Home LiteratureArticle Details
PMID: 16885445 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

DksA is required for growth phase-dependent regulation, growth rate-dependent control, and stringent control of fis expression in Escherichia coli.

Journal of bacteriology ·Vol. 188 ·No. 16 ·2006-08-00 ·Pages 5775-82

Mallik P, Paul BJ, Rutherford ST, Gourse RL, Osuna R

Abstract

DksA is a critical transcription factor in Escherichia coli that binds to RNA polymerase and potentiates control of rRNA promoters and certain amino acid promoters. Given the kinetic similarities between rRNA promoters and the fis promoter (Pfis), we investigated the possibility that DksA might also control transcription from Pfis. We show that the absence of dksA extends transcription from Pfis well into the late logarithmic and stationary growth phases, demonstrating the importance of DksA for growth phase-dependent regulation of fis. We also show that transcription from Pfis increases with steady-state growth rate and that dksA is absolutely required for this regulation. In addition, both DksA and ppGpp are required for inhibition of Pfis promoter activity following amino acid starvation, and these factors act directly and synergistically to negatively control Pfis transcription in vitro. DksA decreases the half-life of the intrinsically short-lived fis promoter-RNA polymerase complex and increases its sensitivity to the concentration of CTP, the predominant initiating nucleotide triphosphate for this promoter. This work extends our understanding of the multiple factors controlling fis expression and demonstrates the generality of the DksA requirement for regulation of kinetically similar promoters.

