σE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay

Molecular Microbiology

Volumn 62, Issue 6, 2006, Pages 1674-1688

  Papenfort, Kai ^a   Pfeiffer, Verena ^a   Mika, Franziska ^a   Lucchini, Sacha ^b   Hinton, Jay C D ^b   Vogel, Jörg ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN A; SIGMA FACTOR; UNTRANSLATED RNA;

ARTICLE; AUTOREGULATION; CONTROLLED STUDY; ENVELOPE STRESS RESPONSE; HOMEOSTASIS; MEMBRANE DAMAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RNA STABILITY; SALMONELLA; STRESS; TRANSCRIPTOMICS; BIOLOGICAL MODEL; DNA MICROARRAY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

BACTERIA (MICROORGANISMS); SALMONELLA;

BACTERIAL OUTER MEMBRANE PROTEINS; BASE SEQUENCE; BLOTTING, NORTHERN; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA STABILITY; RNA, MESSENGER; RNA, UNTRANSLATED; SALMONELLA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIGMA FACTOR;

EID: 33751383274     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05524.x     Document Type: Article

References (68)

1. Ades, S.E., Connolly, L.E., Alba, B.M., and Gross, C.A. (1999) The Escherichia coli sigma(E)-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Genes Dev 13: 2449-2461.
2. Argaman, L., and Altuvia, S. (2000) fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense-target RNA complex. J Mol Biol 300: 1101-1112.
3. Argaman, L., Hershberg, R., Vogel, J., Bejerano, G., Wagner, E.G., Margalit, H., and Altuvia, S. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11: 941-950.
4. Chen, S., Zhang, A., Blyn, L.B., and Storz, G. (2004) MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol 186: 6689-6697.
5. Dartigalongue, C., Missiakas, D., and Raina, S. (2001) Characterization of the Escherichia coli sigma E regulon. J Biol Chem 276: 20866-20875.
6. Datsenko, K.A., 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.
7. Deana, A., and Belasco, J.G. (2005) Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev 19: 2526-2533.
8. Ding, Y., Davis, B.M., and Waldor, M.K. (2004) Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol Microbiol 53: 345-354.
9. Douchin, V., Bohn, C., and Bouloc, P. (2006) Downregulation 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.
10. Figueroa-Bossi, N., Lemire, S., Maloriol, D., Balbontin, R., Casadesus, J., and Bossi, L. (2006) Loss of Hfq activates the sigma-dependent envelope stress response in Salmonella enterica. Mol Microbiol 62: 838-852.
11. von Gabain, A., Belasco, J.G., Schottel, J.L., Chang, A.C., and Cohen, S.N. (1983) Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc Natl Acad Sci USA 80: 653-657.
12. Geissmann, T.A., and Touati, D. (2004) Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 23: 396-405.
13. Gottesman, S. (2004) The small RNA regulators of Escherichia coli: roles and mechanisms*. Annu Rev Microbiol 58: 303-328.
14. Guillier, M., and Gottesman, S. (2006) Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 59: 231-247.
15. Guillier, M., Gottesman, S., and Storz, G. (2006) Modulating the outer membrane with small RNAs. Genes Dev 20: 2338-2348.
16. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
17. Hershberg, R., Altuvia, S., and Margalit, H. (2003) A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res 31: 1813-1820.
18. Hoiseth, S.K., and Stocker, B.A. (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239.
19. Hollien, J., and Weissman, J.S. (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313: 104-107.
20. Humphreys, S., Stevenson, A., Bacon, A., Weinhardt, A.B., and Roberts, M. (1999) The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect Immun 67: 1560-1568.
21. Johansen, J., Rasmussen, A.A., Overgaard, M., and Valentin-Hansen, P. (2006) Conserved small non-coding RNAs that belong to the sigma(E) regulon: role in down-regulation of outer membrane proteins. J Mol Biol 364: 1-8.
22. 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.
23. Kelly, A., Goldberg, M.D., Carroll, R.K., Danino, V., Hinton, J.C., and Dorman, C.J. (2004) A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150: 2037-2053.
24. Koebnik, R., Locher, K.P., and Van Gelder, P. (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37: 239-253.
25. Lee, D.R., and Schnaitman, C.A. (1980) Comparison of outer membrane porin proteins produced by Escherichia coli and Salmonella typhimurium. J Bacteriol 142: 1019-1022.
26. Lenz, D.H., Mok, K.C., Lilley, B.N., Kulkarni, R.V., Wingreen, N.S., and Bassler, B.L. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69-82.
27. Lutz, R., and Bujard, H. (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25: 1203-1210.
28. Majdalani, N., Vanderpool, C.K., and Gottesman, S. (2005) Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40: 93-113.
29. Massé, E., and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99: 4620-4625.
30. Massé, E., Escorcia, F.E., and Gottesman, S. (2003) Coupled degradation of a small regulatory RNAand its mRNA targets in Escherichia coli. Genes Dev 17: 2374-2383.
31. Massé, E., Vanderpool, C.K., and Gottesman, S. (2005) Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187: 6962-6971.
