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. 1981 Dec;148(3):782–787. doi: 10.1128/jb.148.3.782-787.1981

Enhancement of ribosomal ribonucleic acid synthesis by deoxyribonucleic acid gyrase activity in Escherichia coli.

B A Oostra, A J van Vliet, G Ab, M Gruber
PMCID: PMC216275  PMID: 6171557

Abstract

The effect of the deoxyribonucleic acid (DNA) gyrase inhibitors coumermycin A1, novobiocin, and oxolinic acid on ribonucleic acid (RNA) synthesis in Escherichia coli was studied in vivo and in vitro. Preferential inhibition of ribosomal RNA (rRNA) synthesis was observed. No effect of oxolinic acid and coumermycin on rRNA synthesis was seen in mutants having a DNA gyrase which is resistant to these inhibitors. In a temperature-sensitive DNA gyrase mutant rRNA synthesis was decreased at nonpermissive temperatures. Thus, a functional DNA gyrase is required for rRNA synthesis. Purified DNA gyrase had no effect on rRNA synthesis in a purified system. However, DNA gyrase does show preferential stimulation of rRNA synthesis in a system supplemented with other proteins. Apparently, DNA gyrase stimulation of rRNA synthesis requires another protein.

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Selected References

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

  1. Botchan P. An electron microscopic comparison of transcription on linear and superhelical DNA. J Mol Biol. 1976 Jul 25;105(1):161–176. doi: 10.1016/0022-2836(76)90201-1. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Cozzarelli N. R. The mechanism of action of inhibitors of DNA synthesis. Annu Rev Biochem. 1977;46:641–668. doi: 10.1146/annurev.bi.46.070177.003233. [DOI] [PubMed] [Google Scholar]
  5. De Wyngaert M., Hinkle D. C. Involvement of DNA gyrase in replication and transcription of bacteriophage T7 DNA. J Virol. 1979 Feb;29(2):529–535. doi: 10.1128/jvi.29.2.529-535.1979. [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. Falco S. C., Zivin R., Rothman-Denes L. B. Novel template requirements of N4 virion RNA polymerase. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3220–3224. doi: 10.1073/pnas.75.7.3220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. 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]
  11. Giorno R., Stamato T., Lydersen B., Pettijohn D. Transcription in vitro of DNA in isolated bacterial nucleoids. J Mol Biol. 1975 Aug 5;96(2):217–237. doi: 10.1016/0022-2836(75)90344-7. [DOI] [PubMed] [Google Scholar]
  12. Itoh T., Tomizawa J. I. Involvement of DNA gyrase in bacteriophage T7 DNA replication. Nature. 1977 Nov 3;270(5632):78–80. doi: 10.1038/270078a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Kubo M., Kano Y., Nakamura H., Nagata A., Imamoto F. In vivo enhancement of general and specific transcription in Escherichia coli by DNA gyrase activity. Gene. 1979 Oct;7(2):153–171. doi: 10.1016/0378-1119(79)90030-1. [DOI] [PubMed] [Google Scholar]
  15. Mirkin S. M., Bogdanova E. S., Gorlenko Z. M., Gragerov A. I., Larionov O. A. DNA supercoiling and transcription in Escherichia coli: influence of RNA polymerase mutations. Mol Gen Genet. 1979;177(1):169–175. doi: 10.1007/BF00267267. [DOI] [PubMed] [Google Scholar]
  16. Oostra B. A., Ab G., Gruber M. Specific stimulation of ribosomal RNA synthesis in E. coli by a protein factor. Mol Gen Genet. 1980 Jan;177(2):291–295. doi: 10.1007/BF00267441. [DOI] [PubMed] [Google Scholar]
  17. Oostra B. A., Gruber M. Involvement of DNA gyrase in the transcription of ribosomal RNA. Nucleic Acids Res. 1980 Sep 25;8(18):4235–4246. doi: 10.1093/nar/8.18.4235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Oostra B. A., Zantinge B., van Goor A. L., van Ooyen A. J., Gruber M. A rapid and sensitive determination of bacterial rRNA by means of hybridization-competition. Anal Biochem. 1976 Aug;74(2):496–502. doi: 10.1016/0003-2697(76)90231-1. [DOI] [PubMed] [Google Scholar]
  19. Oostra B. A., van Ooyen A. J., Gruber M. In vitro transcription of three different ribosomal RNA cistrons of E. coli; heterogeneity of control regions. Mol Gen Genet. 1977 Mar 28;152(1):1–6. doi: 10.1007/BF00264932. [DOI] [PubMed] [Google Scholar]
  20. Richardson J. P. Initiation of transcription by Escherichia coli RNA polymerase from supercoiled and non-supercoiled bacteriophage PM2 DNA. J Mol Biol. 1975 Feb 5;91(4):477–487. doi: 10.1016/0022-2836(75)90274-0. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Saucier J. M., Wang J. C. Angular alteration of the DNA helix by E. coli RNA polymerase. Nat New Biol. 1972 Oct 11;239(93):167–170. doi: 10.1038/newbio239167a0. [DOI] [PubMed] [Google Scholar]
  23. Shuman H., Schwartz M. The effect of nalidixic acid on the expression of some genes in Escherichia coli K-12. Biochem Biophys Res Commun. 1975 May 5;64(1):204–209. doi: 10.1016/0006-291x(75)90239-9. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Sinden R. R., Pettijohn D. E. Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. Proc Natl Acad Sci U S A. 1981 Jan;78(1):224–228. doi: 10.1073/pnas.78.1.224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Wahle E., Mueller K. Involvement of DNA gyrase in rRNA synthesis in vivo. Mol Gen Genet. 1980;179(3):661–667. doi: 10.1007/BF00271755. [DOI] [PubMed] [Google Scholar]
  29. Wang J. C. Interactions between twisted DNAs and enzymes: the effects of superhelical turns. J Mol Biol. 1974 Aug 25;87(4):797–816. doi: 10.1016/0022-2836(74)90085-0. [DOI] [PubMed] [Google Scholar]
  30. Wells R. D., Goodman T. C., Hillen W., Horn G. T., Klein R. D., Larson J. E., Müller U. R., Neuendorf S. K., Panayotatos N., Stirdivant S. M. DNA structure and gene regulation. Prog Nucleic Acid Res Mol Biol. 1980;24:167–267. doi: 10.1016/s0079-6603(08)60674-1. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. van Ooyen A. J., de Boer H. A., Ab G., Gruber M. Specific inhibition of ribosomal RNA synthesis in vitro by guanosine 3' diphosphate, 5' diphosphate. Nature. 1975 Apr 10;254(5500):530–531. doi: 10.1038/254530a0. [DOI] [PubMed] [Google Scholar]

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