Regulation of the small regulatory RNA MicA by ribonuclease III: A target-dependent pathway

Nucleic Acids Research

Volumn 39, Issue 7, 2011, Pages 2918-2930

  Viegas, Sandra C ^a   Silva, Inês J ^a   Saramago, Margarida ^a   Domingues, Susana ^a   Arraiano, Cecília M ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; OUTER MEMBRANE PROTEIN A; PROTEIN MICA; RIBONUCLEASE E; RIBONUCLEASE III; RNA; TRANSFER RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BASE PAIRING; ENZYME REGULATION; GENE CONTROL; GENE FUNCTION; HUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SALMONELLA TYPHIMURIUM; UNTRANSLATED REGION;

BACTERIAL OUTER MEMBRANE PROTEINS; BASE PAIRING; MUTATION; RIBONUCLEASE III; RNA, MESSENGER; RNA, SMALL UNTRANSLATED; SALMONELLA TYPHIMURIUM;

EUKARYOTA; SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 79954601376     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq1239     Document Type: Article

References (58)

1. Mizuno, T., Chou, M.Y. and Inouye, M. (1984) A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad. Sci. USA, 81, 1966-1970. (Pubitemid 14146587)
2. Livny, J. and Waldor, M.K. (2007) Identification of small RNAs in diverse bacterial species. Curr. Opin. Microbiol., 10, 96-101. (Pubitemid 46590045)
3. Guillier, M. and Gottesman, S. (2006) Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol. Microbiol., 59, 231-247.
4. Papenfort, K., Pfeiffer, V., Mika, F., Lucchini, S., Hinton, J.C. and Vogel, J. (2006) SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol. Microbiol., 62, 1674-1688. (Pubitemid 44813812)
5. Douchin, V., Bohn, C. and Bouloc, P. (2006) Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. J. Biol. Chem., 281, 12253-12259. (Pubitemid 43855309)
6. Johansen, J., Rasmussen, AA., Overgaard, M. and Valentin-Hansen, P. (2006) Conserved small non-coding RNAs that belong to the sigmaE regulon: role in down-regulation of outer membrane proteins. J. Mol. Biol., 364, 1-8. (Pubitemid 44634530)
7. Alba, B.M. and Gross, CA. (2004) Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Microbiol., 52, 613-619. (Pubitemid 38621733)
8. Ruiz, N. and Silhavy, T.J. (2005) Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol., 8, 122-126. (Pubitemid 40417951)
9. Figueroa-Bossi, N., Lemire, S., Maloriol, D., Balbontin, R., Casadesus, J. and Bossi, L. (2006) Loss of Hfq activates the sigmaE-dependent envelope stress response in Salmonella enterica. Mol. Microbiol., 62, 838-852. (Pubitemid 44571606)
10. Vogel, J. and Wagner, E.G (2007) Target identification of small noncoding RNAs in bacteria. Curr. Opin. Microbiol., 10, 262-270. (Pubitemid 46963091)
11. Waters, L.S. and Storz, G (2009) Regulatory RNAs in bacteria. Cell, 136, 615-628.
12. Masse, E., Escorcia, F.E. and Gottesman, S. (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev., 17, 2374-2383. (Pubitemid 37214786)
13. Vogel, J., Argaman, L., Wagner, E.G and Altuvia, S. (2004) The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr. Biol., 14, 2271-2276. (Pubitemid 40033365)
14. Afonyushkin, T., Vecerek, B., Moll, I., Blasi, U. and Kaberdin, V.R. (2005) Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB. Nucleic Acids Res., 33, 1678-1689. (Pubitemid 41418396)
15. Morita, T., Maki, K. and Aiba, H. (2005) RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev., 19, 2176-2186. (Pubitemid 41330319)
16. Andrade, J.M. and Arraiano, C.M. (2008) PNPase is a key player in the regulation of small RNAs that control the expression of outer membrane proteins. RNA, 14, 543-551. (Pubitemid 351397819)
17. Viegas, S.C., Pfeiffer, V., Sittka, A., Silva, I.J., Vogel, J. and Arraiano, C.M. (2007) Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res., 35, 7651-7664.
