Home LiteratureArticle Details
PMID: 16903784 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

The structural basis for promoter -35 element recognition by the group IV sigma factors.

PLoS biology ·Vol. 4 ·No. 9 ·2006-09-00 ·Pages e269

Lane WJ, Darst SA

Abstract

The control of bacterial transcription initiation depends on a primary sigma factor for housekeeping functions, as well as alternative sigma factors that control regulons in response to environmental stresses. The largest and most diverse subgroup of alternative sigma factors, the group IV extracytoplasmic function sigma factors, directs the transcription of genes that regulate a wide variety of responses, including envelope stress and pathogenesis. We determined the 2.3-A resolution crystal structure of the -35 element recognition domain of a group IV sigma factor, Escherichia coli sigma(E)4, bound to its consensus -35 element, GGAACTT. Despite similar function and secondary structure, the primary and group IV sigma factors recognize their -35 elements using distinct mechanisms. Conserved sequence elements of the sigma(E) -35 element induce a DNA geometry characteristic of AA/TT-tract DNA, including a rigid, straight double-helical axis and a narrow minor groove. For this reason, the highly conserved AA in the middle of the GGAACTT motif is essential for -35 element recognition by sigma(E)4, despite the absence of direct protein-DNA interactions with these DNA bases. These principles of sigma(E)4/-35 element recognition can be applied to a wide range of other group IV sigma factors.

MeSH Terms
Amino Acid Sequence Base Sequence Binding Sites Crystallization DNA-Binding Proteins/chemistry DNA-Directed RNA Polymerases/chemistry Escherichia coli Escherichia coli Proteins/chemistry Gene Expression Regulation, Bacterial Models, Biological Models, Molecular Molecular Sequence Data Promoter Regions, Genetic Protein Conformation Regulatory Elements, Transcriptional/physiology Sequence Homology, Amino Acid Sequence Homology, Nucleic Acid Sigma Factor/chemistry
Chemicals
DNA-Binding Proteins Escherichia coli Proteins Sigma Factor DNA-Directed RNA Polymerases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lane William J
The Rockefeller University, New York, New York, United States of America.
Darst Seth A
Conflict of Interest

Competing interests. The authors have declared that no competing interests exist.

