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The Small RNA IstR Inhibits Synthesis of an SOS-Induced Toxic Peptide

2004; Elsevier BV; Volume: 14; Issue: 24 Linguagem: Inglês

10.1016/j.cub.2004.12.003

1879-0445

Jörg Vogel, Liron Argaman, E. Gerhart H. Wagner, Shoshy Altuvia,

DNA and Nucleic Acid Chemistry

More than 60 small RNAs (sRNA) have been identified in E. coli[1Argaman L. Hershberg R. Vogel J. Bejerano G. Wagner E.G.H. Margalit H. Altuvia S. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli.Curr. Biol. 2001; 11: 941-950Abstract Full Text Full Text PDF PubMed Scopus (613) Google Scholar, 2Chen S. Lesnik E.A. Hall T.A. Sampath R. Griffey R.H. Ecker D.J. Blyn L.B. A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome.Biosystems. 2002; 65: 157-177Crossref PubMed Scopus (176) Google Scholar, 3Rivas E. Klein R.J. Jones T.A. Eddy S.R. Computational identification of noncoding RNAs in E. coli by comparative genomics.Curr. Biol. 2001; 11: 1369-1373Abstract Full Text Full Text PDF PubMed Scopus (322) Google Scholar, 4Tjaden B. Saxena R.M. Stolyar S. Haynor D.R. Kolker E. Rosenow C. Transcriptome analysis of Escherichia coli using high-density oligonucleotide probe arrays.Nucleic Acids Res. 2002; 30: 3732-3738Crossref PubMed Scopus (146) Google Scholar, 5Vogel J. Bartels V. Hock Tang T. Churakov G. Slagter-Jäger J.G. Hüttenhofer A. Wagner E.G.H. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria.Nucleic Acids Res. 2003; 31: 6435-6443Crossref PubMed Scopus (349) Google Scholar, 6Wassarman K.M. Repoila F. Rosenow C. Storz G. Gottesman S. Identification of novel small RNAs using comparative genomics and microarrays.Genes Dev. 2001; 15: 1637-1651Crossref PubMed Scopus (568) Google Scholar, 7Zhang A. Wassarman K.M. Rosenow C. Tjaden B.C. Storz G. Gottesman S. Global analysis of small RNA and mRNA targets of Hfq.Mol. Microbiol. 2003; 50 (a): 1111-1124Crossref PubMed Scopus (411) Google Scholar]. The functions of the majority of these sRNAs are still unclear. For the few sRNAs characterized, expression and functional studies indicate that they act under stress conditions [8Wassarman K.M. Small RNAs in bacteria diverse regulators of gene expression in response to environmental changes.Cell. 2002; 109: 141-144Abstract Full Text Full Text PDF PubMed Scopus (144) Google Scholar, 9Altuvia S. Regulatory small RNAs The key to coordinating global regulatory circuits.J. Bacteriol. 2004; 186: 6679-6680Crossref PubMed Scopus (21) Google Scholar, 10Altuvia 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; 90: 43-53Abstract Full Text Full Text PDF PubMed Scopus (364) Google Scholar, 11Sledjeski 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; 15: 3993-4000Crossref PubMed Scopus (284) Google Scholar, 12Majdalani N. Chen S. Murrow J. St John K. Gottesman S. Regulation of RpoS by a novel small RNA The characterization of RprA.Mol. Microbiol. 2001; 39: 1382-1394Crossref PubMed Google Scholar, 13Andersen J. Delihas N. Ikenaka K. Green P.J. Pines O. Ilercil O. Inouye M. The isolation and characterization of RNA coded by the micF gene in Escherichia coli.Nucleic Acids Res. 1987; 15: 2089-2101Crossref PubMed Scopus (45) Google Scholar, 14Massé E. Gottesman S. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli.Proc. Natl. Acad. Sci. USA. 2002; 99: 4620-4625Crossref PubMed Scopus (821) Google Scholar]. Here, we describe a novel E. coli chromosome locus that is part of the SOS response to DNA damage. This locus encodes two sRNAs, IstR-1 and IstR-2, and a toxic peptide, TisB, encoded by tisAB mRNA. Transcription of tisAB and istR-2 is SOS regulated, whereas IstR-1 is present throughout growth. IstR-1 inhibits toxicity by base-pairing to a short region in the tisAB mRNA. This antisense interaction entails RNase III-dependent cleavage, thereby inactivating the mRNA for translation. In the absence of the SOS response, IstR-1 is present in high excess over its target. However, SOS induction leads to depletion of the IstR-1 pool, concomitant with accumulation of tisAB mRNA. Under such conditions, TisB exerts its toxic effect, slowing down growth. We propose that the inhibitory sRNA prevents inadvertent TisB synthesis during normal growth and, possibly, also limits SOS-induced toxicity. Our study adds the SOS regulon to the growing list of global regulatory circuits controlled by sRNA genes.