18. Viegas, S.C. and Arraiano, C.M. (2008) Regulating the regulators: How ribonucleases dictate the rules in the control of small non-coding RNAs. RNA Biol., 5, 230-243.
19. Arraiano, C.M., Andrade, J.M., Domingues, S., Guinote, I.B., Malecki, M., Matos, R.G., Moreira, R.N., Pobre, V., Reis, F.P., Saramago, M. et al. (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol. Rev., 34, 883-923.
20. Carpousis, A.J., Luisi, B.F. and McDowall, K.J. (2009) Endonucleolytic initiation of mRNA decay in Escherichia coli. Prog. Mol. Biol. Transl. Sci., 85, 91-135.
21. Conrad, C. and Rauhut, R. (2002) Ribonuclease III: new sense from nuisance. Int. J. Biochem. Cell Biol., 34, 116-129. (Pubitemid 34112521)
22. Andrade, J.M., Pobre, V., Silva, I.J., Domingues, S. and Arraiano, C.M. (2009) The role of 3'-5' exoribonucleases in RNA degradation. Prog. Mol. Biol. Transl. Sci., 85, 187-229.
23. Kaberdin, V.R. and Blasi, U. (2006) Translation initiation and the fate of bacterial mRNAs. FEMS Microbiol. Rev., 30, 967-979. (Pubitemid 44583798)
24. Datsenko, KA. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad. Sci. USA, 97, 6640-6645. (Pubitemid 30412767)
25. Schmieger, H. (1971) The fate of the bacterial chromosome in P22-infected cells of Salmonella typhimurium. Mol. Gen. Genet., 110, 238-244.
26. Mattatall, N.R. and Sanderson, K.E. (1998) RNase III deficient Salmonella typhimurium LT2 contains intervening sequences (IVSs) in its 23S rRNA. FEMS Microbiol. Lett., 159, 179-185. (Pubitemid 28073888)
27. McDowall, KJ. and Cohen, S.N. (1996) The N-terminal domain of the rne gene product has RNase E activity and is non-overlapping with the arginine-rich RNA-binding site. J. Mol. Biol., 255, 349-355. (Pubitemid 26105558)
28. Amarasinghe, A.K., Calin-Jageman, I., Harmouch, A., Sun, W. and Nicholson, A.W. (2001) Escherichia coli ribonuclease III: affinity purification of hexahistidine-tagged enzyme and assays for substrate binding and cleavage. Methods Enzymol., 342, 143-158. (Pubitemid 32911940)
29. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
30. Chelladurai, B.S., Li, H. and Nicholson, A.W. (1991) A conserved sequence element in ribonuclease III processing signals is not required for accurate in vitro enzymatic cleavage. Nucleic Acids Res., 19, 1759-1766. (Pubitemid 21913276)
31. Jiang, X., Diwa, A. and Belasco, J.G (2000) Regions of RNase E important for 5'-end-dependent RNA cleavage and autoregulated synthesis. J. Bacteriol., 182, 2468-2475. (Pubitemid 30212904)
32. Matsuyama, S., Inokuchi, K. and Mizushima, S. (1984) Promoter exchange between ompF and ompC, genes for osmoregulated major outer membrane proteins of Escherichia coli K-12. J. Bacteriol., 158, 1041-1047. (Pubitemid 14088676)
33. Udekwu, K.I., Darfeuille, F., Vogel, J., Reimegard, J., Holmqvist, E. and Wagner, E.G (2005) Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev., 19, 2355-2366. (Pubitemid 41396912)
34. Bossi, L. and Figueroa-Bossi, N. (2007) A small RNA downregulates LamB maltoporin in Salmonella. Mol. Microbiol., 65, 799-810. (Pubitemid 47077237)
35. Rasmussen, AA., Eriksen, M., Gilany, K., Udesen, C., Franch, T., Petersen, C. and Valentin-Hansen, P. (2005) Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol. Microbiol., 58, 1421-1429. (Pubitemid 41705419)
36. Mackie, GA. (1998) Ribonuclease E is a 5'-end-dependent endonuclease. Nature, 395, 720-723.
37. Kaberdin, V.R., WalshA.P., Jakobsen, T., McDowall, K.J. and von Gabain, A. (2000) Enhanced cleavage of RNA mediated by an interaction between substrates and the arginine-rich domain of E. coli ribonuclease E. J. Mol. Biol., 301, 257-264.
