Post-Transcriptional Control of the Escherichia coli PhoQ-PhoP Two-Component System by Multiple sRNAs Involves a Novel Pairing Region of GcvB

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Coornaert, Audrey ^a   Chiaruttini, Claude ^a   Springer, Mathias ^a   Guillier, Maude ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI PROTEIN; MESSENGER RNA; PHOP PROTEIN; PROTEIN GCVB; PROTEIN MICA; PROTEIN PHOQ; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME PAIRING; ESCHERICHIA COLI; GENE EXPRESSION; GENE REPRESSION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OPERON; PROTEIN RNA BINDING; PROTEIN SYNTHESIS REGULATION; REGULON; RNA DEGRADATION; TRANSCRIPTION REGULATION; TRANSLATION INITIATION;

DNA GLYCOSYLASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MAGNESIUM; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; REGULON; RIBOSOMES; RNA STABILITY;

EID: 84873504430     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003156     Document Type: Article

References (48)

1. Romby P, Springer M (2007) Translational control in prokaryotes. In: Matthews MB, Sonenberg N, Hershey JWB, editors. Translational control in Biology and Medecine: Cold Spring Harbor Laboratory Press. pp 803-827.
2. Mizuno T, Chou M-Y, 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.
3. Storz G, Vogel J, Wassarman KM, (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43: 880-891.
4. Prévost K, Desnoyers G, Jacques JF, Lavoie F, Massé E, (2011) Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage. Genes Dev 25: 385-396.
5. McCullen CA, Benhammou JN, Majdalani N, Gottesman S, (2010) Mechanism of positive regulation by DsrA and RprA small noncoding RNAs: pairing increases translation and protects rpoS mRNA from degradation. J Bacteriol 192: 5559-5571.
6. Obana N, Shirahama Y, Abe K, Nakamura K, (2010) Stabilization of Clostridium perfringens collagenase mRNA by VR-RNA-dependent cleavage in 5′ leader sequence. Mol Microbiol 77: 1416-1428.
7. Ramirez-Pena E, Trevino J, Liu Z, Perez N, Sumby P, (2010) The group A Streptococcus small regulatory RNA FasX enhances streptokinase activity by increasing the stability of the ska mRNA transcript. Mol Microbiol 78: 1332-1347.
8. Mandin P, Gottesman S, (2010) Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29: 3094-3107.
9. 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.
10. Stauffer LT, Stauffer GV, (1994) Characterization of the gcv control region from Escherichia coli. J Bacteriol 176: 6159-6164.
11. Modi SR, Camacho DM, Kohanski MA, Walker GC, Collins JJ, (2011) Functional characterization of bacterial sRNAs using a network biology approach. Proc Natl Acad Sci USA 108: 15522-15527.
12. Sharma CM, Darfeuille F, Plantinga TH, Vogel J, (2007) A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev 21: 2804-2817.
13. Sharma CM, Papenfort K, Pernitzsch SR, Mollenkopf HJ, Hinton JC, et al. (2011) Pervasive post-transcriptional control of genes involved in amino acid metabolism by the Hfq-dependent GcvB small RNA. Mol Microbiol 81: 1144-1165.
14. Pulvermacher SC, Stauffer LT, Stauffer GV, (2009) The small RNA GcvB regulates sstT mRNA expression in Escherichia coli. J Bacteriol 191: 238-248.
15. 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.
16. 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.
17. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, et al. (1998) The oxyS regulatory RNA represses rpoS translation by binding Hfq (HF-1) protein. EMBO J 17: 6061-6068.
18. Guillier M, Gottesman S, (2008) The 5′ end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res 36: 6781-6794.
19. 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.
20. Gogol EB, Rhodius VA, Papenfort K, Vogel J, Gross CA, (2011) Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon. Proc Natl Acad Sci U S A 108: 12875-12880.
21. Udekwu KI, Darfeuille F, Vogel J, Reimegard J, Holmqvist E, et al. (2005) Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes & Dev 19: 2355-2366.
