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PMID: 10856246 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

sigma factor selectivity of Escherichia coli RNA polymerase: role for CRP, IHF and lrp transcription factors.

The EMBO journal ·Vol. 19 ·No. 12 ·2000-06-15 ·Pages 3028-37

Colland F, Barth M, Hengge-Aronis R, Kolb A

Abstract

osmY is a stationary phase-induced and osmotically regulated gene in Escherichia coli that requires the stationary phase RNA polymerase (Esigma(S)) for in vivo expression. We show here that the major RNA polymerase, Esigma(70), also transcribes osmY in vitro and, depending on genetic background, even in vivo. The cAMP receptor protein (CRP) bound to cAMP, the leucine-responsive regulatory protein (Lrp) and the integration host factor (IHF) inhibit transcription initiation at the osmY promoter. The binding site for CRP is centred at -12.5 from the transcription start site, whereas Lrp covers the whole promoter region. The site for IHF maps in the -90 region. By mobility shift assay, permanganate reactivity and in vitro transcription experiments, we show that repression is much stronger with Esigma(70) than with Esigma(S) holoenzyme. We conclude that CRP, Lrp and IHF inhibit open complex formation more efficiently with Esigma(70) than with Esigma(S). This different ability of the two holoenzymes to interact productively with promoters once assembled in complex nucleoprotein structures may be a crucial factor in generating sigma(S) selectivity in vivo.

