σ E ‐dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay

Abstract

Summary The bacterial envelope stress response (ESR) is triggered by the accumulation of misfolded outer membrane proteins (OMPs) upon envelope damage or excessive OMP synthesis, and is mediated by the alternative sigma factor, σ E . Activation of the σ E pathway causes a rapid downregulation of major omp mRNAs, which prevents further build‐up of unassembled OMPs and liberates the translocation and folding apparatus under conditions that require envelope remodelling. The factors that facilitate the rapid removal of the unusually stable omp mRNAs in the ESR were previously unknown. We report that in Salmonella the ESR relies upon two highly conserved, σ E ‐controlled small non‐coding RNAs, RybB and MicA. By using a transcriptomic approach and kinetic analyses of target mRNA decay in vivo , RybB was identified as the factor that selectively accelerates the decay of multiple major omp mRNAs upon induction of the ESR, while MicA is proposed to facilitate rapid decay of the single ompA mRNA. In unstressed bacterial cells, the two σ E ‐dependent small RNAs function within a surveillance loop to maintain envelope homeostasis and to achieve autoregulation of σ E .

Shown for reading. Its publisher allows quoting it, not republishing it.

References 68

1. 1.

   Ades SE, Connolly LE, Alba BM, Gross CA. The Escherichia coli sigma(E)-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Genes Dev. 1999;13:2449-2461.

   Not in our library10.1101/gad.13.18.2449

2. 2.

   Argaman L, Altuvia S. fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense-target RNA complex. J Mol Biol. 2000;300:1101-1112.

   Not in our library10.1006/jmbi.2000.3942

3. 3.

   Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol. 2001;11:941-950.

   Not in our library10.1016/s0960-9822(01)00270-6

4. 4.

   Chen S, Zhang A, Blyn LB, Storz G. MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol. 2004;186:6689-6697.

   Not in our library10.1128/jb.186.20.6689-6697.2004

5. 5.

   Dartigalongue C, Missiakas D, Raina S. Characterization of the Escherichia coli sigma E regulon. J Biol Chem. 2001;276:20866-20875.

   Not in our library10.1074/jbc.m100464200

6. 6.
   One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products · 2000

   Not checked
7. 7.

   Deana A, Belasco JG. Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev. 2005;19:2526-2533.

   Not in our library10.1101/gad.1348805

8. 8.

   Ding Y, Davis BM, Waldor MK. Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol Microbiol. 2004;53:345-354.

   Not in our library10.1111/j.1365-2958.2004.04142.x

9. 9.

   Douchin V, Bohn C, Bouloc P. Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. J Biol Chem. 2006;281:12253-12259.

   Not in our library10.1074/jbc.m600819200

10. 10.

    Figueroa-Bossi N, Lemire S, Maloriol D, Balbontin R, Casadesus J, Bossi L. Loss of Hfq activates the sigma-dependent envelope stress response in Salmonella enterica. Mol Microbiol. 2006;62:838-852.

    Not in our library10.1111/j.1365-2958.2006.05413.x

11. 11.

    von Gabain A, Belasco JG, Schottel JL, Chang AC, Cohen SN. Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc Natl Acad Sci USA. 1983;80:653-657.

    Not in our library10.1073/pnas.80.3.653

12. 12.

    Geissmann TA, Touati D. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J. 2004;23:396-405.

    Not in our library10.1038/sj.emboj.7600058

13. 13.

    Gottesman S. The small RNA regulators of Escherichia coli: roles and mechanisms*. Annu Rev Microbiol. 2004;58:303-328.

    Not in our library10.1146/annurev.micro.58.030603.123841

14. 14.

    Guillier M, Gottesman S. Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol. 2006;59:231-247.

    Not in our library10.1111/j.1365-2958.2005.04929.x

15. 15.

    Guillier M, Gottesman S, Storz G. Modulating the outer membrane with small RNAs. Genes Dev. 2006;20:2338-2348.

    Not in our library10.1101/gad.1457506

16. 16.

