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PMID: 14671322 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A role for mechanosensitive channels in survival of stationary phase: regulation of channel expression by RpoS.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 100 ·No. 26 ·2003-12-23 ·Pages 15959-64

Stokes NR, Murray HD, Subramaniam C, Gourse RL, Louis P, Bartlett W, Miller S, Booth IR

Abstract

The mechanosensitive (MS) channels MscS and MscL are essential for the survival of hypoosmotic shock by Escherichia coli cells. We demonstrate that MscS and MscL are induced by osmotic stress and by entry into stationary phase. Reduced levels of MS proteins and reduced expression of mscL- and mscS-LacZ fusions in an rpoS mutant strain suggested that the RNA polymerase holoenzyme containing sigmaS is responsible, at least in part, for regulating production of MS channel proteins. Consistent with the model that the effect of sigmaS is direct, the MscS and MscL promoters both use RNA polymerase containing sigmaS in vitro. Conversely, clpP or rssB mutations, which cause enhanced levels of sigmaS, show increased MS channel protein synthesis. RpoS null mutants are sensitive to hypoosmotic shock upon entry into stationary phase. These data suggest that MscS and MscL are components of the RpoS regulon and play an important role in ensuring structural integrity in stationary phase bacteria.

MeSH Terms
Bacterial Proteins/physiology Base Sequence DNA Primers Escherichia coli/genetics Escherichia coli Proteins/genetics Gene Expression Regulation, Bacterial/genetics Genes, Reporter Ion Channels/genetics,physiology Mechanotransduction, Cellular/genetics,physiology Plasmids/genetics Sigma Factor/physiology Transcription, Genetic beta-Galactosidase/genetics
Chemicals
Bacterial Proteins DNA Primers Escherichia coli Proteins Ion Channels MscL protein, E coli MscS protein, E coli Sigma Factor sigma factor KatF protein, Bacteria beta-Galactosidase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Stokes Neil R
Department of Molecular and Cell Biology, Institute of Medical Sciences, University of Aberdeen, Aberdeen AB25 2ZD, Scotland, United Kingdom.
Murray Heath D
Subramaniam Chandrasekaran
Gourse Richard L
Louis Petra
Bartlett Wendy
Miller Samantha
Booth Ian R
References (44)
44 references, click to expand
  1. Insect mechanoreception: what a long, strange TRP it's been.
    Curr Biol. 2000 May 18;10(10):R384-7 PMID: 10837217
  2. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  3. Promoter recognition and discrimination by EsigmaS RNA polymerase.
    Mol Microbiol. 2001 Nov;42(4):939-54 PMID: 11737638
  4. rRNA promoter activity in the fast-growing bacterium Vibrio natriegens.
    J Bacteriol. 2002 Mar;184(5):1349-58 PMID: 11844764
  5. Mechanotransduction in Caenorhabditis elegans: the role of DEG/ENaC ion channels.
    Cell Biochem Biophys. 2001;35(1):1-18 PMID: 11898851
  6. NTP-sensing by rRNA promoters in Escherichia coli is direct.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8602-7 PMID: 12060720
  7. Stress and the single cell: intrapopulation diversity is a mechanism to ensure survival upon exposure to stress.
    Int J Food Microbiol. 2002 Sep 15;78(1-2):19-30 PMID: 12222634
  8. Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli.
    EMBO J. 2002 Oct 15;21(20):5323-30 PMID: 12374733
  9. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  10. Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system.
    J Bacteriol. 1985 Dec;164(3):1224-32 PMID: 3905768
  11. High-copy-number and low-copy-number plasmid vectors for lacZ alpha-complementation and chloramphenicol- or kanamycin-resistance selection.
    Gene. 1987;61(1):63-74 PMID: 3327753
  12. A mechanosensitive ion channel in the yeast plasma membrane.
    Science. 1988 Nov 4;242(4879):762-5 PMID: 2460920
  13. E.coli Fis protein activates ribosomal RNA transcription in vitro and in vivo.
    EMBO J. 1990 Nov;9(11):3733-42 PMID: 2209559
  14. The stationary phase of the bacterial life cycle.
    Annu Rev Microbiol. 1993;47:855-74 PMID: 8257118
  15. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone.
    Nature. 1994 Mar 17;368(6468):265-8 PMID: 7511799
  16. Penicillin-binding proteins are regulated by rpoS during transitions in growth states of Escherichia coli.
    Antimicrob Agents Chemother. 1994 Feb;38(2):205-10 PMID: 8192444
  17. The growth phase-dependent synthesis of cyclopropane fatty acids in Escherichia coli is the result of an RpoS(KatF)-dependent promoter plus enzyme instability.
