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. 1977 Oct;74(10):4365–4369. doi: 10.1073/pnas.74.10.4365

Transcription termination at the trp operon attenuators of Escherichia coli and Salmonella typhimurium: RNA secondary structure and regulation of termination.

F Lee, C Yanofsky
PMCID: PMC431942  PMID: 337297

Abstract

Transcription termination at the attenuators of the trp operons of Escherichia coli and Salmonella typhimurium was studied in vitro using DNA restriction fragments as templates. Readthrough transcription beyond the terminators occurred with 5 and 30% efficiency, respectively, in E. coli and S. typhimurium. This difference is correlated with the stability of proposed secondary structures of the respective trp leader transcripts. Secondary structure analyses of the two leader transcripts revealed a well-conserved pattern of RNA base paring. This and the possibility that trp leader RNA is translated suggest a model for regulation of transcription termination that is based on ribosome movement along the RNA and a shift between alternative RNA base-pairing configuration.

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Selected References

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  1. Armstrong A., Hagopian H., Ingram V. M., Wagner E. K. Chemical studies on amino acid acceptor ribonucleic acids. VII. Partial ribonuclease digestion of alanine and valine soluble ribonucleic acid from yeast. Biochemistry. 1966 Sep;5(9):3027–3036. doi: 10.1021/bi00873a036. [DOI] [PubMed] [Google Scholar]
  2. Armstrong K. A., Hershfield V., Helinski D. R. Gene cloning and containment properties of plasmid Col E1 and its derivatives. Science. 1977 Apr 8;196(4286):172–174. doi: 10.1126/science.322277. [DOI] [PubMed] [Google Scholar]
  3. Arnott S., Bond P. J. Structures for Poly(U)-poly(A)-poly(U)triple stranded polynucleotides. Nat New Biol. 1973 Jul 25;244(134):99–101. doi: 10.1038/newbio244099a0. [DOI] [PubMed] [Google Scholar]
  4. Artz S. W., Broach J. R. Histidine regulation in Salmonella typhimurium: an activator attenuator model of gene regulation. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3453–3457. doi: 10.1073/pnas.72.9.3453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bennett G. N., Schweingruber M. E., Brown K. D., Squires C., Yanofsky C. Nucleotide sequence of region preceding trp mRNA initiation site and its role in promoter and operator function. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2351–2355. doi: 10.1073/pnas.73.7.2351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bertrand K., Korn L., Lee F., Platt T., Squires C. L., Squires C., Yanofsky C. New features of the regulation of the tryptophan operon. Science. 1975 Jul 4;189(4196):22–26. doi: 10.1126/science.1094538. [DOI] [PubMed] [Google Scholar]
  7. Bertrand K., Yanofsky C. Regulation of transcription termination in the leader region of the tryptophan operon of Escherichia coli involves tryptophan or its metabolic product. J Mol Biol. 1976 May 15;103(2):339–349. doi: 10.1016/0022-2836(76)90316-8. [DOI] [PubMed] [Google Scholar]
  8. Borer P. N., Dengler B., Tinoco I., Jr, Uhlenbeck O. C. Stability of ribonucleic acid double-stranded helices. J Mol Biol. 1974 Jul 15;86(4):843–853. doi: 10.1016/0022-2836(74)90357-x. [DOI] [PubMed] [Google Scholar]
  9. Hiraga S. Operator mutants of the tryptophan operon in Escherichia coli. J Mol Biol. 1969 Jan 14;39(1):159–179. doi: 10.1016/0022-2836(69)90340-4. [DOI] [PubMed] [Google Scholar]
