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. 1992 Aug 11;20(15):4077–4081. doi: 10.1093/nar/20.15.4077

The mechanism of trans-activation of the Escherichia coli operon thrU(tufB) by the protein FIS. A model.

H Verbeek 1, L Nilsson 1, L Bosch 1
PMCID: PMC334090  PMID: 1380692

Abstract

Transcription of the thrU(tufB) operon is trans-activated by the protein FIS which binds to the promoter upstream activator sequence (UAS). Deletions of parts of the UAS and insertions show that optimal trans-activation requires occupation by FIS of the two FIS-binding regions on the UAS and specific helical positioning of these regions. On the basis of these and other data, a model for the mechanism of thrU(tufB) trans-activation by FIS is proposed. This model implies that the mechanisms underlying stimulation by FIS of two totally different processes: inversion of viral DNA segments and transcription of stable RNA operons, are essentially the same.

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Selected References

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

  1. Bosch L., Nilsson L., Vijgenboom E., Verbeek H. FIS-dependent trans-activation of tRNA and rRNA operons of Escherichia coli. Biochim Biophys Acta. 1990 Aug 27;1050(1-3):293–301. doi: 10.1016/0167-4781(90)90184-4. [DOI] [PubMed] [Google Scholar]
  2. Bossi L., Smith D. M. Conformational change in the DNA associated with an unusual promoter mutation in a tRNA operon of Salmonella. Cell. 1984 Dec;39(3 Pt 2):643–652. doi: 10.1016/0092-8674(84)90471-9. [DOI] [PubMed] [Google Scholar]
  3. Bruist M. F., Glasgow A. C., Johnson R. C., Simon M. I. Fis binding to the recombinational enhancer of the Hin DNA inversion system. Genes Dev. 1987 Oct;1(8):762–772. doi: 10.1101/gad.1.8.762. [DOI] [PubMed] [Google Scholar]
  4. Bétermier M., Lefrère V., Koch C., Alazard R., Chandler M. The Escherichia coli protein, Fis: specific binding to the ends of phage Mu DNA and modulation of phage growth. Mol Microbiol. 1989 Apr;3(4):459–468. doi: 10.1111/j.1365-2958.1989.tb00192.x. [DOI] [PubMed] [Google Scholar]
  5. Gourse R. L., de Boer H. A., Nomura M. DNA determinants of rRNA synthesis in E. coli: growth rate dependent regulation, feedback inhibition, upstream activation, antitermination. Cell. 1986 Jan 17;44(1):197–205. doi: 10.1016/0092-8674(86)90498-8. [DOI] [PubMed] [Google Scholar]
  6. Grundy F. J., Howe M. M. Involvement of the invertible G segment in bacteriophage mu tail fiber biosynthesis. Virology. 1984 Apr 30;134(2):296–317. doi: 10.1016/0042-6822(84)90299-x. [DOI] [PubMed] [Google Scholar]
  7. Heichman K. A., Johnson R. C. The Hin invertasome: protein-mediated joining of distant recombination sites at the enhancer. Science. 1990 Aug 3;249(4968):511–517. doi: 10.1126/science.2166334. [DOI] [PubMed] [Google Scholar]
  8. Heumann H., Lederer H., Baer G., May R. P., Kjems J. K., Crespi H. L. Spatial arrangement of DNA-dependent RNA polymerase of Escherichia coli and DNA in the specific complex. A neutron small angle scattering study. J Mol Biol. 1988 May 5;201(1):115–125. doi: 10.1016/0022-2836(88)90443-3. [DOI] [PubMed] [Google Scholar]
  9. Huber H. E., Iida S., Arber W., Bickle T. A. Site-specific DNA inversion is enhanced by a DNA sequence element in cis. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3776–3780. doi: 10.1073/pnas.82.11.3776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hübner P., Arber W. Mutational analysis of a prokaryotic recombinational enhancer element with two functions. EMBO J. 1989 Feb;8(2):577–585. doi: 10.1002/j.1460-2075.1989.tb03412.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hübner P., Haffter P., Iida S., Arber W. Bent DNA is needed for recombinational enhancer activity in the site-specific recombination system Cin of bacteriophage P1. The role of FIS protein. J Mol Biol. 1989 Feb 5;205(3):493–500. doi: 10.1016/0022-2836(89)90220-9. [DOI] [PubMed] [Google Scholar]
  12. Igarashi K., Hanamura A., Makino K., Aiba H., Aiba H., Mizuno T., Nakata A., Ishihama A. Functional map of the alpha subunit of Escherichia coli RNA polymerase: two modes of transcription activation by positive factors. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8958–8962. doi: 10.1073/pnas.88.20.8958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Igarashi K., Ishihama A. Bipartite functional map of the E. coli RNA polymerase alpha subunit: involvement of the C-terminal region in transcription activation by cAMP-CRP. Cell. 1991 Jun 14;65(6):1015–1022. doi: 10.1016/0092-8674(91)90553-b. [DOI] [PubMed] [Google Scholar]