22. Rasmussen AA, Eriksen M, Gilany K, Udesen C, Franch T, et al. (2005) Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol Microbiol 58: 1421-1429.
23. Bossi L, Figueroa-Bossi N, (2007) A small RNA downregulates LamB maltoporin in Salmonella. Mol Microbiol 65: 799-810.
24. Coornaert A, Lu A, Mandin P, Springer M, Gottesman S, et al. (2010) MicA sRNA links the PhoP regulon to cell envelope stress. Mol Microbiol 76: 467-479.
25. Zwir I, Shin D, Kato A, Nishino K, Latifi T, et al. (2005) Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci USA 102: 2862-2867.
26. Kato A, Tanabe H, Utsumi R, (1999) Molecular characterization of the PhoP-PhoQ two-component system in Escherichia coli K-12: identification of extracellular Mg2+-responsive promoters. J Bacteriol 181: 5516-5520.
27. Rice JB, Vanderpool CK, (2011) The small RNA SgrS controls sugar-phosphate accumulation by regulating multiple PTS genes. Nucleic Acids Res 39: 3806-3819.
28. Moon K, Gottesman S, (2011) Competition among Hfq-binding small RNAs in Escherichia coli. Mol Microbiol 82: 1545-1562.
29. Balbontin R, Fiorini F, Figueroa-Bossi N, Casadesus J, Bossi L, (2010) Recognition of heptameric seed sequence underlies multi-target regulation by RybB small RNA in Salmonella enterica. Mol Microbiol 78: 380-394.
30. Papenfort K, Bouvier M, Mika F, Sharma CM, Vogel J, (2010) Evidence for an autonomous 5′ target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci USA 107: 20435-20440.
31. Tjaden B, (2008) TargetRNA: a tool for predicting targets of small RNA action in bacteria. Nucleic Acids Res 36: W109-113.
32. Hussein R, Lim HN, (2010) Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci USA 108: 1110-1115.
33. Peer A, Margalit H, (2011) Accessibility and evolutionary conservation mark bacterial small-rna target-binding regions. J Bacteriol 193: 1690-1701.
34. Stauffer LT, Stauffer GV, (2012) The Escherichia coli GcvB sRNA uses genetic redundancy to control cycA expression. ISRN Microbiology 2012: Article ID 636273.
35. Park SY, Cromie MJ, Lee EJ, Groisman EA, (2010) A bacterial mRNA leader that employs different mechanisms to sense disparate intracellular signals. Cell 142: 737-748.
36. Lee EJ, Groisman EA, (2012) Tandem attenuators control expression of the Salmonella mgtCBR virulence operon. Mol Microbiol 86: 212-224.
37. Eguchi Y, Okada T, Minagawa S, Oshima T, Mori H, et al. (2004) Signal transduction cascade between EvgA/EvgS and PhoP/PhoQ two-component systems of Escherichia coli. J Bacteriol 186: 3006-3014.
38. Raghavan R, Groisman EA, Ochman H, (2011) Genome-wide detection of novel regulatory RNAs in E. coli. Genome Res 21: 1487-1497.
39. Gopel Y, Gorke B, (2012) Rewiring two-component signal transduction with small RNAs. Curr Opin Microbiol 15: 132-139.
40. Beisel CL, Storz G, (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34: 866-882.
41. Bougdour A, Cunning C, Baptiste PJ, Elliott T, Gottesman S, (2008) Multiple pathways for regulation of sigmaS (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol Microbiol 68: 298-313.
42. Lutz R, 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.
43. Moon K, Gottesman S, (2009) A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 74: 1314-1330.
44. Morita T, Kawamoto H, Mizota T, Inada T, Aiba H, (2004) Enolase in RNA degradosome plays a crucial role in the rapid decay of glucose transporteer mRNA in response to metabolic stress in Escherichia coli. Mol Microbiol 54: 1063-1075.
45. Miller JH (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.
46. Schupp JM, Trais SE, Price LB, Shand RF, Keim P, (1995) Rapid bacterial permeabilization reagent useful for enzyme assays. Biotechniques 19: 18-19.
47. Guillier M, Gottesman S, (2006) Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 59: 231-247.
48. Hartz D, McPheeters DS, Traut R, Gold L, (1988) Extension inhibition analysis of translation initiation complexes. Methods Enzymol 164: 419-425.