Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA

EMBO Journal

Volumn 29, Issue 18, 2010, Pages 3094-3107

  Mandin, Pierre ^a   Gottesman, Susan ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

ArcA; ArcZ; Hfq; RpoS

Indexed keywords

BETA GALACTOSIDASE; PROTEIN DSRA; PROTEIN OXYS; PROTEIN RPRA; RIBOSOME RNA; SIGMA FACTOR RPOS; UNCLASSIFIED DRUG; UNTRANSLATED RNA; BACTERIAL RNA; HOST FACTOR 1; OXYGEN; SIGMA FACTOR;

ANAEROBIC GROWTH; ARCA GENE; ARCB GENE; ARTICLE; BACTERIAL GENE; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; NEGATIVE FEEDBACK; PRIORITY JOURNAL; REGULON; SEQUENCE ALIGNMENT; STRESS; UNTRANSLATED REGION; AEROBIC METABOLISM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEQUENCE HOMOLOGY;

AEROBIOSIS; ANAEROBIOSIS; BASE SEQUENCE; BLOTTING, NORTHERN; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; MOLECULAR SEQUENCE DATA; OXYGEN; RNA, BACTERIAL; RNA, UNTRANSLATED; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIGMA FACTOR;

ARCA; ESCHERICHIA COLI;

EID: 77956879952     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.179     Document Type: Article

References (71)