MeSH Terms
Bacterial Proteins/genetics,metabolism Base Sequence Binding Sites Carrier Proteins/genetics Cyclic AMP Receptor Protein/metabolism DNA-Binding Proteins/metabolism DNA-Directed RNA Polymerases/metabolism Escherichia coli/genetics Escherichia coli Proteins Gene Expression Regulation, Bacterial Integration Host Factors Leucine-Responsive Regulatory Protein Molecular Sequence Data Periplasmic Binding Proteins Promoter Regions, Genetic Protein Binding Sigma Factor/metabolism Transcription Factors/metabolism Transcription, Genetic
Chemicals
Bacterial Proteins Carrier Proteins Cyclic AMP Receptor Protein DNA-Binding Proteins Escherichia coli Proteins Integration Host Factors Lrp protein, E coli Periplasmic Binding Proteins Sigma Factor Transcription Factors sigma factor KatF protein, Bacteria Leucine-Responsive Regulatory Protein osmY protein, E coli RNA polymerase sigma 70 DNA-Directed RNA Polymerases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Colland F
Institut Pasteur, Unité de Physicochimie des Macromolécules Biologiques (URA 1773 du CNRS), 75724 Paris, Cedex 15, France.
Barth M
Hengge-Aronis R
Kolb A
References (61)
61 references, click to expand
  1. Interplay between global regulators of Escherichia coli: effect of RpoS, Lrp and H-NS on transcription of the gene osmC.
    Mol Microbiol. 1998 Jun;28(5):971-80 PMID: 9663683
  2. Deletion analysis of the fis promoter region in Escherichia coli: antagonistic effects of integration host factor and Fis.
    J Bacteriol. 1997 Oct;179(20):6367-77 PMID: 9335285
  3. The kinetics of sigma subunit directed promoter recognition by E. coli RNA polymerase.
    J Mol Biol. 1999 Jan 22;285(3):955-64 PMID: 9918716
  4. Lrp binds to two regions in the dadAX promoter region of Escherichia coli to repress and activate transcription directly.
    Mol Microbiol. 1999 Apr;32(1):29-40 PMID: 10216857
  5. Protein-nucleic acid interactions during open complex formation investigated by systematic alteration of the protein and DNA binding partners.
    Biochemistry. 1999 May 11;38(19):5959-67 PMID: 10320321
  6. Repression of transcription initiation in bacteria.
    J Bacteriol. 1999 May;181(10):2987-91 PMID: 10321997
  7. Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival.
    Genes Cells. 1999 Mar;4(3):135-43 PMID: 10320479
  8. Interplay of global regulators and cell physiology in the general stress response of Escherichia coli.
    Curr Opin Microbiol. 1999 Apr;2(2):148-52 PMID: 10322169
  9. Transcriptional organization and in vivo role of the Escherichia coli rsd gene, encoding the regulator of RNA polymerase sigma D.
    J Bacteriol. 1999 Jun;181(12):3768-76 PMID: 10368152
  10. Positioning of sigma(S), the stationary phase sigma factor, in Escherichia coli RNA polymerase-promoter open complexes.
    EMBO J. 1999 Jul 15;18(14):4049-59 PMID: 10406809
  11. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid.
    J Bacteriol. 1999 Oct;181(20):6361-70 PMID: 10515926
  12. Expression of the Escherichia coli ada regulon in stationary phase: evidence for rpoS-dependent negative regulation of alkA transcription.
    J Bacteriol. 1999 Nov;181(21):6836-9 PMID: 10542189
  13. Involvement of differential efficiency of transcription by esigmas and esigma70 RNA polymerase holoenzymes in growth phase regulation of the Escherichia coli osmE promoter.
    Mol Microbiol. 2000 Feb;35(4):845-53 PMID: 10692161
  14. A new method for sequencing DNA.
    Proc Natl Acad Sci U S A. 1977 Feb;74(2):560-4 PMID: 265521
  15. Overexpression and purification of the sigma subunit of Escherichia coli RNA polymerase.
    Gene. 1983 Dec;26(2-3):109-18 PMID: 6231214
  16. E. coli integration host factor binds to specific sites in DNA.
    Cell. 1984 Dec;39(3 Pt 2):707-16 PMID: 6096022
  17. Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli.
    J Bacteriol. 1987 Oct;169(10):4499-506 PMID: 3308843
  18. Scanning calorimetric study of the thermal unfolding of catabolite activator protein from Escherichia coli in the absence and presence of cyclic mononucleotides.
    Biochemistry. 1988 Jul 12;27(14):5257-61 PMID: 2844254
  19. Integration host factor: a protein for all reasons.
    Cell. 1988 Nov 18;55(4):545-54 PMID: 2972385
  20. Promoters largely determine the efficiency of repressor action.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):8973-7 PMID: 3057497
  21. KMnO4 as a probe for lac promoter DNA melting and mechanism in vivo.
    J Biol Chem. 1989 May 15;264(14):8074-81 PMID: 2722774
  22. Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel sigma transcription factor.
    Nucleic Acids Res. 1989 Dec 11;17(23):9979-91 PMID: 2690013
  23. Integration host factor is a negative effector of in vivo and in vitro expression of ompC in Escherichia coli.
    J Bacteriol. 1990 Sep;172(9):5293-8 PMID: 2203749
  24. Searching for and predicting the activity of sites for DNA binding proteins: compilation and analysis of the binding sites for Escherichia coli integration host factor (IHF).
    Nucleic Acids Res. 1990 Sep 11;18(17):4993-5000 PMID: 2205834
  25. Identification of a central regulator of stationary-phase gene expression in Escherichia coli.
    Mol Microbiol. 1991 Jan;5(1):49-59 PMID: 1849609
  26. Spatial arrangement of sigma-factor and core enzyme of Escherichia coli RNA polymerase. A neutron solution scattering study.
    J Mol Biol. 1991 Jun 20;219(4):747-55 PMID: 2056537
  27. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees.
    Science. 1991 Aug 30;253(5023):1001-7 PMID: 1653449
  28. Life after log.
    J Bacteriol. 1992 Jan;174(2):345-8 PMID: 1729229
  29. osmY, a new hyperosmotically inducible gene, encodes a periplasmic protein in Escherichia coli.
    J Bacteriol. 1992 Jun;174(11):3637-44 PMID: 1317380
  30. The sigma 70 family: sequence conservation and evolutionary relationships.
