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. 1996 Mar 19;93(6):2488–2492. doi: 10.1073/pnas.93.6.2488

The response regulator SprE controls the stability of RpoS.

L A Pratt 1, T J Silhavy 1
PMCID: PMC39824  PMID: 8637901

Abstract

In Escherichia coli, the sigma factor, RpoS, is a central regulator in stationary-phase cells. We have identified a gene, sprE (stationary-phase regulator), as essential for the negative regulation of rpoS expression. SprE negatively regulates the rpoS gene product at the level of protein stability, perhaps in response to nutrient availability. The ability of SprE to destabilize RpoS is dependent on the ClpX/ClpP protease. Based on homology, SprE is a member of the response regulator family of proteins. SprE is the first response regulator identified that is implicated in the control of protein stability. Moreover, SprE is the first reported protein that appears to regulate rpoS in response to a specific environmental parameter.

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Selected References

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  1. Böhringer J., Fischer D., Mosler G., Hengge-Aronis R. UDP-glucose is a potential intracellular signal molecule in the control of expression of sigma S and sigma S-dependent genes in Escherichia coli. J Bacteriol. 1995 Jan;177(2):413–422. doi: 10.1128/jb.177.2.413-422.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bösl M., Kersten H. Organization and functions of genes in the upstream region of tyrT of Escherichia coli: phenotypes of mutants with partial deletion of a new gene (tgs). J Bacteriol. 1994 Jan;176(1):221–231. doi: 10.1128/jb.176.1.221-231.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Gentry D. R., Hernandez V. J., Nguyen L. H., Jensen D. B., Cashel M. Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp. J Bacteriol. 1993 Dec;175(24):7982–7989. doi: 10.1128/jb.175.24.7982-7989.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Gottesman S., Clark W. P., de Crecy-Lagard V., Maurizi M. R. ClpX, an alternative subunit for the ATP-dependent Clp protease of Escherichia coli. Sequence and in vivo activities. J Biol Chem. 1993 Oct 25;268(30):22618–22626. [PubMed] [Google Scholar]
  5. Hengge-Aronis R., Klein W., Lange R., Rimmele M., Boos W. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol. 1991 Dec;173(24):7918–7924. doi: 10.1128/jb.173.24.7918-7924.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hengge-Aronis R., Lange R., Henneberg N., Fischer D. Osmotic regulation of rpoS-dependent genes in Escherichia coli. J Bacteriol. 1993 Jan;175(1):259–265. doi: 10.1128/jb.175.1.259-265.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hengge-Aronis R. Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli. Cell. 1993 Jan 29;72(2):165–168. doi: 10.1016/0092-8674(93)90655-a. [DOI] [PubMed] [Google Scholar]
  8. Huisman G. W., Kolter R. Sensing starvation: a homoserine lactone--dependent signaling pathway in Escherichia coli. Science. 1994 Jul 22;265(5171):537–539. doi: 10.1126/science.7545940. [DOI] [PubMed] [Google Scholar]
  9. Kawaji H., Mizuno T., Mizushima S. Influence of molecular size and osmolarity of sugars and dextrans on the synthesis of outer membrane proteins O-8 and O-9 of Escherichia coli K-12. J Bacteriol. 1979 Dec;140(3):843–847. doi: 10.1128/jb.140.3.843-847.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kleckner N., Bender J., Gottesman S. Uses of transposons with emphasis on Tn10. Methods Enzymol. 1991;204:139–180. doi: 10.1016/0076-6879(91)04009-d. [DOI] [PubMed] [Google Scholar]
  11. Lange R., Barth M., Hengge-Aronis R. 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):7910–7917. doi: 10.1128/jb.175.24.7910-7917.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lange R., Hengge-Aronis R. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J Bacteriol. 1991 Jul;173(14):4474–4481. doi: 10.1128/jb.173.14.4474-4481.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lange R., Hengge-Aronis R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol. 1991 Jan;5(1):49–59. doi: 10.1111/j.1365-2958.1991.tb01825.x. [DOI] [PubMed] [Google Scholar]