  14. Johnson R. C., Simon M. I. Hin-mediated site-specific recombination requires two 26 bp recombination sites and a 60 bp recombinational enhancer. Cell. 1985 Jul;41(3):781–791. doi: 10.1016/s0092-8674(85)80059-3. [DOI] [PubMed] [Google Scholar]
  15. Kahmann R., Rudt F., Koch C., Mertens G. G inversion in bacteriophage Mu DNA is stimulated by a site within the invertase gene and a host factor. Cell. 1985 Jul;41(3):771–780. doi: 10.1016/s0092-8674(85)80058-1. [DOI] [PubMed] [Google Scholar]
  16. Kanaar R., van de Putte P., Cozzarelli N. R. Gin-mediated DNA inversion: product structure and the mechanism of strand exchange. Proc Natl Acad Sci U S A. 1988 Feb;85(3):752–756. doi: 10.1073/pnas.85.3.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kostrewa D., Granzin J., Koch C., Choe H. W., Raghunathan S., Wolf W., Labahn J., Kahmann R., Saenger W. Three-dimensional structure of the E. coli DNA-binding protein FIS. Nature. 1991 Jan 10;349(6305):178–180. doi: 10.1038/349178a0. [DOI] [PubMed] [Google Scholar]
  18. Lamond A. I., Travers A. A. Requirement for an upstream element for optimal transcription of a bacterial tRNA gene. Nature. 1983 Sep 15;305(5931):248–250. doi: 10.1038/305248a0. [DOI] [PubMed] [Google Scholar]
  19. Meisenberger O., Heumann H., Pilz I. Small-angle X-ray study of DNA-dependent RNA polymerase holoenzyme from Escherichia coli. FEBS Lett. 1981 Jan 12;123(1):22–24. doi: 10.1016/0014-5793(81)80010-5. [DOI] [PubMed] [Google Scholar]
  20. Nilsson L., Vanet A., Vijgenboom E., Bosch L. The role of FIS in trans activation of stable RNA operons of E. coli. EMBO J. 1990 Mar;9(3):727–734. doi: 10.1002/j.1460-2075.1990.tb08166.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nilsson L., Verbeek H., Vijgenboom E., van Drunen C., Vanet A., Bosch L. FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions. J Bacteriol. 1992 Feb;174(3):921–929. doi: 10.1128/jb.174.3.921-929.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Osuna R., Finkel S. E., Johnson R. C. Identification of two functional regions in Fis: the N-terminus is required to promote Hin-mediated DNA inversion but not lambda excision. EMBO J. 1991 Jun;10(6):1593–1603. doi: 10.1002/j.1460-2075.1991.tb07680.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ross W., Thompson J. F., Newlands J. T., Gourse R. L. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J. 1990 Nov;9(11):3733–3742. doi: 10.1002/j.1460-2075.1990.tb07586.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Siebenlist U., Simpson R. B., Gilbert W. E. coli RNA polymerase interacts homologously with two different promoters. Cell. 1980 Jun;20(2):269–281. doi: 10.1016/0092-8674(80)90613-3. [DOI] [PubMed] [Google Scholar]
  25. Thompson J. F., Moitoso de Vargas L., Koch C., Kahmann R., Landy A. Cellular factors couple recombination with growth phase: characterization of a new component in the lambda site-specific recombination pathway. Cell. 1987 Sep 11;50(6):901–908. doi: 10.1016/0092-8674(87)90516-2. [DOI] [PubMed] [Google Scholar]
  26. Travers A. A. Conserved features of coordinately regulated E. coli promoters. Nucleic Acids Res. 1984 Mar 26;12(6):2605–2618. doi: 10.1093/nar/12.6.2605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Travers A. A., Lamond A. I., Mace H. A., Berman M. L. RNA polymerase interactions with the upstream region of the E. coli tyrT promoter. Cell. 1983 Nov;35(1):265–273. doi: 10.1016/0092-8674(83)90229-5. [DOI] [PubMed] [Google Scholar]
  28. Verbeek H., Nilsson L., Baliko G., Bosch L. Potential binding sites of the trans-activator FIS are present upstream of all rRNA operons and of many but not all tRNA operons. Biochim Biophys Acta. 1990 Aug 27;1050(1-3):302–306. doi: 10.1016/0167-4781(90)90185-5. [DOI] [PubMed] [Google Scholar]
  29. Verbeek H., Nilsson L., Bosch L. FIS-induced bending of a region upstream of the promoter activates transcription of the E coli thrU(tufB) operon. Biochimie. 1991 Jun;73(6):713–718. doi: 10.1016/0300-9084(91)90051-2. [DOI] [PubMed] [Google Scholar]
  30. Vijgenboom E., Nilsson L., Bosch L. The elongation factor EF-Tu from E. coli binds to the upstream activator region of the tRNA-tufB operon. Nucleic Acids Res. 1988 Nov 11;16(21):10183–10197. doi: 10.1093/nar/16.21.10183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yuan H. S., Finkel S. E., Feng J. A., Kaczor-Grzeskowiak M., Johnson R. C., Dickerson R. E. The molecular structure of wild-type and a mutant Fis protein: relationship between mutational changes and recombinational enhancer function or DNA binding. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9558–9562. doi: 10.1073/pnas.88.21.9558. [DOI] [PMC free article] [PubMed] [Google Scholar]

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