    Guzman LM, Belin D, Carson MJ, Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol. 1995;177:4121-4130.

    Not in our library10.1128/jb.177.14.4121-4130.1995

17. 17.

    Hershberg R, Altuvia S, Margalit H. A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res. 2003;31:1813-1820.

    Not in our library10.1093/nar/gkg297

18. 18.

    Hoiseth SK, Stocker BA. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature. 1981;291:238-239.

    Not in our library10.1038/291238a0

19. 19.

    Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science. 2006;313:104-107.

    Not in our library10.1126/science.1129631

20. 20.

    Humphreys S, Stevenson A, Bacon A, Weinhardt AB, Roberts M. The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect Immun. 1999;67:1560-1568.

    Not in our library10.1128/iai.67.4.1560-1568.1999

21. 21.

    Johansen J, Rasmussen AA, Overgaard M, Valentin-Hansen P. Conserved small non-coding RNAs that belong to the sigma(E) regulon: role in down-regulation of outer membrane proteins. J Mol Biol. 2006;364:1-8.

    Not in our library10.1016/j.jmb.2006.09.004

22. 22.

    Kawamoto H, Koide Y, Morita T, Aiba H. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol Microbiol. 2006;61:1013-1022.

    Not in our library10.1111/j.1365-2958.2006.05288.x

23. 23.

    Kelly A, Goldberg MD, Carroll RK, Danino V, Hinton JC, Dorman CJ. A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology. 2004;150:2037-2053.

    Not in our library10.1099/mic.0.27209-0

24. 24.

    Koebnik R, Locher KP, Van Gelder P. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol. 2000;37:239-253.

    Not in our library10.1046/j.1365-2958.2000.01983.x

25. 25.

    Lee DR, Schnaitman CA. Comparison of outer membrane porin proteins produced by Escherichia coli and Salmonella typhimurium. J Bacteriol. 1980;142:1019-1022.

    Not in our library10.1128/jb.142.3.1019-1022.1980

26. 26.

    Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell. 2004;118:69-82.

    Not in our library10.1016/j.cell.2004.06.009

27. 27.

    Lutz R, Bujard H. 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. 1997;25:1203-1210.

    Not in our library10.1093/nar/25.6.1203

28. 28.

    Majdalani N, Vanderpool CK, Gottesman S. Bacterial small RNA regulators. Crit Rev Biochem Mol Biol. 2005;40:93-113.

    Not in our library10.1080/10409230590918702

29. 29.

    Massé E, Gottesman S. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA. 2002;99:4620-4625.

    Not in our library10.1073/pnas.032066599

30. 30.

    Massé E, Escorcia FE, Gottesman S. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 2003;17:2374-2383.

    Not in our library10.1101/gad.1127103

31. 31.

    Massé E, Vanderpool CK, Gottesman S. Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol. 2005;187:6962-6971.

    Not in our library10.1128/jb.187.20.6962-6971.2005

32. 32.

    Mecsas J, Rouviere PE, Erickson JW, Donohue TJ, Gross CA. The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev. 1993;7:2618-2628.

    Not in our library10.1101/gad.7.12b.2618

33. 33.

    Missiakas D, Betton JM, Raina S. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol. 1996;21:871-884.

    Not in our library10.1046/j.1365-2958.1996.561412.x

34. 34.

    Miticka H, Rowley G, Rezuchova B, Homerova D, Humphreys S, Farn J, et al. Transcriptional analysis of the rpoE gene encoding extracytoplasmic stress response sigma factor sigmaE in Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett. 2003;226:307-314.

    Not in our library10.1016/s0378-1097(03)00600-1

35. 35.

    Mizuno T, Chou MY, Inouye M. A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci USA. 1984;81:1966-1970.

    Not in our library10.1073/pnas.81.7.1966

36. 36.

    Mock M, Pugsley AP. The BtuB group col plasmids and homology between the colicins they encode. J Bacteriol. 1982;150:1069-1076.

    Not in our library10.1128/jb.150.3.1069-1076.1982

37. 37.

