New insights into small RNA-dependent translational regulation in prokaryotes

Trends in Genetics

Volumn 29, Issue 2, 2013, Pages 92-98

  Desnoyers, Guillaume ^a,b   Bouchard, Marie Pier ^a,b   Massé, Eric ^a,b  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b ATLANTIC CANCER RESEARCH INSTITUTE   (Canada)

Author keywords

Bacterial small RNAs; Enterobacteria; MRNA decay; Ribosome binding site; Translation repression

Indexed keywords

FERRIC UPTAKE REGULATOR; MESSENGER RNA; RIBONUCLEASE E; TRANSFER RNA;

BASE PAIRING; ESCHERICHIA COLI; GENE CONTROL; GENE REPRESSION; GENETIC CODE; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN RNA BINDING; REVIEW; RIBOSOME; RNA BINDING; RNA SEQUENCE; RNA STRUCTURE; RNA TRANSLATION; SALMONELLA; TRANSLATION REGULATION;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, GENETIC; PROKARYOTIC CELLS; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA STABILITY; RNA, BACTERIAL; RNA, MESSENGER; RNA, SMALL UNTRANSLATED;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; PROKARYOTA;

EID: 84872855335     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2012.10.004     Document Type: Review

References (82)

1. Mizuno T., et al. A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc. Natl. Acad. Sci. U.S.A. 1984, 81:1966-1970.
2. Waters L.S., Storz G. Regulatory RNAs in bacteria. Cell 2009, 136:615-628.
3. Prevost K., et al. The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol. Microbiol. 2007, 64:1260-1273.
4. Urban J.H., Vogel J. Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol. 2008, 6:e64.
5. Majdalani N., et al. 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. 1998, 95:12462-12467.
6. Lease R.A., Belfort M. A trans-acting RNA as a control switch in Escherichia coli: DsrA modulates function by forming alternative structures. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:9919-9924.
7. Beisel C.L., Storz G. The base-pairing RNA spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli. Mol. Cell 2011, 41:286-297.
8. Masse E., et al. Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol. 2005, 187:6962-6971.
9. Papenfort K., et al. Evidence for an autonomous 5' target recognition domain in an Hfq-associated small RNA. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20435-20440.
10. Sharma C.M., et al. Pervasive post-transcriptional control of genes involved in amino acid metabolism by the Hfq-dependent GcvB small RNA. Mol. Microbiol. 2011, 81:1144-1165.
11. Filipowicz W., et al. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat. Rev. Genet. 2008, 9:102-114.
12. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
13. Fabian M.R., Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat. Struct. Mol. Biol. 2012, 19:586-593.
14. Kozak M. Initiation of translation in prokaryotes and eukaryotes. Gene 1999, 234:187-208.
15. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc. Natl. Acad. Sci. U.S.A. 1974, 71:1342-1346.
16. de Smit M.H., van Duin J. Secondary structure of the ribosome binding site determines translational efficiency: a quantitative analysis. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:7668-7672.
17. Johansson J., et al. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 2002, 110:551-561.
18. Winkler W., et al. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 2002, 419:952-956.
19. Mironov A.S., et al. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 2002, 111:747-756.
20. Bouvier M., et al. Small RNA binding to 5' mRNA coding region inhibits translational initiation. Mol. Cell 2008, 32:827-837.
21. Beyer D., et al. How the ribosome moves along the mRNA during protein synthesis. J. Biol. Chem. 1994, 269:30713-30717.
22. Huttenhofer A., Noller H.F. Footprinting mRNA-ribosome complexes with chemical probes. EMBO J. 1994, 13:3892-3901.
23. Masse E., et al. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 2003, 17:2374-2383.
24. Prevost K., et al. Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage. Genes Dev. 2011, 25:385-396.
25. Morita T., et al. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev. 2005, 19:2176-2186.
26. Ikeda Y., et al. Hfq binding at RhlB-recognition region of RNase E is crucial for the rapid degradation of target mRNAs mediated by sRNAs in Escherichia coli. Mol. Microbiol. 2011, 79:419-432.
27. Bazzini A.A., et al. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 2012, 336:233-237.
28. Sledjeski D.D., et al. Hfq is necessary for regulation by the untranslated RNA DsrA. J. Bacteriol. 2001, 183:1997-2005.
29. Moller T., et al. Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol. Cell 2002, 9:23-30.
30. Zhang A., et al. The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol. Cell 2002, 9:11-22.
31. Kawamoto H., et al. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol. Microbiol. 2006, 61:1013-1022.
32. Carpousis A.J. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 2007, 61:71-87.