38. Lin-Chao, S. and Cohen, S.N. (1991) The rate of processing and degradation of antisense RNAI regulates the replication of ColE1-type plasmids in vivo. Cell, 65, 1233-1242. (Pubitemid 121001336)
39. Mackie, G.A. (2000) Stabilization of circular rpsT mRNA demonstrates the 5'-end dependence of RNase E action in vivo. J. Biol. Chem., 275, 25069-25072.
40. Celesnik, H., DeanaA. and Belasco, J.G. (2007) Initiation of RNA decay in Escherichia coli by 5' pyrophosphate removal. Mol. Cell, 27, 79-90. (Pubitemid 46991386)
41. Kime, L., Jourdan, S.S., Stead, JA., Hidalgo-SastreA. and McDowall, K.J. (2010) Rapid cleavage of RNA by RNase E in the absence of 5' monophosphate stimulation. Mol. Microbiol., 76, 590-604.
42. Rowley, G., Spector, M., Kormanec, J. and Roberts, M. (2006) Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol., 4, 383-394. (Pubitemid 43771856)
43. Nicholson, A.W. (1999) Function, mechanism and regulation of bacterial ribonucleases. FEMS Microbiol. Rev., 23, 371-390. (Pubitemid 29236184)
44. Simons, R.W. and Kleckner, N. (1988) Biological regulation by antisense RNA in prokaryotes. Annu. Rev. Genet., 22, 567-600.
45. Krinke, L. and Wulff, D.L. (1987) OOP RNA, produced from multicopy plasmids, inhibits lambda cII gene expression through an RNase III-dependent mechanism. Genes Dev., 1, 1005-1013.
46. Jerome, L.J., van Biesen, T. and Frost, L.S. (1999) Degradation of FinP antisense RNA from F-like plasmids: the RNA-binding protein, FinO, protects FinP from ribonuclease E. J. Mol. Biol., 285, 1457-1473. (Pubitemid 29060448)
47. Gerdes, K., Nielsen, A., Thorsted, P. and Wagner, E.G (1992) Mechanism of killer gene activation. Antisense RNA-dependent RNase III cleavage ensures rapid turn-over of the stable hok, srnB and pndA effector messenger RNAs. J. Mol. Biol., 226, 637-649.
48. Storz, G, Altuvia, S. and Wassarman, K.M. (2005) An abundance of RNA regulators. Annu. Rev. Biochem., 74, 199-217. (Pubitemid 40995506)
49. Darfeuille, F., Unoson, C., Vogel, J. and Wagner, E.G (2007) An antisense RNA inhibits translation by competing with standby ribosomes. Mol. Cell, 26, 381-392. (Pubitemid 46687099)
50. Huntzinger, E., Boisset, S., Saveanu, C., Benito, Y., Geissmann, T., Namane, A., Lina, G, Etienne, J., Ehresmann, B., Ehresmann, C. et al. (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J., 24, 824-835. (Pubitemid 40396111)
51. Boisset, S., Geissmann, T., Huntzinger, E., Fechter, P., Bendridi, N., Possedko, M., Chevalier, C., Helfer, A.C., Benito, Y., Jacquier, A. et al. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev., 21, 1353-1366. (Pubitemid 46871039)
52. Coornaert, A., Lu, A., Mandin, P., Springer, M., Gottesman, S. and Guillier, M. (2010) MicA sRNA links the PhoP regulon to cell envelope stress. Mol. Microbiol., 76, 467-479.
53. Vogel, J. and Papenfort, K. (2006) Small non-coding RNAs and the bacterial outer membrane. Curr. Opin. Microbiol., 9, 605-611. (Pubitemid 44791989)
54. Kawamoto, H., Koide, Y., Morita, T. and Aiba, H. (2006) Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol. Microbiol., 61, 1013-1022. (Pubitemid 44134177)
55. Melefors, O. and von Gabain, A. (1988) Site-specific endonucleolytic cleavages and the regulation of stability of E. coli ompA mRNA. Cell, 52, 893-901.
56. Vytvytska, O., Jakobsen, J.S., Balcunaite, G, Andersen, J.S., Baccarini, M. and von Gabain, A. (1998) Host factor I, Hfq, binds to Escherichia coli ompA mRNA in a growth rate-dependent fashion and regulates its stability. Proc Natl Acad. Sci. USA, 95, 14118-14123. (Pubitemid 28549330)
57. Hoiseth, S.K. and Stocker, BA. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature, 291, 238-239. (Pubitemid 11081517)
58. Studier, F.W. and Moffatt, BA. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol., 189, 113-130.