    Morita T, Maki K, Aiba H. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev. 2005;19:2176-2186.

    Not in our library10.1101/gad.1330405

38. 38.

    Morita T, Mochizuki Y, Aiba H. Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc Natl Acad Sci USA. 2006;103:4858-4863.

    Not in our library10.1073/pnas.0509638103

39. 39.

    Nagy G, Danino V, Dobrindt U, Pallen M, Chaudhuri R, Emody L, et al. Down-regulation of key virulence factors makes the Salmonella enterica serovar Typhimurium rfaH mutant a promising live-attenuated vaccine candidate. Infect Immun. 2006;74:5914-5925.

    Not in our library10.1128/iai.00619-06

40. 40.

    Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev. 2003;67:593-656.

    Not in our library10.1128/mmbr.67.4.593-656.2003

41. 41.

    Paland N, Rajalingam K, Machuy N, Szczepek A, Wehrl W, Rudel T. NF-kappaB and inhibitor of apoptosis proteins are required for apoptosis resistance of epithelial cells persistently infected with Chlamydophila pneumoniae. Cell Microbiol. 2006;8:1643-1655.

    Not in our library10.1111/j.1462-5822.2006.00739.x

42. 42.

    Raivio TL, Silhavy TJ. The sigmaE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr Opin Microbiol. 1999;2:159-165.

    Not in our library10.1016/s1369-5274(99)80028-9

43. 43.

    Rasmussen AA, Eriksen M, Gilany K, Udesen C, Franch T, Petersen C, Valentin-Hansen P. Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol Microbiol. 2005;58:1421-1429.

    Not in our library10.1111/j.1365-2958.2005.04911.x

44. 44.
    Conserved and Variable Functions of the σE Stress Response in Related Genomes · 2005

    No notice
45. 45.

    Rowley G, Spector M, Kormanec J, Roberts M. Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat Rev Microbiol. 2006;4:383-394.

    Not in our library10.1038/nrmicro1394

46. 46.

    Ruiz N, Silhavy TJ. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol. 2005;8:122-126.

    Not in our library10.1016/j.mib.2005.02.013

47. 47.

    Schmidt M, Zheng P, Delihas N. Secondary structures of Escherichia coli antisense micF RNA, the 5′-end of the target ompF mRNA, and the RNA/RNA duplex. Biochemistry. 1995;34:3621-3631.

    Not in our library10.1021/bi00011a017

48. 48.

    Schmieger H. A method for detection of phage mutants with altered transducing ability. Mol Gen Genet. 1971;110:378-381.

    Not in our library10.1007/bf00438281

49. 49.
    The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium · 2006

    No notice
50. 50.

    Skovierova H, Rowley G, Rezuchova B, Homerova D, Lewis C, Roberts M, Kormanec J. Identification of the sigmaE regulon of Salmonella enterica serovar Typhimurium. Microbiology. 2006;152:1347-1359.

    Not in our library10.1099/mic.0.28744-0

51. 51.

    Storz G, Opdyke JA, Zhang A. Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol. 2004;7:140-144.

    Not in our library10.1016/j.mib.2004.02.015

52. 52.

    Storz G, Altuvia S, Wassarman KM. An abundance of RNA regulators. Annu Rev Biochem. 2005;74:199-217.

    Not in our library10.1146/annurev.biochem.74.082803.133136

53. 53.

    Testerman TL, Vazquez-Torres A, Xu Y, Jones-Carson J, Libby SJ, Fang FC. The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol Microbiol. 2002;43:771-782.

    Not in our library10.1046/j.1365-2958.2002.02787.x

54. 54.

    Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, Gottesman S, Storz G. Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res. 2006;34:2791-2802.

    Not in our library10.1093/nar/gkl356

55. 55.

    Udekwu KI, Darfeuille F, Vogel J, Reimegard J, Holmqvist E, Wagner EG. Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev. 2005;19:2355-2366.

    Not in our library10.1101/gad.354405

56. 56.

    Urban JH, Vogel J. Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res. 2006.

    Not in our library10.1093/nar/gkl1040

57. 57.