32. Mecsas, J., Rouviere, P.E., Erickson, J.W., Donohue, T.J., and Gross, C.A. (1993) The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev 7: 2618-2628.
33. Missiakas, D., Betton, J.M., and Raina, S. (1996) New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol 21: 871-884.
34. Miticka, H., Rowley, G., Rezuchova, B., Homerova, D., Humphreys, S., Farn, J., et al. (2003) Transcriptional analysis of the rpoE gene encoding extracytoplasmic stress response sigma factor sigmaE in Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett 226: 307-314.
35. 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.
36. Mock, M., and Pugsley, A.P. (1982) The BtuB group col plasmids and homology between the colicins they encode. J Bacteriol 150: 1069-1076.
37. 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.
38. Morita, T., Mochizuki, Y., and Aiba, H. (2006) Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc Natl Acad Sci USA 103: 4858-4863.
39. Nagy, G., Danino, V., Dobrindt, U., Pallen, M., Chaudhuri, R., Emody, L., et al. (2006) Down-regulation of key virulence factors makes the Salmonella enterica serovar Typhimurium rfaH mutant a promising live-attenuated vaccine candidate. Infect Immun 74: 5914-5925.
40. Nikaido, H. (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67: 593-656.
41. Paland, N., Rajalingam, K., Machuy, N., Szczepek, A., Wehrl, W., and Rudel, T. (2006) NF-kappaB and inhibitor of apoptosis proteins are required for apoptosis resistance of epithelial cells persistently infected with Chlamydophila pneumoniae. Cell Microbiol 8: 1643-1655.
42. Raivio, T.L., and Silhavy, T.J. (1999) The sigmaE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr Opin Microbiol 2: 159-165.
43. Rasmussen, A.A., 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.
44. Rhodius, V.A., Suh, W.C., Nonaka, G., West, J., and Gross, C.A. (2006) Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 4: e2.
45. 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.
46. Ruiz, N., and Silhavy, T.J. (2005) Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 8: 122-126.
47. Schmidt, M., Zheng, P., and Delihas, N. (1995) Secondary structures of Escherichia coli antisense micF RNA, the 5′-end of the target ompF mRNA, and the RNA/RNA duplex. Biochemistry 34: 3621-3631.
48. Schmieger, H. (1971) A method for detection of phage mutants with altered transducing ability. Mol Gen Genet 110: 378-381.
49. Sittka, A., Pfeiffer, V., Tedin, K., and Vogel, J. (2006) The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol doi: 10.1111/j.1365-2958.2006.05489.x.
50. Skovierova, H., Rowley, G., Rezuchova, B., Homerova, D., Lewis, C., Roberts, M., and Kormanec, J. (2006) Identification of the sigmaE regulon of Salmonella enterica serovar Typhimurium. Microbiology 152: 1347-1359.
51. Storz, G., Opdyke, J.A., and Zhang, A. (2004) Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 7: 140-144.
52. Storz, G., Altuvia, S., and Wassarman, K.M. (2005) An abundance of RNA regulators. Annu Rev Biochem 74: 199-217.
53. Testerman, T.L., Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Libby, S.J., and Fang, F.C. (2002) The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol Microbiol 43: 771-782.
54. Tjaden, B., Goodwin, S.S., Opdyke, J.A., Guillier, M., Fu, D.X., Gottesman, S., and Storz, G. (2006) Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res 34: 2791-2802.
55. 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.
56. Urban, J.H., and Vogel, J. (2006) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res (in press).
57. Valentin-Hansen, P., Eriksen, M., and Udesen, C. (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 51: 1525-1533.
58. Vanderpool, C.K., and Gottesman, S. (2004) Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54: 1076-1089.
59. Vogel, J., and Papenfort, K. (2006) Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol doi: 10.1016/j.mib.2006.10.006.
60. Vogel, J., and Sharma, C.S. (2005) How to find small noncoding RNAs in bacteria. Biol Chem 386: 1219-1238.
61. Vogel, J., Bartels, V., Tang, T.H., Churakov, G., Slagter-Jager, J.G., Hüttenhofer, A., and Wagner, E.G. (2003) RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31: 6435-6443.
62. 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.
63. 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.
64. Vytvytska, O., Moll, I., Kaberdin, V.R., von Gabain, A., and Bläsi, U. (2000) Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev 14: 1109-1118.
65. Wade, J.T., Roa, D.C., Grainger, D.C., Hurd, D., Busby, S.J., Struhl, K., and Nudler, E. (2006) Extensive functional overlap between sigma factors in Escherichia coli. Nat Struct Mol Biol 13: 806-814.
66. Wagner, E.G., and Darfeuille, F. (2006) Small regulatory RNAs in bacteria. In Small RNAs: Analysis and Regulatory Functions. Nellen, W. (ed.). Springer Verlag: Berlin, pp. 1-30.
67. Wassarman, K.M., Repoila, F., Rosenow, C., Storz, G., and Gottesman, S. (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 15: 1637-1651.
68. Zhang, A., Wassarman, K.M., Rosenow, C., Tjaden, B.C., Storz, G., and Gottesman, S. (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50: 1111-1124.