Abstract
The OxyS regulatory RNA integrates the adaptive response to hydrogen peroxide with other cellular stress responses and protects against DNA damage. Among the OxyS targets is the rpoS-encoded sigma(s) subunit of RNA polymerase. Sigma(s) is a central regulator of genes induced by osmotic stress, starvation and entry into stationary phase. We examined the mechanism whereby OxyS represses rpoS expression and found that the OxyS RNA inhibits translation of the rpoS message. This repression is dependent on the hfq-encoded RNA-binding protein (also denoted host factor I, HF-I). Co-immunoprecipitation and gel mobility shift experiments revealed that the OxyS RNA binds Hfq, suggesting that OxyS represses rpoS translation by altering Hfq activity.
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- Altuvia S., Weinstein-Fischer D., Zhang A., Postow L., Storz G. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell. 1997 Jul 11;90(1):43–53. doi: 10.1016/s0092-8674(00)80312-8. [DOI] [PubMed] [Google Scholar]
- Altuvia S., Zhang A., Argaman L., Tiwari A., Storz G. The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding. EMBO J. 1998 Oct 15;17(20):6069–6075. doi: 10.1093/emboj/17.20.6069. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barth M., Marschall C., Muffler A., Fischer D., Hengge-Aronis R. 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):3455–3464. doi: 10.1128/jb.177.12.3455-3464.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bartolomé B., Jubete Y., Martínez E., de la Cruz F. Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene. 1991 Jun 15;102(1):75–78. doi: 10.1016/0378-1119(91)90541-i. [DOI] [PubMed] [Google Scholar]
- Brown L., Elliott T. Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol. 1996 Jul;178(13):3763–3770. doi: 10.1128/jb.178.13.3763-3770.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown L., Elliott T. Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J Bacteriol. 1997 Feb;179(3):656–662. doi: 10.1128/jb.179.3.656-662.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carmichael G. G., Weber K., Niveleau A., Wahba A. J. The host factor required for RNA phage Qbeta RNA replication in vitro. Intracellular location, quantitation, and purification by polyadenylate-cellulose chromatography. J Biol Chem. 1975 May 25;250(10):3607–3612. [PubMed] [Google Scholar]
- Hengge-Aronis R. 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):887–893. doi: 10.1046/j.1365-2958.1996.511405.x. [DOI] [PubMed] [Google Scholar]
- Kajitani M., Kato A., Wada A., Inokuchi Y., Ishihama A. Regulation of the Escherichia coli hfq gene encoding the host factor for phage Q beta. J Bacteriol. 1994 Jan;176(2):531–534. doi: 10.1128/jb.176.2.531-534.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lange R., Hengge-Aronis R. 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):1600–1612. doi: 10.1101/gad.8.13.1600. [DOI] [PubMed] [Google Scholar]
- Loewen P. C., Hengge-Aronis R. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu Rev Microbiol. 1994;48:53–80. doi: 10.1146/annurev.mi.48.100194.000413. [DOI] [PubMed] [Google Scholar]
- Loewen P. C., Triggs B. L. Genetic mapping of katF, a locus that with katE affects the synthesis of a second catalase species in Escherichia coli. J Bacteriol. 1984 Nov;160(2):668–675. doi: 10.1128/jb.160.2.668-675.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muffler A., Fischer D., Altuvia S., Storz G., Hengge-Aronis R. The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli. EMBO J. 1996 Mar 15;15(6):1333–1339. [PMC free article] [PubMed] [Google Scholar]
- Muffler A., Fischer D., Hengge-Aronis R. The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev. 1996 May 1;10(9):1143–1151. doi: 10.1101/gad.10.9.1143. [DOI] [PubMed] [Google Scholar]
- Muffler A., Traulsen D. D., Fischer D., Lange R., Hengge-Aronis R. The RNA-binding protein HF-I plays a global regulatory role which is largely, but not exclusively, due to its role in expression of the sigmaS subunit of RNA polymerase in Escherichia coli. J Bacteriol. 1997 Jan;179(1):297–300. doi: 10.1128/jb.179.1.297-300.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pratt L. A., Silhavy T. J. The response regulator SprE controls the stability of RpoS. Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2488–2492. doi: 10.1073/pnas.93.6.2488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Senear A. W., Steitz J. A. Site-specific interaction of Qbeta host factor and ribosomal protein S1 with Qbeta and R17 bacteriophage RNAs. J Biol Chem. 1976 Apr 10;251(7):1902–1912. [PubMed] [Google Scholar]
- Shi X., Waasdorp B. C., Bennett G. N. Modulation of acid-induced amino acid decarboxylase gene expression by hns in Escherichia coli. J Bacteriol. 1993 Feb;175(4):1182–1186. doi: 10.1128/jb.175.4.1182-1186.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sledjeski D. D., Gupta A., Gottesman S. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J. 1996 Aug 1;15(15):3993–4000. [PMC free article] [PubMed] [Google Scholar]
- Tsui H. C., Leung H. C., Winkler M. E. Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol. 1994 Jul;13(1):35–49. doi: 10.1111/j.1365-2958.1994.tb00400.x. [DOI] [PubMed] [Google Scholar]
- 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]