    J Bacteriol. 1992 Jun;174(12):3843-9 PMID: 1597408
  31. Osmotic regulation of rpoS-dependent genes in Escherichia coli.
    J Bacteriol. 1993 Jan;175(1):259-65 PMID: 8416901
  32. The role of the sigma factor sigma S (KatF) in bacterial global regulation.
    Annu Rev Microbiol. 1994;48:53-80 PMID: 7826018
  33. Sigma S-dependent growth-phase induction of the csgBA promoter in Escherichia coli can be achieved in vivo by sigma 70 in the absence of the nucleoid-associated protein H-NS.
    Mol Microbiol. 1994 Sep;13(6):1021-32 PMID: 7854117
  34. Quantitative control of the stationary phase-specific sigma factor, sigma S, in Escherichia coli: involvement of the nucleoid protein H-NS.
    EMBO J. 1995 Feb 1;14(3):594-602 PMID: 7859747
  35. A snapshot of a dynamic nuclear building block.
    Nat Struct Biol. 1997 Oct;4(10):763-6 PMID: 9334735
  36. Molecular analysis of the regulation of csiD, a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on sigma s and requires activation by cAMP-CRP.
    J Mol Biol. 1998 Feb 20;276(2):339-53 PMID: 9512707
  37. A stationary phase protein in Escherichia coli with binding activity to the major sigma subunit of RNA polymerase.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4953-8 PMID: 9560209
  38. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli.
    Mol Microbiol. 1993 Feb;7(4):523-36 PMID: 8459772
  39. Heterogeneity of the principal sigma factor in Escherichia coli: the rpoS gene product, sigma 38, is a second principal sigma factor of RNA polymerase in stationary-phase Escherichia coli.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3511-5 PMID: 8475100
  40. Lrp, a major regulatory protein in Escherichia coli, bends DNA and can organize the assembly of a higher-order nucleoprotein structure.
    EMBO J. 1993 Jun;12(6):2495-501 PMID: 8508774
  41. Transcriptional regulation by cAMP and its receptor protein.
    Annu Rev Biochem. 1993;62:749-95 PMID: 8394684
  42. In vitro functional characterization of overproduced Escherichia coli katF/rpoS gene product.
    Biochemistry. 1993 Oct 19;32(41):11112-7 PMID: 8218173
  43. Complex transcriptional control of the sigma s-dependent stationary-phase-induced and osmotically regulated osmY (csi-5) gene suggests novel roles for Lrp, cyclic AMP (cAMP) receptor protein-cAMP complex, and integration host factor in the stationary-phase response of Escherichia coli.
    J Bacteriol. 1993 Dec;175(24):7910-7 PMID: 8253679
  44. Molecular characterization of the promoter of osmY, an rpoS-dependent gene.
    J Bacteriol. 1994 Jan;176(1):100-7 PMID: 8282684
  45. Identification and characterization of stationary phase-inducible genes in Escherichia coli.
    Mol Microbiol. 1993 Oct;10(2):407-20 PMID: 7934831
  46. The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability.
    Genes Dev. 1994 Jul 1;8(13):1600-12 PMID: 7525405
  47. Selectivity of the Escherichia coli RNA polymerase E sigma 38 for overlapping promoters and ability to support CRP activation.
    Nucleic Acids Res. 1995 Mar 11;23(5):819-26 PMID: 7708498
  48. Promoter determinants for Escherichia coli RNA polymerase holoenzyme containing sigma 38 (the rpoS gene product).
    Nucleic Acids Res. 1995 Mar 11;23(5):827-34 PMID: 7708499
  49. Expression of the genes coding for the Escherichia coli integration host factor are controlled by growth phase, rpoS, ppGpp and by autoregulation.
    Mol Microbiol. 1994 Dec;14(5):1021-31 PMID: 7715442
  50. Role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of sigma S and many sigma S-dependent genes in Escherichia coli.
    J Bacteriol. 1995 Jun;177(12):3455-64 PMID: 7768855
  51. Promoter selectivity control of Escherichia coli RNA polymerase by ionic strength: differential recognition of osmoregulated promoters by E sigma D and E sigma S holoenzymes.
    Mol Microbiol. 1995 May;16(4):649-56 PMID: 7476160
  52. Leucine-responsive regulatory protein: a global regulator of gene expression in E. coli.
    Annu Rev Microbiol. 1995;49:747-75 PMID: 8561478
  53. Promoter selectivity of Escherichia coli RNA polymerase E sigma 70 and E sigma 38 holoenzymes. Effect of DNA supercoiling.
    J Biol Chem. 1996 Jan 26;271(4):1998-2004 PMID: 8567650
  54. The leucine-responsive regulatory protein (Lrp) from Escherichia coli. Stoichiometry and minimal requirements for binding to DNA.
    J Biol Chem. 1996 Mar 22;271(12):6611-7 PMID: 8636076
  55. The leucine-responsive regulatory protein (Lrp) acts as a specific repressor for sigma s-dependent transcription of the Escherichia coli aidB gene.
    Mol Microbiol. 1996 Jun;20(5):947-55 PMID: 8809748
  56. Mode of promoter recognition by the Escherichia coli RNA polymerase holoenzyme containing the sigma S subunit: identification of the recognition sequence of the fic promoter.
    Mol Microbiol. 1995 Dec;18(5):841-50 PMID: 8825088
  57. Effects of nutrition and growth rate on Lrp levels in Escherichia coli.
    J Bacteriol. 1996 Dec;178(23):6930-6 PMID: 8955316
  58. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn.
    Cell. 1996 Dec 27;87(7):1295-306 PMID: 8980235
  59. Comparative analysis of the interactions of Escherichia coli sigma S and sigma 70 RNA polymerase holoenzyme with the stationary-phase-specific bolAp1 promoter.
    Biochemistry. 1997 Feb 18;36(7):1748-54 PMID: 9048558
  60. A nucleoprotein activation complex between the leucine-responsive regulatory protein and DNA upstream of the gltBDF operon in Escherichia coli.
    J Mol Biol. 1997 Jul 11;270(2):152-68 PMID: 9236118
  61. The ftsQ1p gearbox promoter of Escherichia coli is a major sigma S-dependent promoter in the ddlB-ftsA region.
    Mol Microbiol. 1998 Oct;30(2):419-30 PMID: 9791185
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2000-06-15
Pages
3028-37
Language
English
Region
England
NLM ID
8208664
PMCID
PMC203352
Subset
IM
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