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. 1989 Nov;86(22):8882–8886. doi: 10.1073/pnas.86.22.8882

The unexpected antitermination of gyrA-directed transcripts is enhanced by DNA relaxation.

M Carty 1, R Menzel 1
PMCID: PMC298394  PMID: 2554334

Abstract

We show that transcription originating at the gyrA promoter of Escherichia coli is less subject to termination at the lambda Toop terminator (22% read-through) than is transcription originating from either the galOP (1% read-through) or topA (3% read-through) control regions. Furthermore, termination of the gyrA transcripts decreases (60% read-through) upon relaxation of the template DNA. We believe that events related to stimulation of transcription at the gyrA promoter by DNA relaxation are responsible for the enhanced terminator read-through.

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Selected References

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  1. Axley M. J., Stadtman T. C. Anaerobic induction of Escherichia coli formate dehydrogenase (hydrogenase-linked) is enhanced by gyrase inactivation. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1023–1027. doi: 10.1073/pnas.85.4.1023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balke V. L., Gralla J. D. Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J Bacteriol. 1987 Oct;169(10):4499–4506. doi: 10.1128/jb.169.10.4499-4506.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Borowiec J. A., Gralla J. D. Supercoiling response of the lac ps promoter in vitro. J Mol Biol. 1985 Aug 20;184(4):587–598. doi: 10.1016/0022-2836(85)90305-5. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Gellert M. DNA topoisomerases. Annu Rev Biochem. 1981;50:879–910. doi: 10.1146/annurev.bi.50.070181.004311. [DOI] [PubMed] [Google Scholar]
  6. Goldstein E., Drlica K. Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4046–4050. doi: 10.1073/pnas.81.13.4046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Goliger J. A., Yang X. J., Guo H. C., Roberts J. W. Early transcribed sequences affect termination efficiency of Escherichia coli RNA polymerase. J Mol Biol. 1989 Jan 20;205(2):331–341. doi: 10.1016/0022-2836(89)90344-6. [DOI] [PubMed] [Google Scholar]
  8. Grayhack E. J., Yang X. J., Lau L. F., Roberts J. W. Phage lambda gene Q antiterminator recognizes RNA polymerase near the promoter and accelerates it through a pause site. Cell. 1985 Aug;42(1):259–269. doi: 10.1016/s0092-8674(85)80121-5. [DOI] [PubMed] [Google Scholar]
  9. Higgins C. F., Dorman C. J., Stirling D. A., Waddell L., Booth I. R., May G., Bremer E. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell. 1988 Feb 26;52(4):569–584. doi: 10.1016/0092-8674(88)90470-9. [DOI] [PubMed] [Google Scholar]
  10. Howard B. H., de Crombrugghe B., Rosenberg M. Transcription in vitro of bacteriophage lambda 4S RNA: studies on termination and rho protein. Nucleic Acids Res. 1977 Apr;4(4):827–842. doi: 10.1093/nar/4.4.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jovanovich S. B., Lebowitz J. Estimation of the effect of coumermycin A1 on Salmonella typhimurium promoters by using random operon fusions. J Bacteriol. 1987 Oct;169(10):4431–4435. doi: 10.1128/jb.169.10.4431-4435.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jovanovich S. B., Lesley S. A., Burgess R. R. In vitro use of monoclonal antibodies in Escherichia coli S-30 extracts to determine the RNA polymerase sigma subunit required by a promoter. J Biol Chem. 1989 Mar 5;264(7):3794–3798. [PubMed] [Google Scholar]
  13. McKenney K., Shimatake H., Court D., Schmeissner U., Brady C., Rosenberg M. A system to study promoter and terminator signals recognized by Escherichia coli RNA polymerase. Gene Amplif Anal. 1981;2:383–415. [PubMed] [Google Scholar]
  14. Menzel R. A microtiter plate-based system for the semiautomated growth and assay of bacterial cells for beta-galactosidase activity. Anal Biochem. 1989 Aug 15;181(1):40–50. doi: 10.1016/0003-2697(89)90391-6. [DOI] [PubMed] [Google Scholar]
  15. Menzel R., Gellert M. Fusions of the Escherichia coli gyrA and gyrB control regions to the galactokinase gene are inducible by coumermycin treatment. J Bacteriol. 1987 Mar;169(3):1272–1278. doi: 10.1128/jb.169.3.1272-1278.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Menzel R., Gellert M. Modulation of transcription by DNA supercoiling: a deletion analysis of the Escherichia coli gyrA and gyrB promoters. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4185–4189. doi: 10.1073/pnas.84.12.4185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Roland K. L., Liu C. G., Turnbough C. L., Jr Role of the ribosome in suppressing transcriptional termination at the pyrBI attenuator of Escherichia coli K-12. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7149–7153. doi: 10.1073/pnas.85.19.7149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rosenthal E. R., Calvo J. M. Effect of DNA superhelicity on transcription termination. Mol Gen Genet. 1987 May;207(2-3):430–434. doi: 10.1007/BF00331611. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Schwarz E., Scherer G., Hobom G., Kössel H. Nucleotide sequence of cro, cII and part of the O gene in phage lambda DNA. Nature. 1978 Mar 30;272(5652):410–414. doi: 10.1038/272410a0. [DOI] [PubMed] [Google Scholar]
  22. Shure M., Pulleyblank D. E., Vinograd J. The problems of eukaryotic and prokaryotic DNA packaging and in vivo conformation posed by superhelix density heterogeneity. Nucleic Acids Res. 1977;4(5):1183–1205. doi: 10.1093/nar/4.5.1183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
  24. Telesnitsky A. P., Chamberlin M. J. Sequences linked to prokaryotic promoters can affect the efficiency of downstream termination sites. J Mol Biol. 1989 Jan 20;205(2):315–330. doi: 10.1016/0022-2836(89)90343-4. [DOI] [PubMed] [Google Scholar]
  25. Tse-Dinh Y. C., Beran R. K. Multiple promoters for transcription of the Escherichia coli DNA topoisomerase I gene and their regulation by DNA supercoiling. J Mol Biol. 1988 Aug 20;202(4):735–742. doi: 10.1016/0022-2836(88)90554-2. [DOI] [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. Wood D. C., Lebowitz J. Effect of supercoiling on the abortive initiation kinetics of the RNA-I promoter of ColE1 plasmid DNA. J Biol Chem. 1984 Sep 25;259(18):11184–11187. [PubMed] [Google Scholar]
  28. Wright J. J., Hayward R. S. Transcriptional termination at a fully rho-independent site in Escherichia coli is prevented by uninterrupted translation of the nascent RNA. EMBO J. 1987 Apr;6(4):1115–1119. doi: 10.1002/j.1460-2075.1987.tb04866.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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