Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1983 May;80(9):2510–2513. doi: 10.1073/pnas.80.9.2510

recF-dependent induction of recA synthesis by coumermycin, a specific inhibitor of the B subunit of DNA gyrase.

C L Smith
PMCID: PMC393855  PMID: 6302690

Abstract

Genetic and biochemical studies on enzymes known to be involved in regulating DNA supercoiling yield a complex spectrum of effects on the Escherichia coli SOS system. Previous studies indicated that only inhibition of DNA gyrase by antibiotics that act on the DNA gyrase A subunit results in turning on the E. coli SOS system. Here we show that coumermycin, an antibiotic that acts on the DNA gyrase B subunit, can also induce. Like nalidixic acid induction, coumermycin induction is dependent on the recBC DNase. In both cases induction apparently results from a response of the cell to the DNA gyrase-inhibitor complex rather than just the loss of DNA gyrase activity. However, unlike induction by the DNA gyrase A-specific antibiotics, coumermycin induction also requires the recF gene product. This demonstrates a functional relationship between DNA gyrase and the recF gene product.

Full text

PDF
2510

Selected References

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

  1. Armengod M. E. Role of the recF gene of Escherichia coli K-12 in lambda recombination. Mol Gen Genet. 1981;181(4):497–504. doi: 10.1007/BF00428742. [DOI] [PubMed] [Google Scholar]
  2. Barbour S. D., Clark A. J. Biochemical and genetic studies of recombination proficiency in Escherichia coli. I. Enzymatic activity associated with recB+ and recC+ genes. Proc Natl Acad Sci U S A. 1970 Apr;65(4):955–961. doi: 10.1073/pnas.65.4.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Botchan P., Wang J. C., Echols H. Effect of circularity and superhelicity on transcription from bacteriophagelambda DNA. Proc Natl Acad Sci U S A. 1973 Nov;70(11):3077–3081. doi: 10.1073/pnas.70.11.3077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clark A. J. Recombination deficient mutants of E. coli and other bacteria. Annu Rev Genet. 1973;7:67–86. doi: 10.1146/annurev.ge.07.120173.000435. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Crowl R. M., Ahmed S. U., Boyce R. P. Expression of lambda red genes restores recB--dependent protein X induction in E. coli. Nature. 1978 Sep 7;275(5675):71–72. doi: 10.1038/275071a0. [DOI] [PubMed] [Google Scholar]
  7. Crumplin G. C., Smith J. T. Nalidixic acid and bacterial chromosome replication. Nature. 1976 Apr 15;260(5552):643–645. doi: 10.1038/260643a0. [DOI] [PubMed] [Google Scholar]
  8. Drlica K., Engle E. C., Manes S. H. DNA gyrase on the bacterial chromosome: possibility of two levels of action. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6879–6883. doi: 10.1073/pnas.77.11.6879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Engle E. C., Manes S. H., Drlica K. Differential effects of antibiotics inhibiting gyrase. J Bacteriol. 1982 Jan;149(1):92–98. doi: 10.1128/jb.149.1.92-98.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fairweather N. F., Orr E., Holland I. B. Inhibition of deoxyribonucleic acid gyrase: effects on nucleic acid synthesis and cell division in Escherichia coli K-12. J Bacteriol. 1980 Apr;142(1):153–161. doi: 10.1128/jb.142.1.153-161.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Filutowicz M. Requirement of DNA gyrase for the initiation of chromosome replication in Escherichia coli K-12. Mol Gen Genet. 1980 Jan;177(2):301–309. doi: 10.1007/BF00267443. [DOI] [PubMed] [Google Scholar]
  13. Gellert M. DNA topoisomerases. Annu Rev Biochem. 1981;50:879–910. doi: 10.1146/annurev.bi.50.070181.004311. [DOI] [PubMed] [Google Scholar]
  14. Gellert M., Fisher L. M., O'Dea M. H. DNA gyrase: purification and catalytic properties of a fragment of gyrase B protein. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6289–6293. doi: 10.1073/pnas.76.12.6289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. Gudas L. J., Pardee A. B. DNA synthesis inhibition and the induction of protein X in Escherichia coli. J Mol Biol. 1976 Mar 15;101(4):459–477. doi: 10.1016/0022-2836(76)90240-0. [DOI] [PubMed] [Google Scholar]