1. Aiso T, Ohki R (2003) Instability of sensory histidine kinase mRNAs in Escherichia coli. Genes Cells 8: 179-187
2. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G (1997) A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 90: 43-53
3. Antal M, Bordeau V, Douchin V, Felden B (2005) A small bacterial RNA regulates a putative ABC transporter. J Biol Chem 280: 7901-7908
4. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, Altuvia S (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11 : 941-950
5. Bongaerts J, Zoske S, Weidner U, Unden G (1995) Transcrip-tional regulation of the proton translocating NADH dehydrogen-ase genes (nuoA-N) of Escherichia coli by electron acceptors, electron donors and gene regulators. Mol Microbiol 16: 521-534
6. Bouché F, Bouché JP (1989) Genetic evidence that DicF, a second division inhibitor encoded by the Escherichia coli dicB operon, is probably RNA. Mol Microbiol 3: 991-994
7. S (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol Microbiol 68: 298-313
8. S stability in Escherichia coli. Genes Dev 20: 884-897
9. Brennan RG, Link TM (2007) Hfq structure, function and ligand binding. Curr Opin Microbiol 10: 125-133
10. Brown L, Elliott T (1996) Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol 178: 3763-3770
11. Brown L, Elliott T (1997) Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J Bacteriol 179: 656-662
12. Chen S, Zhang A, Blyn LB, Storz G (2004) MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol 186: 6689-6697
13. Chung CT, Miller RH (1988) A rapid and convenient method for the preparation and storage of competent bacterial cells. Nucleic Acids Res 16: 3580
14. Coornaert A, Lu A, Mandin P, Springer M, Gottesman S, Guillier M (2010) MicA sRNA links the PhoP regulon to cell envelope stress. Mol Microbiol 76: 467-479
15. De Lay N, Gottesman S (2009) The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 191: 461-476
16. Douchin V, Bohn C, Bouloc P (2006) Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramem-brane proteolysis protease RseP in Escherichia coli. J Biol Chem 281: 12253-12259
17. Durand S, Storz G (2010) Reprogramming of anaerobic metabolism by the FnrS small RNA. Mol Microbiol 75: 1215-1231
18. Georgellis D, Kwon O, Lin EC (2001) Quinones as the redox signal for the arc two-component system of bacteria. Science 292: 2314-2316
19. Gottesman S (2004) The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 58: 303-328
20. Gottesman S, McCullen CA, Guillier M, Vanderpool CK, Majdalani N, Benhammou J, Thompson KM, Fitz Gerald PC, Sowa NA, Fitz Gerald DJ (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71: 1-11
21. Guillier M, Gottesman S (2006) Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 59: 231-247
22. Gunsalus RP, Park SJ (1994) Aerobic-anaerobic gene regulation in Escherichia coli: control by the ArcAB and Fnr regulons. Res Microbiol 145: 437-450
23. S (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66: 373-395
24. Jousselin A, Metzinger L, Felden B (2009) On the facultative requirement of the bacterial RNA chaperone, Hfq. Trends Microbiol 17: 399-405
25. Kim SJ, Han YH, Kim IH, Kim HK (1999) Involvement of ArcA and Fnr in expression of Escherichia coli thiol peroxidase gene. IUBMB Life 48: 215-218
26. S subunit of RNA polymerase in Escherichia coli. J Bacteriol 177: 4676-4680
27. Lease RA, Cusick M, Belfort M (1998) Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci USA 95: 12456-12461
28. Majdalani N, Chen S, Murrow J, St John K, Gottesman S (2001) Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol 39: 1382-1394
29. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S (1998) DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci USA 95: 12462-12467
30. Majdalani N, Hernandez D, Gottesman S (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46: 813-826
31. Malpica R, Franco B, Rodriguez C, Kwon O, Georgellis D (2004) Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc Natl Acad Sci USA 101: 13318-13323
32. Malpica R, Sandoval GR, Rodriguez C, Franco B, Georgellis D (2006) Signaling by the arc two-component system provides a link between the redox state of the quinone pool and gene expression. Antioxid Redox Signal 8: 781-795
33. Mandin P, Gottesman S (2009) A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA-DpiB two-component system. Mol Microbiol 72: 551-565
34. Massé E, Escorcia FE, Gottesman S (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17: 2374-2383
35. Massé E, 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
36. McGuire AM, De Wulf P, Church GM, Lin EC (1999) Aweight matrix for binding recognition by the redox-response regulator ArcA-P of Escherichia coli. Mol Microbiol 32: 219-221
37. S (RpoS) in E. coli. Genes Dev 19: 2770-2781
38. Miller J (1992) A Short Course in Bacterial Genetics: A laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
39. Mizuno T, Chou MY, 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
40. Mller T, Franch T, Udesen C, Gerdes K, Valentin-Hansen P (2002) Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 16: 1696-1706
41. Moon K, Gottesman S (2009) A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 74: 1314-1330
42. Morita T, Kawamoto H, Mizota T, Inada T, Aiba H (2004) Enolase in the RNA degradosome plays a crucial role in the rapid decay of glucose transporter mRNA in the response to phosphosugar stress in Escherichia coli. Mol Microbiol 54: 1063-1075
43. Muffler A, Fischer D, Hengge-Aronis R (1996) The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev 10: 1143-1151
44. Opdyke JA, Kang JG, Storz G (2004) GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186: 6698-6705 (Pubitemid 39332106)
45. Papenfort K, Pfeiffer V, Lucchini S, Sonawane A, Hinton JC, Vogel J (2008) Systematic deletion of Salmonella small RNA genes iden tifies CyaR, a conserved CRP-dependent riboregulator of OmpX synthesis. Mol Microbiol 68: 890-906
46. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74: 139-158
47. Reams SG, Lee N, Mat-Jan F, Clark DP (1997) Effect of chelating agents and respiratory inhibitors on regulation of the cadA gene in Escherichia coli. Arch Microbiol 167: 209-216
48. Repoila F, Majdalani N, Gottesman S (2003) Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol Microbiol 48: 855-861
49. Ruiz N, Silhavy TJ (2003) Constitutive activation of the Escherichia coli Pho regulon upregulates rpoS translation in an Hfq-dependent fashion. J Bacteriol 185: 5984-5992
50. Schurdell MS, Woodbury GM, McCleary WR (2007) Genetic evidence suggests that the intergenic region between pstA and pstB plays a role in the regulation of rpoS translation during phosphate limitation. J Bacteriol 189: 1150-1153
51. Shalel-Levanon S, San KY, Bennett GN (2005) Effect of ArcA and FNR on the expression of genes related to the oxygen regulation and the glycolysis pathway in Escherichia coli under microaerobic growth conditions. Biotechnol Bioeng 92: 147-159
52. Sharma CM, Vogel J (2009) Experimental approaches for the discovery and characterization of regulatory small RNA. Curr Opin Microbiol 12: 536-546
53. Silhavy T, Berman M, Enquist L (1984) Experiments with Gene Fusions. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory
54. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, Hinton JC, Vogel J (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcrip-tional regulator, Hfq. PLoS Genet 4: e1000163
55. Sledjeski DD, Gupta A, Gottesman S (1996) The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J 15: 3993-4000
56. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA (2010) Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci USA 107 : 9602-9607
57. Soper TJ, Woodson SA (2008) The rpoS mRNA leader recruits Hfq to facilitate annealing with DsrA sRNA. RNA 14: 1907-1917
58. S by the proteolytic targeting factor RssB and ClpX. EMBO J 22: 4111-4120
59. E regulates and is regulated by a small RNA in Escherichia coli. J Bacteriol 189: 4243-4256
60. Udekwu KI, Darfeuille F, Vogel J, Reimegard J, Holmqvist E, Wagner EG (2005) Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 19: 2355-2366
61. 0 rpoS mRNA leader region. Biochemistry 47: 11184-11195
62. Urban JH, Vogel J (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 35: 1018-1037
63. Urban JH, Vogel J (2008) Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6: e64
64. Urbanowski ML, Stauffer LT, Stauffer GV (2000) The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol Microbiol 37: 856-868
65. Vanderpool CK, Gottesman S (2004) Involvement of a novel tran-scriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54: 1076-1089
66. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Huttenhofer A, Wagner EG (2003) RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31: 6435-6443
67. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 15: 1637-1651
68. Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136: 615-628
69. S-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187: 1591-1603
70. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17: 6061-6068
71. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, Gottesman S (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50: 1111-1124