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. 1998 Oct 15;17(20):6069–6075. doi: 10.1093/emboj/17.20.6069

The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding.

S Altuvia 1, A Zhang 1, L Argaman 1, A Tiwari 1, G Storz 1
PMCID: PMC1170933  PMID: 9774350

Abstract

OxyS is a small untranslated RNA which is induced in response to oxidative stress in Escherichia coli. This novel RNA acts as a global regulator to activate or repress the expression of as many as 40 genes, including the fhlA-encoded transcriptional activator and the rpoS-encoded sigma(s) subunit of RNA polymerase. Deletion analysis of OxyS showed that different domains of the small RNA are required for the regulation of fhlA and rpoS. We examined the mechanism of OxyS repression of fhlA and found that the OxyS RNA inhibits fhlA translation by pairing with a short sequence overlapping the Shine-Dalgarno sequence, thereby blocking ribosome binding/translation.

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Selected References

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  1. Altuvia S., Kornitzer D., Teff D., Oppenheim A. B. Alternative mRNA structures of the cIII gene of bacteriophage lambda determine the rate of its translation initiation. J Mol Biol. 1989 Nov 20;210(2):265–280. doi: 10.1016/0022-2836(89)90329-x. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Andersen J., Delihas N. micF RNA binds to the 5' end of ompF mRNA and to a protein from Escherichia coli. Biochemistry. 1990 Oct 2;29(39):9249–9256. doi: 10.1021/bi00491a020. [DOI] [PubMed] [Google Scholar]
  4. Andersen J., Forst S. A., Zhao K., Inouye M., Delihas N. The function of micF RNA. micF RNA is a major factor in the thermal regulation of OmpF protein in Escherichia coli. J Biol Chem. 1989 Oct 25;264(30):17961–17970. [PubMed] [Google Scholar]
  5. Blomberg P., Nordström K., Wagner E. G. Replication control of plasmid R1: RepA synthesis is regulated by CopA RNA through inhibition of leader peptide translation. EMBO J. 1992 Jul;11(7):2675–2683. doi: 10.1002/j.1460-2075.1992.tb05333.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Delihas N. Regulation of gene expression by trans-encoded antisense RNAs. Mol Microbiol. 1995 Feb;15(3):411–414. doi: 10.1111/j.1365-2958.1995.tb02254.x. [DOI] [PubMed] [Google Scholar]
  7. Delihas N., Rokita S. E., Zheng P. Natural antisense RNA/target RNA interactions: possible models for antisense oligonucleotide drug design. Nat Biotechnol. 1997 Aug;15(8):751–753. doi: 10.1038/nbt0897-751. [DOI] [PubMed] [Google Scholar]
  8. Hartz D., McPheeters D. S., Traut R., Gold L. Extension inhibition analysis of translation initiation complexes. Methods Enzymol. 1988;164:419–425. doi: 10.1016/s0076-6879(88)64058-4. [DOI] [PubMed] [Google Scholar]
  9. Humphreys G. O., Willshaw G. A., Smith H. R., Anderson E. S. Mutagenesis of plasmid DNA with hydroxylamine: isolation of mutants of multi-copy plasmids. Mol Gen Genet. 1976 Apr 23;145(1):101–108. doi: 10.1007/BF00331564. [DOI] [PubMed] [Google Scholar]
  10. Kornitzer D., Teff D., Altuvia S., Oppenheim A. B. Genetic analysis of bacteriophage lambda cIII gene: mRNA structural requirements for translation initiation. J Bacteriol. 1989 May;171(5):2563–2572. doi: 10.1128/jb.171.5.2563-2572.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Ma C., Simons R. W. The IS10 antisense RNA blocks ribosome binding at the transposase translation initiation site. EMBO J. 1990 Apr;9(4):1267–1274. doi: 10.1002/j.1460-2075.1990.tb08235.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Malmgren C., Engdahl H. M., Romby P., Wagner E. G. An antisense/target RNA duplex or a strong intramolecular RNA structure 5' of a translation initiation signal blocks ribosome binding: the case of plasmid R1. RNA. 1996 Oct;2(10):1022–1032. [PMC free article] [PubMed] [Google Scholar]
  14. Malmgren C., Wagner E. G., Ehresmann C., Ehresmann B., Romby P. Antisense RNA control of plasmid R1 replication. The dominant product of the antisense rna-mrna binding is not a full RNA duplex. J Biol Chem. 1997 May 9;272(19):12508–12512. doi: 10.1074/jbc.272.19.12508. [DOI] [PubMed] [Google Scholar]
  15. Maupin J. A., Shanmugam K. T. Genetic regulation of formate hydrogenlyase of Escherichia coli: role of the fhlA gene product as a transcriptional activator for a new regulatory gene, fhlB. J Bacteriol. 1990 Sep;172(9):4798–4806. doi: 10.1128/jb.172.9.4798-4806.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Schlensog V., Böck A. Identification and sequence analysis of the gene encoding the transcriptional activator of the formate hydrogenlyase system of Escherichia coli. Mol Microbiol. 1990 Aug;4(8):1319–1327. doi: 10.1111/j.1365-2958.1990.tb00711.x. [DOI] [PubMed] [Google Scholar]
  17. Siemering K. R., Praszkier J., Pittard A. J. Mechanism of binding of the antisense and target RNAs involved in the regulation of IncB plasmid replication. J Bacteriol. 1994 May;176(9):2677–2688. doi: 10.1128/jb.176.9.2677-2688.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Sledjeski D., Gottesman S. A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2003–2007. doi: 10.1073/pnas.92.6.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tomizawa J. Control of ColE1 plasmid replication. Interaction of Rom protein with an unstable complex formed by RNA I and RNA II. J Mol Biol. 1990 Apr 20;212(4):695–708. doi: 10.1016/0022-2836(90)90231-a. [DOI] [PubMed] [Google Scholar]
  22. Wagner E. G., Simons R. W. Antisense RNA control in bacteria, phages, and plasmids. Annu Rev Microbiol. 1994;48:713–742. doi: 10.1146/annurev.mi.48.100194.003433. [DOI] [PubMed] [Google Scholar]
  23. Zhang A., Altuvia S., Tiwari A., Argaman L., Hengge-Aronis R., Storz G. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J. 1998 Oct 15;17(20):6061–6068. doi: 10.1093/emboj/17.20.6061. [DOI] [PMC free article] [PubMed] [Google Scholar]

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