    Mol Microbiol. 1994 Mar;11(6):1009-17 PMID: 8022273
  18. Stringent control and growth-rate-dependent control have nonidentical promoter sequence requirements.
    Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1117-21 PMID: 7862645
  19. Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease.
    J Bacteriol. 1996 Jan;178(2):470-6 PMID: 8550468
  20. Posttranscriptional osmotic regulation of the sigma(s) subunit of RNA polymerase in Escherichia coli.
    J Bacteriol. 1996 Mar;178(6):1607-13 PMID: 8626288
  21. The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli.
    EMBO J. 1996 Mar 15;15(6):1333-9 PMID: 8635466
  22. Single residue substitutions that change the gating properties of a mechanosensitive channel in Escherichia coli.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11652-7 PMID: 8876191
  23. Back to log phase: sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli.
    Mol Microbiol. 1996 Sep;21(5):887-93 PMID: 8885260
  24. Membrane topology and multimeric structure of a mechanosensitive channel protein of Escherichia coli.
    EMBO J. 1996 Sep 16;15(18):4798-805 PMID: 8890153
  25. 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
  26. Mutational analysis of potential zinc-binding residues in the active site of the enterococcal D-Ala-D-Ala dipeptidase VanX.
    Biochemistry. 1997 Aug 26;36(34):10498-505 PMID: 9265630
  27. Importance of RpoS and Dps in survival of exposure of both exponential- and stationary-phase Escherichia coli cells to the electrophile N-ethylmaleimide.
    J Bacteriol. 1998 Mar;180(5):1030-6 PMID: 9495739
  28. One face of a transmembrane helix is crucial in mechanosensitive channel gating.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11471-5 PMID: 9736761
  29. Homologs of the vancomycin resistance D-Ala-D-Ala dipeptidase VanX in Streptomyces toyocaensis, Escherichia coli and Synechocystis: attributes of catalytic efficiency, stereoselectivity and regulation with implications for function.
    Chem Biol. 1998 Sep;5(9):489-504 PMID: 9751644
  30. Role of the Escherichia coli SurA protein in stationary-phase survival.
    J Bacteriol. 1998 Nov;180(21):5704-11 PMID: 9791122
  31. Identification of conserved, RpoS-dependent stationary-phase genes of Escherichia coli.
    J Bacteriol. 1998 Dec;180(23):6283-91 PMID: 9829938
  32. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel.
    Science. 1998 Dec 18;282(5397):2220-6 PMID: 9856938
  33. Mechanosensitive channels of bacteria.
    Methods Enzymol. 1999;294:458-82 PMID: 9916243
  34. Augmentation of killing of Escherichia coli O157 by combinations of lactate, ethanol, and low-pH conditions.
    Appl Environ Microbiol. 1999 Mar;65(3):1308-11 PMID: 10049898
  35. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity.
    EMBO J. 1999 Apr 1;18(7):1730-7 PMID: 10202137
  36. 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
  37. Managing hypoosmotic stress: aquaporins and mechanosensitive channels in Escherichia coli.
    Curr Opin Microbiol. 1999 Apr;2(2):166-9 PMID: 10322175
  38. VanX, a bacterial D-alanyl-D-alanine dipeptidase: resistance, immunity, or survival function?
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11028-32 PMID: 10500118
  39. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  40. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel.
    Science. 2002 Nov 22;298(5598):1582-7 PMID: 12446901
  41. Domain organization of the MscS mechanosensitive channel of Escherichia coli.
    EMBO J. 2003 Jan 2;22(1):36-46 PMID: 12505982
  42. Two families of mechanosensitive channel proteins.
    Microbiol Mol Biol Rev. 2003 Mar;67(1):66-85, table of contents PMID: 12626684
  43. Potassium transport loci in Escherichia coli K-12.
    J Bacteriol. 1971 Nov;108(2):639-44 PMID: 4942756
  44. Biological cost of AmpC production for Salmonella enterica serotype Typhimurium.
    Antimicrob Agents Chemother. 2000 Nov;44(11):3137-43 PMID: 11036037
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.2536607100
Published
2003-12-23
Epub
2003-00-11
Pages
15959-64
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC307675
Subset
IM
Grants
NIGMS NIH HHS · R01 GM037048 · United States
NIGMS NIH HHS · R37 GM037048 · United States
NIGMS NIH HHS · R01 GM37048 · United States
External Links
PubMed source DOI: 10.1073/pnas.2536607100 PMC Full Text View journal details
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