MeSH Terms
Cytidine Triphosphate/metabolism DNA-Directed RNA Polymerases/metabolism Escherichia coli/genetics,growth & development Escherichia coli Proteins/genetics,metabolism Factor For Inversion Stimulation Protein Gene Expression Regulation, Bacterial/physiology Transcription Factors/genetics,metabolism Transcription, Genetic
Chemicals
Escherichia coli Proteins Factor For Inversion Stimulation Protein Fis protein, E coli Transcription Factors dksA protein, E coli Cytidine Triphosphate DNA-Directed RNA Polymerases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Mallik Prabhat
Department of Biological Sciences, University at Albany, 1400 Washington Avenue, Albany, NY 12222, USA.
Paul Brian J
Rutherford Steven T
Gourse Richard L
Osuna Robert
References (61)
61 references, click to expand
  1. Control of rRNA expression by small molecules is dynamic and nonredundant.
    Mol Cell. 2003 Jul;12(1):125-34 PMID: 12887898
  2. The Escherichia coli Fis promoter is regulated by changes in the levels of its transcription initiation nucleotide CTP.
    J Biol Chem. 2004 Dec 3;279(49):50818-28 PMID: 15385561
  3. Transcript cleavage factors GreA and GreB act as transient catalytic components of RNA polymerase.
    EMBO J. 2003 Dec 1;22(23):6322-34 PMID: 14633991
  4. Growth phase-dependent regulation and stringent control of fis are conserved processes in enteric bacteria and involve a single promoter (fis P) in Escherichia coli.
    J Bacteriol. 2004 Jan;186(1):122-35 PMID: 14679232
  5. Donation of catalytic residues to RNA polymerase active center by transcription factor Gre.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15469-74 PMID: 14668436
  6. Relationship between growth rate and ATP concentration in Escherichia coli: a bioassay for available cellular ATP.
    J Biol Chem. 2004 Feb 27;279(9):8262-8 PMID: 14670952
  7. Unique roles of the rrn P2 rRNA promoters in Escherichia coli.
    Mol Microbiol. 2004 Jun;52(5):1375-87 PMID: 15165240
  8. Regulation through the secondary channel--structural framework for ppGpp-DksA synergism during transcription.
    Cell. 2004 Aug 6;118(3):297-309 PMID: 15294156
  9. DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP.
    Cell. 2004 Aug 6;118(3):311-22 PMID: 15294157
  10. A dedicated translation factor controls the synthesis of the global regulator Fis.
    EMBO J. 2004 Aug 18;23(16):3375-85 PMID: 15297874
  11. Cloning, expression, purification, crystallization and initial crystallographic analysis of transcription factor DksA from Escherichia coli.
    Acta Crystallogr D Biol Crystallogr. 2004 Sep;60(Pt 9):1611-3 PMID: 15333933
  12. A procedure for the rapid, large-scall purification of Escherichia coli DNA-dependent RNA polymerase involving Polymin P precipitation and DNA-cellulose chromatography.
    Biochemistry. 1975 Oct 21;14(21):4634-8 PMID: 1101952
  13. Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate.
    J Bacteriol. 1982 Sep;151(3):1261-8 PMID: 6179924
  14. 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):901-8 PMID: 2957063
  15. Analysis of the promoters and transcripts involved in IS10 anti-sense RNA control.
    Gene. 1988 Dec 10;72(1-2):219-36 PMID: 2468561
  16. Guanosine 3'-diphosphate 5'-diphosphate is not required for growth rate-dependent control of rRNA synthesis in Escherichia coli.
    Proc Natl Acad Sci U S A. 1990 Jul;87(14):5533-7 PMID: 2196571
  17. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo.
    EMBO J. 1990 Nov;9(11):3733-42 PMID: 2209559
  18. Residual guanosine 3',5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations.
    J Biol Chem. 1991 Mar 25;266(9):5980-90 PMID: 2005134
  19. FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions.
    J Bacteriol. 1992 Feb;174(3):921-9 PMID: 1732224
  20. The E.coli fis promoter is subject to stringent control and autoregulation.
    EMBO J. 1992 Mar;11(3):1075-83 PMID: 1547773
  21. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli.
    J Bacteriol. 1992 Dec;174(24):8043-56 PMID: 1459953
  22. The Fis protein: it's not just for DNA inversion anymore.
    Mol Microbiol. 1992 Nov;6(22):3257-65 PMID: 1484481
  23. Compilation of E. coli mRNA promoter sequences.
    Nucleic Acids Res. 1993 Apr 11;21(7):1507-16 PMID: 8479900
  24. Factor for inversion stimulation-dependent growth rate regulation of individual tRNA species in Escherichia coli.
    J Biol Chem. 1994 Apr 1;269(13):9460-5 PMID: 7511587
  25. Growth rate-dependent control of the rrnB P1 core promoter in Escherichia coli.
    J Bacteriol. 1994 Sep;176(17):5560-4 PMID: 8071240
  26. Crystal structure of the GreA transcript cleavage factor from Escherichia coli.
    Nature. 1995 Feb 16;373(6515):636-40 PMID: 7854424
  27. Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli.
    J Bacteriol. 1995 Feb;177(4):938-47 PMID: 7860604
  28. Sequence, regulation, and functions of fis in Salmonella typhimurium.
    J Bacteriol. 1995 Apr;177(8):2021-32 PMID: 7536730
  29. Control of rRNA transcription in Escherichia coli.
    Microbiol Rev. 1995 Dec;59(4):623-45 PMID: 8531889
  30. Invariance of the nucleoside triphosphate pools of Escherichia coli with growth rate.
    J Biol Chem. 2000 Feb 11;275(6):3931-5 PMID: 10660546
  31. rRNA transcription in Escherichia coli.
    Annu Rev Genet. 2004;38:749-70 PMID: 15568992
  32. DksA potentiates direct activation of amino acid promoters by ppGpp.