  14. Loewen P. C., von Ossowski I., Switala J., Mulvey M. R. KatF (sigma S) synthesis in Escherichia coli is subject to posttranscriptional regulation. J Bacteriol. 1993 Apr;175(7):2150–2153. doi: 10.1128/jb.175.7.2150-2153.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. McCann M. P., Fraley C. D., Matin A. The putative sigma factor KatF is regulated posttranscriptionally during carbon starvation. J Bacteriol. 1993 Apr;175(7):2143–2149. doi: 10.1128/jb.175.7.2143-2149.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McCann M. P., Kidwell J. P., Matin A. The putative sigma factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J Bacteriol. 1991 Jul;173(13):4188–4194. doi: 10.1128/jb.173.13.4188-4194.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mulvey M. R., Loewen P. C. Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel sigma transcription factor. Nucleic Acids Res. 1989 Dec 11;17(23):9979–9991. doi: 10.1093/nar/17.23.9979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mulvey M. R., Switala J., Borys A., Loewen P. C. Regulation of transcription of katE and katF in Escherichia coli. J Bacteriol. 1990 Dec;172(12):6713–6720. doi: 10.1128/jb.172.12.6713-6720.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nguyen L. H., Jensen D. B., Thompson N. E., Gentry D. R., Burgess R. R. In vitro functional characterization of overproduced Escherichia coli katF/rpoS gene product. Biochemistry. 1993 Oct 19;32(41):11112–11117. doi: 10.1021/bi00092a021. [DOI] [PubMed] [Google Scholar]
  20. Parkinson J. S., Kofoid E. C. Communication modules in bacterial signaling proteins. Annu Rev Genet. 1992;26:71–112. doi: 10.1146/annurev.ge.26.120192.000443. [DOI] [PubMed] [Google Scholar]
  21. Pratt L. A., Silhavy T. J. OmpR mutants specifically defective for transcriptional activation. J Mol Biol. 1994 Nov 4;243(4):579–594. doi: 10.1016/0022-2836(94)90033-7. [DOI] [PubMed] [Google Scholar]
  22. Russo F. D., Slauch J. M., Silhavy T. J. Mutations that affect separate functions of OmpR the phosphorylated regulator of porin transcription in Escherichia coli. J Mol Biol. 1993 May 20;231(2):261–273. doi: 10.1006/jmbi.1993.1281. [DOI] [PubMed] [Google Scholar]
  23. Sak B. D., Eisenstark A., Touati D. Exonuclease III and the catalase hydroperoxidase II in Escherichia coli are both regulated by the katF gene product. Proc Natl Acad Sci U S A. 1989 May;86(9):3271–3275. doi: 10.1073/pnas.86.9.3271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schellhorn H. E., Stones V. L. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol. 1992 Jul;174(14):4769–4776. doi: 10.1128/jb.174.14.4769-4776.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schweder T., Lee K. H., Lomovskaya O., Matin A. Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J Bacteriol. 1996 Jan;178(2):470–476. doi: 10.1128/jb.178.2.470-476.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Siegele D. A., Kolter R. Life after log. J Bacteriol. 1992 Jan;174(2):345–348. doi: 10.1128/jb.174.2.345-348.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Slauch J. M., Silhavy T. J. cis-acting ompF mutations that result in OmpR-dependent constitutive expression. J Bacteriol. 1991 Jul;173(13):4039–4048. doi: 10.1128/jb.173.13.4039-4048.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Snyder W. B., Silhavy T. J. Enhanced export of beta-galactosidase fusion proteins in prlF mutants is Lon dependent. J Bacteriol. 1992 Sep;174(17):5661–5668. doi: 10.1128/jb.174.17.5661-5668.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Takayanagi Y., Tanaka K., Takahashi H. Structure of the 5' upstream region and the regulation of the rpoS gene of Escherichia coli. Mol Gen Genet. 1994 Jun 3;243(5):525–531. doi: 10.1007/BF00284200. [DOI] [PubMed] [Google Scholar]
  30. Tanaka K., Takayanagi Y., Fujita N., Ishihama A., Takahashi H. 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):3511–3515. doi: 10.1073/pnas.90.8.3511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Touati E., Dassa E., Boquet P. L. Pleiotropic mutations in appR reduce pH 2.5 acid phosphatase expression and restore succinate utilisation in CRP-deficient strains of Escherichia coli. Mol Gen Genet. 1986 Feb;202(2):257–264. doi: 10.1007/BF00331647. [DOI] [PubMed] [Google Scholar]
  32. Yamashino T., Ueguchi C., Mizuno T. 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. doi: 10.1002/j.1460-2075.1995.tb07035.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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