    Valentin-Hansen P, Eriksen M, Udesen C. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol. 2004;51:1525-1533.

    Not in our library10.1111/j.1365-2958.2003.03935.x

58. 58.

    Vanderpool CK, Gottesman S. Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol. 2004;54:1076-1089.

    Not in our library10.1111/j.1365-2958.2004.04348.x

59. 59.

    Vogel J, Papenfort K. Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol. 2006.

    Not in our library10.1016/j.mib.2006.10.006

60. 60.

    Vogel J, Sharma CS. How to find small non-coding RNAs in bacteria. Biol Chem. 2005;386:1219-1238.

    Not in our library10.1515/bc.2005.140

61. 61.

    Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Hüttenhofer A, Wagner EG. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res. 2003;31:6435-6443.

    Not in our library10.1093/nar/gkg867

62. 62.

    Vogel J, Argaman L, Wagner EG, Altuvia S. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol. 2004;14:2271-2276.

    Not in our library10.1016/j.cub.2004.12.003

63. 63.

    Vytvytska O, Jakobsen JS, Balcunaite G, Andersen JS, Baccarini M, von Gabain A. 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. 1998;95:14118-14123.

    Not in our library10.1073/pnas.95.24.14118

64. 64.

    Vytvytska O, Moll I, Kaberdin VR, von Gabain A, Bläsi U. Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev. 2000;14:1109-1118.

    Not in our library

65. 65.

    Wade JT, Roa DC, Grainger DC, Hurd D, Busby SJ, Struhl K, Nudler E. Extensive functional overlap between sigma factors in Escherichia coli. Nat Struct Mol Biol. 2006;13:806-814.

    Not in our library10.1038/nsmb1130

66. 66.

    Wagner EG, Darfeuille F, Nellen W. Small regulatory RNAs in bacteria. Small RNAs: Analysis and Regulatory Functions. 2006;1-30.

    Not in our library

67. 67.

    Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S. Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev. 2001;15:1637-1651.

    Not in our library10.1101/gad.901001

68. 68.

    Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S. Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol. 2003;50:1111-1124.

    Not in our library10.1046/j.1365-2958.2003.03734.x

Cited by papers we hold 14

• Pseudomonas aeruginosa: pathogenesis, virulence factors, antibiotic resistance, interaction with host, technology advances and emerging therapeutics · 2022
  No notice
• Maintaining Integrity Under Stress: Envelope Stress Response Regulation of Pathogenesis in Gram-Negative Bacteria · 2019
  No notice
• Molecular mechanism of mRNA repression in trans by a ProQ‐dependent small RNA · 2017
  No notice
• The Impact of 18 Ancestral and Horizontally-Acquired Regulatory Proteins upon the Transcriptome and sRNA Landscape of Salmonella enterica serovar Typhimurium · 2016
  No notice
• ChIP-Seq Analysis of the σE Regulon of Salmonella enterica Serovar Typhimurium Reveals New Genes Implicated in Heat Shock and Oxidative Stress Response. · 2015
  Not checked
• RNA-seq Brings New Insights to the Intra-Macrophage Transcriptome of Salmonella Typhimurium · 2015
  No notice
• Vibrio cholerae utilizes direct sRNA regulation in expression of a biofilm matrix protein. · 2014
  Not checked
• Small Regulatory RNAs in the Control of Motility and Biofilm Formation in E. coli and Salmonella · 2013
  No notice
• The Seed Region of a Small RNA Drives the Controlled Destruction of the Target mRNA by the Endoribonuclease RNase E · 2012
  No notice
• Global Analysis of Extracytoplasmic Stress Signaling in Escherichia coli · 2009
  No notice
• Two Seemingly Homologous Noncoding RNAs Act Hierarchically to Activate glmS mRNA Translation · 2008
  No notice
• A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles · 2008
  No notice
• Deep Sequencing Analysis of Small Noncoding RNA and mRNA Targets of the Global Post-Transcriptional Regulator, Hfq · 2008
  No notice
• The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium · 2006
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.