    Proc Natl Acad Sci U S A. 2005 May 31;102(22):7823-8 PMID: 15899978
  33. Regulation of rRNA transcription is remarkably robust: FIS compensates for altered nucleoside triphosphate sensing by mutant RNA polymerases at Escherichia coli rrn P1 promoters.
    J Bacteriol. 2000 Apr;182(7):1969-77 PMID: 10715005
  34. Fis, a DNA nucleoid-associated protein, is involved in Salmonella typhimurium SPI-1 invasion gene expression.
    Mol Microbiol. 2001 Jan;39(1):79-88 PMID: 11123690
  35. PromEC: An updated database of Escherichia coli mRNA promoters with experimentally identified transcriptional start sites.
    Nucleic Acids Res. 2001 Jan 1;29(1):277 PMID: 11125111
  36. Mechanism of regulation of transcription initiation by ppGpp. I. Effects of ppGpp on transcription initiation in vivo and in vitro.
    J Mol Biol. 2001 Jan 26;305(4):673-88 PMID: 11162084
  37. Mechanism of regulation of transcription initiation by ppGpp. II. Models for positive control based on properties of RNAP mutants and competition for RNAP.
    J Mol Biol. 2001 Jan 26;305(4):689-702 PMID: 11162085
  38. Role of the nucleoid-associated protein Fis in the regulation of virulence properties of enteropathogenic Escherichia coli.
    Mol Microbiol. 2001 Aug;41(3):549-59 PMID: 11532124
  39. Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli.
    Mol Microbiol. 2001 Sep;41(5):983-97 PMID: 11555281
  40. Involvement of FIS in the H-NS-mediated regulation of virF gene of Shigella and enteroinvasive Escherichia coli.
    Mol Microbiol. 2001 Oct;42(2):439-52 PMID: 11703666
  41. Architecture of Fis-activated transcription complexes at the Escherichia coli rrnB P1 and rrnE P1 promoters.
    J Mol Biol. 2002 Feb 22;316(3):501-16 PMID: 11866514
  42. The C-terminal domains of the RNA polymerase alpha subunits: contact site with Fis and localization during co-activation with CRP at the Escherichia coli proP P2 promoter.
    J Mol Biol. 2002 Feb 22;316(3):517-29 PMID: 11866515
  43. Factors affecting start site selection at the Escherichia coli fis promoter.
    J Bacteriol. 2002 Sep;184(17):4783-91 PMID: 12169603
  44. Regulation of the Escherichia coli rrnB P2 promoter.
    J Bacteriol. 2003 Jan;185(1):28-34 PMID: 12486037
  45. Kinetic properties of rrn promoters in Escherichia coli.
    Biochimie. 2002 Oct;84(10):981-96 PMID: 12504278
  46. Antagonistic involvement of FIS and H-NS proteins in the transcriptional control of hns expression.
    Mol Microbiol. 1996 Mar;19(5):965-75 PMID: 8830277
  47. The ndh-binding protein (Nbp) regulates the ndh gene of Escherichia coli in response to growth phase and is identical to Fis.
    Mol Microbiol. 1996 Jun;20(5):1043-55 PMID: 8809757
  48. FIS is a regulator of metabolism in Escherichia coli.
    Mol Microbiol. 1996 Oct;22(1):21-9 PMID: 8899705
  49. Regulation of HU alpha and HU beta by CRP and FIS in Escherichia coli.
    J Mol Biol. 1996 Oct 25;263(2):126-39 PMID: 8913296
  50. Molecular anatomy of a transcription activation patch: FIS-RNA polymerase interactions at the Escherichia coli rrnB P1 promoter.
    EMBO J. 1997 Jan 2;16(1):154-62 PMID: 9009276
  51. 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
  52. Fis, an accessorial factor for transcriptional activation of the mar (multiple antibiotic resistance) promoter of Escherichia coli in the presence of the activator MarA, SoxS, or Rob.
    J Bacteriol. 1997 Dec;179(23):7410-9 PMID: 9393706
  53. Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria.
    Science. 1997 Dec 19;278(5346):2092-7 PMID: 9405339
  54. Regulation of transcription initiation at the Escherichia coli nir operon promoter: a new mechanism to account for co-dependence on two transcription factors.
    Mol Microbiol. 1998 Jan;27(2):493-505 PMID: 9484902
  55. The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like "stringent" RNA polymerases in Escherichia coli.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2908-13 PMID: 9501189
  56. Multiple cis-acting sites positively regulate Escherichia coli nrd expression.
    Mol Microbiol. 1998 Jun;28(6):1315-22 PMID: 9680219
  57. Identification and characterization of the fis operon in enteric bacteria.
    J Bacteriol. 1998 Nov;180(22):5932-46 PMID: 9811652
  58. Functional determinants of the Escherichia coli fis promoter: roles of -35, -10, and transcription initiation regions in the response to stringent control and growth phase-dependent regulation.
    J Bacteriol. 1999 Feb;181(4):1269-80 PMID: 9973355
  59. Multiple mechanisms are used for growth rate and stringent control of leuV transcriptional initiation in Escherichia coli.
    J Bacteriol. 1999 Sep;181(18):5771-82 PMID: 10482520
  60. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid.
    J Bacteriol. 1999 Oct;181(20):6361-70 PMID: 10515926
  61. Structure and function of the transcription elongation factor GreB bound to bacterial RNA polymerase.
    Cell. 2003 Aug 8;114(3):335-45 PMID: 12914698
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2006-08-00
Pages
5775-82
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC1540068
Subset
IM
Grants
NIGMS NIH HHS · R29 GM052051 · United States
NIGMS NIH HHS · R01 GM052051 · United States
NIGMS NIH HHS · GM52051 · United States
NIGMS NIH HHS · R01 GM037048 · United States
NIGMS NIH HHS · GM37048 · United States
NIGMS NIH HHS · R37 GM037048 · United States
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