  19. Horii Z., Clark A. J. Genetic analysis of the recF pathway to genetic recombination in Escherichia coli K12: isolation and characterization of mutants. J Mol Biol. 1973 Oct 25;80(2):327–344. doi: 10.1016/0022-2836(73)90176-9. [DOI] [PubMed] [Google Scholar]
  20. Karu A. E., Belk E. D. Induction of E. coli recA protein via recBC and alternate pathways: quantitation by enzyme-linked immunosorbent assay (ELISA). Mol Gen Genet. 1982;185(2):275–282. doi: 10.1007/BF00330798. [DOI] [PubMed] [Google Scholar]
  21. Kreuzer K. N., Cozzarelli N. R. Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth. J Bacteriol. 1979 Nov;140(2):424–435. doi: 10.1128/jb.140.2.424-435.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kushner S. R., Nagaishi H., Templin A., Clark A. J. Genetic recombination in Escherichia coli: the role of exonuclease I. Proc Natl Acad Sci U S A. 1971 Apr;68(4):824–827. doi: 10.1073/pnas.68.4.824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Little J. W., Mount D. W. The SOS regulatory system of Escherichia coli. Cell. 1982 May;29(1):11–22. doi: 10.1016/0092-8674(82)90085-x. [DOI] [PubMed] [Google Scholar]
  24. Little J. W., Mount D. W., Yanisch-Perron C. R. Purified lexA protein is a repressor of the recA and lexA genes. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4199–4203. doi: 10.1073/pnas.78.7.4199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mahajan S. K., Datta A. R. Nature of recombinants produced by the RecBC and the RecF pathways in Escherichia coli. Nature. 1977 Apr 14;266(5603):652–653. doi: 10.1038/266652a0. [DOI] [PubMed] [Google Scholar]
  26. Phizicky E. M., Roberts J. W. Induction of SOS functions: regulation of proteolytic activity of E. coli RecA protein by interaction with DNA and nucleoside triphosphate. Cell. 1981 Jul;25(1):259–267. doi: 10.1016/0092-8674(81)90251-8. [DOI] [PubMed] [Google Scholar]
  27. Pisetsky D., Berkower I., Wickner R., Hurwitz J. Role of ATP in DNA synthesis in Escherichia coli. J Mol Biol. 1972 Nov 28;71(3):557–571. doi: 10.1016/s0022-2836(72)80023-8. [DOI] [PubMed] [Google Scholar]
  28. Ream L. W., Margossian L., Clark A. J., Hansen F. G., von Meyenburg K. Genetic and physical mapping of recF in Escherichia coli K-12. Mol Gen Genet. 1980;180(1):115–121. doi: 10.1007/BF00267359. [DOI] [PubMed] [Google Scholar]
  29. Roberts J. W., Roberts C. W., Craig N. L. Escherichia coli recA gene product inactivates phage lambda repressor. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4714–4718. doi: 10.1073/pnas.75.10.4714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rothman R. H., Clark A. J. The dependence of postreplication repair on uvrB in a recF mutant of Escherichia coli K-12. Mol Gen Genet. 1977 Oct 24;155(3):279–286. doi: 10.1007/BF00272806. [DOI] [PubMed] [Google Scholar]
  31. Sanzey B. Modulation of gene expression by drugs affecting deoxyribonucleic acid gyrase. J Bacteriol. 1979 Apr;138(1):40–47. doi: 10.1128/jb.138.1.40-47.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith C. L., Kubo M., Imamoto F. Promoter-specific inhibition of transcription by antibiotics which act on DNA gyrase. Nature. 1978 Oct 5;275(5679):420–423. doi: 10.1038/275420a0. [DOI] [PubMed] [Google Scholar]
  33. 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. 1978 Apr;75(4):1657–1661. doi: 10.1073/pnas.75.4.1657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Snyder M., Drlica K. DNA gyrase on the bacterial chromosome: DNA cleavage induced by oxolinic acid. J Mol Biol. 1979 Jun 25;131(2):287–302. doi: 10.1016/0022-2836(79)90077-9. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Vapnek D., Alton N. K., Bassett C. L., Kushner S. R. Amplification in Escherichia coli of enzymes involved in genetic recombination: construction of hybrid ColE1 plasmids carrying the structural gene for exonuclease I. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3492–3496. doi: 10.1073/pnas.73.10.3492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yang H. L., Heller K., Gellert M., Zubay G. Differential sensitivity of gene expression in vitro to inhibitors of DNA gyrase. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3304–3308. doi: 10.1073/pnas.76.7.3304. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES