71(2):127–147. doi: 10.1016/0022-2836(72)90342-7. [DOI] [PubMed] [Google Scholar]
  30. von Wright A., Bridges B. A. Effect of gyrB-mediated changes in chromosome structure on killing of Escherichia coli by ultraviolet light: experiments with strains differing in deoxyribonucleic acid repair capacity. J Bacteriol. 1981 Apr;146(1):18–23. doi: 10.1128/jb.146.1.18-23.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

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