  10. Korn L. J., Yanofsky C. Polarity suppressors defective in transcription termination at the attenuator of the tryptophan operon of Escherichia coli have altered rho factor. J Mol Biol. 1976 Sep 15;106(2):231–241. doi: 10.1016/0022-2836(76)90082-6. [DOI] [PubMed] [Google Scholar]
  11. Korn L. J., Yanofsky C. Polarity suppressors increase expression of the wild-type tryptophan operon of Escherichia coli. J Mol Biol. 1976 May 15;103(2):395–409. doi: 10.1016/0022-2836(76)90319-3. [DOI] [PubMed] [Google Scholar]
  12. Lee F., Squires C. L., Squires C., Yanofsky C. Termination of transcription in vitro in the Escherichia coli tryptophan operon leader region. J Mol Biol. 1976 May 15;103(2):383–393. doi: 10.1016/0022-2836(76)90318-1. [DOI] [PubMed] [Google Scholar]
  13. Maniatis T., Jeffrey A., van deSande H. Chain length determination of small double- and single-stranded DNA molecules by polyacrylamide gel electrophoresis. Biochemistry. 1975 Aug 26;14(17):3787–3794. doi: 10.1021/bi00688a010. [DOI] [PubMed] [Google Scholar]
  14. Morse D. E., Morse A. N. Dual-control of the tryptophan operon is mediated by both tryptophanyl-tRNA synthetase and the repressor. J Mol Biol. 1976 May 15;103(2):209–226. doi: 10.1016/0022-2836(76)90310-7. [DOI] [PubMed] [Google Scholar]
  15. Platt T., Squires C., Yanofsky C. Ribosome-protected regions in the leader-trpE sequence of Escherichia coli tryptophan operon messenger RNA. J Mol Biol. 1976 May 15;103(2):411–420. doi: 10.1016/0022-2836(76)90320-x. [DOI] [PubMed] [Google Scholar]
  16. Roberts J. W. Transcription termination and late control in phage lambda. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3300–3304. doi: 10.1073/pnas.72.9.3300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rosenberg M., de Chrombrugghe B., Musso R. Determination of nucleotide sequences beyond the sites of transcriptional termination. Proc Natl Acad Sci U S A. 1976 Mar;73(3):717–721. doi: 10.1073/pnas.73.3.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schmeissner U., Ganem D., Miller J. H. Genetic studies of the lac repressor. II. Fine structure deletion map of the lacI gene, and its correlation with the physical map. J Mol Biol. 1977 Jan 15;109(2):303–326. doi: 10.1016/s0022-2836(77)80036-3. [DOI] [PubMed] [Google Scholar]
  19. Selker E., Brown K., Yanofsky C. Mitomycin C-induced expression of trpA of Salmonella typhimurium inserted into the plasmid ColE1. J Bacteriol. 1977 Jan;129(1):388–394. doi: 10.1128/jb.129.1.388-394.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Squires C. L., Lee F. D., Yanofsky C. Interaction of the trp repressor and RNA polymerase with the trp operon. J Mol Biol. 1975 Feb 15;92(1):93–111. doi: 10.1016/0022-2836(75)90093-5. [DOI] [PubMed] [Google Scholar]
  21. Squires C., Lee F., Bertrand K., Squires C. L., Bronson M. J., Yanofsky C. Nucleotide sequence of the 5' end of tryptophan messenger RNA of Escherichia coli. J Mol Biol. 1976 May 15;103(2):351–381. doi: 10.1016/0022-2836(76)90317-x. [DOI] [PubMed] [Google Scholar]
  22. Steitz J. A., Jakes K. How ribosomes select initiator regions in mRNA: base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4734–4738. doi: 10.1073/pnas.72.12.4734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stent G. S. Genetic transcription. Proc R Soc Lond B Biol Sci. 1966 Mar 22;164(995):181–197. doi: 10.1098/rspb.1966.0022. [DOI] [PubMed] [Google Scholar]
  24. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  25. Weidner H., Yuan R., Crothers D. M. Does 5S RNA function by a switch between two secondary structures? Nature. 1977 Mar 10;266(5598):193–194. doi: 10.1038/266193a0. [DOI] [PubMed] [Google Scholar]

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