Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation

PLoS Biology

Volumn 6, Issue 3, 2008, Pages 0631-0642

  Urban, Johannes H ^a   Vogel, Jörg ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; MESSENGER RNA; PROTEIN SUBUNIT; TRANSFER RNA; BACTERIAL PROTEIN; COMPONENT S, GLUTAMATE MUTASE PROTEIN, BACTERIA; ENZYME ACTIVATOR; ESCHERICHIA COLI PROTEIN; PCNB PROTEIN, E COLI; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; UNTRANSLATED RNA;

AMINO ACID METABOLISM; ARTICLE; CHROMOSOME; ESCHERICHIA COLI; NONHUMAN; POLYADENYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SEQUENCE; RNA STABILITY; RNA STRUCTURE; RNA TRANSLATION; SEQUENCE HOMOLOGY; WILD TYPE; BIOSYNTHESIS; CHEMISTRY; CONFORMATION; ENZYME ACTIVATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN SYNTHESIS; RNA PROCESSING;

ESCHERICHIA COLI;

BACTERIAL PROTEINS; BASE SEQUENCE; ENZYME ACTIVATION; ENZYME ACTIVATORS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; POLYADENYLATION; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN BIOSYNTHESIS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL; RNA, MESSENGER; RNA, UNTRANSLATED; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 41749124288     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060064     Document Type: Article

References (56)

1. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR (2004) Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428: 281-286.
2. Barrick JE, Corbino KA, Winkler WC, Nahvi A, Mandal M, et al. (2004) New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc Natl Acad Sci U S A 101: 6421-6426.
3. Urban JH, Papenfort K, Thomsen J, Schmitz RA, Vogel J (2007) A Conserved small RNA promotes discoordinate expression of the glmUS operon mRNA to activate GlmS synthesis. J Mol Biol 373: 521-528.
4. Kalamorz F, Reichenbach B, Marz W, Rak B, Görke B (2007) Feedback control of glucosamine-6-phosphate synthase GlmS expression depends on the small RNA GlmZ and involves the novel protein YhbJ in Escherichia coli. Mol Microbiol 65: 1518-1533.
5. Joanny G, Le Derout J, Brechemier-Baey D, Labas V, Vinh J, et al. (2007) Polyadenylation of a functional mRNA controls gene expression in Escherichia coli. Nucleic Acids Res 35: 2494-2502.
6. Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, et al. (2003) RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 31: 6435-6443.
7. Rivas E, Klein RJ, Jones TA, Eddy SR (2001) Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol 11: 1369-1373.
8. 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.
9. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, et al. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11: 941-950.
10. Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9: 11-22.
11. Møller T, Franch T, Hojrup P, Keene DR, Bachinger HP, et al. (2002) Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 9: 23-30.
12. Cao GJ, Sarkar N (1992) Identification of the gene for an Escherichia coli poly(A) polymerase. Proc Natl Acad Sci U S A 89: 10380-10384.
13. Kushner SR (2004) mRNA decay in prokaryotes and eukaryotes: different approaches to a similar problem. IUBMB Life 56: 585-594.
14. Dreyfus M, Regnier P (2002) The poly(A) tail of mRNAs: bodyguard in eukaryotes, scavenger in bacteria. Cell 111: 611-613.
15. Plumbridge J (1995) Co-ordinated regulation of amino sugar biosynthesis and degradation: the NagC repressor acts as both an activator and a repressor for the transcription of the glmUS operon and requires two separated NagC binding sites. EMBO J 14: 3958-3965.
16. 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 U S A 95: 12462-12467.
17. Lease RA, Cusick ME, Belfort M (1998) Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci U S A 95: 12456-12461.
18. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
19. Vogel J, Börner T (2002) Lariat formation and a hydrolytic pathway in plant chloroplast group II intron splicing. EMBO J 21: 3794-3803.
20. Vogel J, Hess WR (2001) Complete 5′ and 3′ end maturation of group II intron-containing tRNA precursors. RNA 7: 285-292.
21. Yanofsky C (2007) RNA-based regulation of genes of tryptophan synthesis and degradation, in bacteria. RNA 13: 1141-1154.
22. Nudler E, Mironov AS (2004) The riboswitch control of bacterial metabolism. Trends Biochem Sci 29: 11-17.
23. Winkler WC, Breaker RR (2005) Regulation of bacterial gene expression by riboswitches. Annu Rev Microbiol 59: 487-517.
24. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR (2003) Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113: 577-586.
25. Majdalani N, Vanderpool CK, Gottesman S (2005) Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40: 93-113.
26. Storz G, Altuvia S, Wassarman KM (2005) An abundance of RNA regulators. Annu Rev Biochem 74: 199-217.
27. Deana A, Belasco JG (2005) Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev 19: 2526-2533.
28. Iost I, Dreyfus M (1995) The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J 14: 3252-3261.
29. Zhang A, Wassarman KM, Rosenow C, Tjaden BC, Storz G, et al. (2003) Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50: 1111-1124.
30. Prevost K, Salvail H, Desnoyers G, Jacques JF, Phaneuf E, et al. (2007) The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol Microbiol 64: 1260-1273.
31. Hammer BK, Bassler BL (2007) Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 104: 11145-11149.
32. Jasiecki J, Wegrzyn G (2003) Growth-rate dependent RNA polyadenylation in Escherichia coli. EMBO Rep 4: 172-177.
33. Mohanty BK, Kushner SR (2006) The majority of Escherichia coli mRNAs undergo post-transcriptional modification in exponentially growing cells. Nucleic Acids Res 34: 5695-5704.
34. Xu F, Lin-Chao S, Cohen SN (1993) The Escherichia coli pcnB gene promotes adenylylation of antisense RNAI of ColE1-type plasmids in vivo and degradation of RNAI decay intermediates. Proc Natl Acad Sci U S A 90: 6756-6760.
35. Söderbom F, Binnie U, Masters M, Wagner EG (1997) Regulation of plasmid R1 replication: PcnB and RNase E expedite the decay of the antisense RNA, CopA. Mol Microbiol 26: 493-504.
36. Viegas SC, Pfeiffer V, Sittka A, Silva IJ, Vogel J, et al. (2007) Characterization of the role of ribonucleases in Salmonella small RNA decay. Nucleic Acids Res 35: 7651-7664.
37. Weilbacher T, Suzuki K, Dubey AK, Wang X, Gudapaty S, et al. (2003) A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 48: 657-670.
38. Liu MY, Gui G, Wei B, Preston JF 3rd, Oakford L, et al. (1997) The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem 272: 17502-17510.
39. Axmann IM, Kensche P, Vogel J, Kohl S, Herzel H, et al. (2005) Identification of cyanobacterial non-coding RNAs by comparative genome analysis. Genome Biol 6: R73.
40. Kay E, Dubuis C, Haas D (2005) Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci U S A 102: 17136-17141.
41. Guillier M, Gottesman S (2006) Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 59: 231-247.
42. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, et al. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69-82.
43. Tu KC, Bassler BL (2007) Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev 21: 221-233.
44. Bougdour A, Wickner S, Gottesman S (2006) Modulating RssB activity: IraP, a novel regulator of sigma(S) stability in Escherichia coli. Genes Dev 20: 884-897.
45. Turgay K, Hamoen LW, Venema G, Dubnau D (1997) Biochemical characterization of a molecular switch involving the heat shock protein ClpC, which controls the activity of ComK, the competence transcription factor of Bacillus subtilis. Genes Dev 11: 119-128.
46. Ogura M, Liu L, Lacelle M, Nakano MM, Zuber P (1999) Mutational analysis of ComS: evidence for the interaction of ComS and MecA in the regulation of competence development in Bacillus subtilis. Mol Microbiol 32: 799-812.
47. O'Hara EB, Chekanova JA, Ingle CA, Kushner ZR, Peters E, et al. (1995) Polyadenylylation helps regulate mRNA decay in Escherichia coli. Proc Natl Acad Sci U S A 92: 1807-1811.
48. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
49. 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.
50. Vogel J, Argaman L, Wagner EG, Altuvia S (2004) The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 14: 2271-2276.
51. Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton JC, et al. (2006) sigma(E)-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62: 1674-1688.
52. Urban JH, Vogel J (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 35: 1018-1037.
53. Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16: 10881-10890.
54. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
55. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10: 1507-1517.
56. Sittka A, Pfeiffer V, Tedin K, Vogel J (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 63: 193-217.