References (49)
49 references, click to expand
  1. Conserved and variable functions of the sigmaE stress response in related genomes.
    PLoS Biol. 2006 Jan;4(1):e2 PMID: 16336047
  2. Multiple sigma subunits and the partitioning of bacterial transcription space.
    Annu Rev Microbiol. 2003;57:441-66 PMID: 14527287
  3. Cross-validated maximum likelihood enhances crystallographic simulated annealing refinement.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):5018-23 PMID: 9144182
  4. Identification of nucleotides critical for activity of the sigmaE-dependent rpoEp3 promoter in Salmonella enterica serovar Typhimurium.
    FEMS Microbiol Lett. 2004 Sep 1;238(1):227-33 PMID: 15336426
  5. SigmaE is an essential sigma factor in Escherichia coli.
    J Bacteriol. 1997 Nov;179(21):6862-4 PMID: 9352942
  6. Characterization of the Escherichia coli sigma E regulon.
    J Biol Chem. 2001 Jun 15;276(24):20866-75 PMID: 11274153
  7. The sigmaE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigmaE.
    Mol Microbiol. 1997 Apr;24(2):373-85 PMID: 9159523
  8. Helix geometry, hydration, and G.A mismatch in a B-DNA decamer.
    Science. 1987 Oct 23;238(4826):498-504 PMID: 3310237
  9. Bacterial RNA polymerases: the wholo story.
    Curr Opin Struct Biol. 2003 Feb;13(1):31-9 PMID: 12581657
  10. Periplasmic stress and ECF sigma factors.
    Annu Rev Microbiol. 2001;55:591-624 PMID: 11544368
  11. Electrostatics of nanosystems: application to microtubules and the ribosome.
    Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10037-41 PMID: 11517324
  12. The extracytoplasmic function sigma factors: role and regulation.
    Mol Microbiol. 1998 Jun;28(6):1059-66 PMID: 9680198
  13. Sigma factors and global gene regulation in Mycobacterium tuberculosis.
    J Bacteriol. 2004 Feb;186(4):895-902 PMID: 14761983
  14. The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium.
    Infect Immun. 1999 Apr;67(4):1560-8 PMID: 10084987
  15. Hierarchies of base pair preferences in the P22 ant promoter.
    J Bacteriol. 1991 Mar;173(6):1944-50 PMID: 2001998
  16. The structure of an oligo(dA).oligo(dT) tract and its biological implications.
    Nature. 1987 Nov 19-25;330(6145):221-6 PMID: 3670410
  17. Crystal structure of Escherichia coli sigmaE with the cytoplasmic domain of its anti-sigma RseA.
    Mol Cell. 2003 Apr;11(4):1067-78 PMID: 12718891
  18. Bacterial RNA polymerase.
    Curr Opin Struct Biol. 2001 Apr;11(2):155-62 PMID: 11297923
  19. Propeller-twisting of base-pairs and the conformational mobility of dinucleotide steps in DNA.
    J Mol Biol. 1996 May 31;259(1):95-103 PMID: 8648652
  20. Improved methods for building protein models in electron density maps and the location of errors in these models.
    Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9 PMID: 2025413
  21. Structure of the bacterial RNA polymerase promoter specificity sigma subunit.
    Mol Cell. 2002 Mar;9(3):527-39 PMID: 11931761
  22. Contribution of cation-pi interactions to the stability of protein-DNA complexes.
    J Mol Biol. 2000 Sep 15;302(2):395-410 PMID: 10970741
  23. The sigma 70 family: sequence conservation and evolutionary relationships.
    J Bacteriol. 1992 Jun;174(12):3843-9 PMID: 1597408
  24. Modulation of the Escherichia coli sigmaE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins.
    Mol Microbiol. 1997 Apr;24(2):355-71 PMID: 9159522
  25. WebLogo: a sequence logo generator.
    Genome Res. 2004 Jun;14(6):1188-90 PMID: 15173120
  26. A phylogenomic study of the general stress response sigma factor sigmaB of Bacillus subtilis and its regulatory proteins.
    J Mol Microbiol Biotechnol. 2002 Jul;4(4):427-52 PMID: 12125823
  27. Identification of target promoters for the Bacillus subtilis sigma X factor using a consensus-directed search.
    J Mol Biol. 1998 May 29;279(1):165-73 PMID: 9636707
  28. DNA A-tract bending in three dimensions: solving the dA4T4 vs. dT4A4 conundrum.
    Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1177-82 PMID: 14739342
  29. The functional and regulatory roles of sigma factors in transcription.
    Cold Spring Harb Symp Quant Biol. 1998;63:141-55 PMID: 10384278
  30. A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae.
    J Bacteriol. 1994 May;176(10):3089-91 PMID: 8188613
  31. The extracytoplasmic sigma factor, final sigma(E), is required for intracellular survival of nontypeable Haemophilus influenzae in J774 macrophages.
    Infect Immun. 2002 Feb;70(2):708-15 PMID: 11796603
  32. Role of the extracytoplasmic-function sigma factor sigma(H) in Mycobacterium tuberculosis global gene expression.
    Mol Microbiol. 2002 Jul;45(2):365-74 PMID: 12123450
  33. The extracytoplasmic function (ECF) sigma factors.
    Adv Microb Physiol. 2002;46:47-110 PMID: 12073657
  34. Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the sigmaR regulon.
    Mol Microbiol. 2001 Nov;42(4):1007-20 PMID: 11737643
  35. Structure of a ternary transcription activation complex.
    Mol Cell. 2004 Jan 16;13(1):45-53 PMID: 14731393
  36. Region 4 of sigma as a target for transcription regulation.
    Mol Microbiol. 2003 May;48(4):863-74 PMID: 12753182
  37. Intrinsic bending and deformability at the T-A step of CCTTTAAAGG: a comparative analysis of T-A and A-T steps within A-tracts.
    J Mol Biol. 2001 Oct 5;312(5):1037-49 PMID: 11580248
  38. Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex.
    Science. 2002 May 17;296(5571):1285-90 PMID: 12016307
  39. Regulation of the Escherichia coli sigma-dependent envelope stress response.
    Mol Microbiol. 2004 May;52(3):613-9 PMID: 15101969
  40. The Mycobacterium tuberculosis ECF sigma factor sigmaE: role in global gene expression and survival in macrophages.
    Mol Microbiol. 2001 Jul;41(2):423-37 PMID: 11489128
  41. The alternative sigma factor sigma(E) plays an important role in intestinal survival and virulence in Vibrio cholerae.
    Infect Immun. 2002 Oct;70(10):5355-62 PMID: 12228259
  42. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures.
    Nucleic Acids Res. 2003 Sep 1;31(17):5108-21 PMID: 12930962
  43. Promoter recognition and discrimination by EsigmaS RNA polymerase.
    Mol Microbiol. 2001 Nov;42(4):939-54 PMID: 11737638
  44. The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival.
    Mol Microbiol. 2002 Feb;43(3):771-82 PMID: 11929531
  45. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution.
    J Mol Biol. 2002 Jun 21;319(5):1097-113 PMID: 12079350
  46. Cation-pi/H-bond stair motifs at protein-DNA interfaces.
    J Mol Biol. 2002 May 24;319(1):67-76 PMID: 12051937
  47. The algT (algU) gene of Pseudomonas aeruginosa, a key regulator involved in alginate biosynthesis, encodes an alternative sigma factor (sigma E).
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7941-5 PMID: 7644517
  48. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7573-7 PMID: 8052622
  49. Defining the Bacillus subtilis sigma(W) regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches.
    J Mol Biol. 2002 Feb 22;316(3):443-57 PMID: 11866510
Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
DOI
10.1371/journal.pbio.0040269
Published
2006-09-00
Pages
e269
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC1540707
Subset
IM
Grants
NIGMS NIH HHS · R01 GM053759 · United States
NIGMS NIH HHS · T32 GM007739 · United States
NIGMS NIH HHS · GM07739 · United States
NIGMS NIH HHS · GM53759 · United States
Databases
PDB
1KX4, 2H27
Corrections
CommentIn
PMID: 20076632
External Links
PubMed source DOI: 10.1371/journal.pbio.0040269 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2