33. Morita T., et al. Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4858-4863.
34. Papenfort K., et al. SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol. Microbiol. 2006, 62:1674-1688.
35. Guillier M., Gottesman S. Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol. Microbiol. 2006, 59:231-247.
36. Darfeuille F., et al. An antisense RNA inhibits translation by competing with standby ribosomes. Mol. Cell 2007, 26:381-392.
37. Unoson C., Wagner E.G. Dealing with stable structures at ribosome binding sites: bacterial translation and ribosome standby. RNA Biol. 2007, 4:113-117.
38. de Smit M.H., van Duin J. Translational standby sites: how ribosomes may deal with the rapid folding kinetics of mRNA. J. Mol. Biol. 2003, 331:737-743.
39. Studer S.M., Joseph S. Unfolding of mRNA secondary structure by the bacterial translation initiation complex. Mol. Cell 2006, 22:105-115.
40. Oppenheim D.S., Yanofsky C. Translational coupling during expression of the tryptophan operon of Escherichia coli. Genetics 1980, 95:785-795.
41. Schumperli D., et al. Translational coupling at an intercistronic boundary of the Escherichia coli galactose operon. Cell 1982, 30:865-871.
42. Vecerek B., et al. Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding. EMBO J. 2007, 26:965-975.
43. Sonnleitner E., et al. The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol. Microbiol. 2011, 80:868-885.
44. Urbanowski M.L., et al. The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol. Microbiol. 2000, 37:856-868.
45. Martin-Farmer J., Janssen G.R. A downstream CA repeat sequence increases translation from leadered and unleadered mRNA in Escherichia coli. Mol. Microbiol. 1999, 31:1025-1038.
46. Sharma C.M., et al. A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev. 2007, 21:2804-2817.
47. Holmqvist E., et al. Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J. 2010, 29:1840-1850.
48. Desnoyers G., Masse E. Noncanonical repression of translation initiation through small RNA recruitment of the RNA chaperone Hfq. Genes Dev. 2012, 26:726-739.
49. Moller T., et al. Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev. 2002, 16:1696-1706.
50. Komarova A.V., et al. AU-rich sequences within 5' untranslated leaders enhance translation and stabilize mRNA in Escherichia coli. J. Bacteriol. 2005, 187:1344-1349.
51. Komarova A.V., et al. Protein S1 counteracts the inhibitory effect of the extended Shine-Dalgarno sequence on translation. RNA 2002, 8:1137-1147.
52. Salvail H., et al. A small RNA promotes siderophore production through transcriptional and metabolic remodeling. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15223-15228.
53. Masse E., Gottesman S. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:4620-4625.
54. Johansen J., et al. Conserved small non-coding RNAs that belong to the sigmaE regulon: role in down-regulation of outer membrane proteins. J. Mol. Biol. 2006, 364:1-8.
55. Dreyfus M. Killer and protective ribosomes. Prog. Mol. Biol. Transl. Sci. 2009, 85:423-466.
56. Pfeiffer V., et al. Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat. Struct. Mol. Biol. 2009, 16:840-846.
57. Bandyra K.J., et al. The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol. Cell 2012, 47:943-953.
58. Mackie G.A. Ribonuclease E is a 5'-end-dependent endonuclease. Nature 1998, 395:720-723.
59. Deana A., et al. The bacterial enzyme RppH triggers messenger RNA degradation by 5' pyrophosphate removal. Nature 2008, 451:355-358.
60. Corcoran C.P., et al. Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA. Mol. Microbiol. 2012, 84:428-445.
61. Frohlich K.S., et al. A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD. Nucleic Acids Res. 2012, 40:3623-3640.
62. Beisel C.L., et al. Multiple factors dictate target selection by Hfq-binding small RNAs. EMBO J. 2012, 31:1961-1974.
63. Franze de Fernandez M.T., et al. Factor fraction required for the synthesis of bacteriophage Qbeta-RNA. Nature 1968, 219:588-590.
64. Schumacher M.A., et al. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J. 2002, 21:3546-3556.
65. Wilusz C.J., Wilusz J. Eukaryotic Lsm proteins: lessons from bacteria. Nat. Struct. Mol. Biol. 2005, 12:1031-1036.
66. Vogel J., Luisi B.F. Hfq and its constellation of RNA. Nat. Rev. Microbiol. 2011, 9:578-589.
67. Geissmann T.A., Touati D. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J. 2004, 23:396-405.
68. Folichon M., et al. The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation. Nucleic Acids Res. 2003, 31:7302-7310.
69. Hajnsdorf E., Regnier P. Host factor Hfq of Escherichia coli stimulates elongation of poly(A) tails by poly(A) polymerase I. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:1501-1505.
70. Mohanty B.K., et al. The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli. Mol. Microbiol. 2004, 54:905-920.
71. Rabhi M., et al. The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rho-dependent terminators. EMBO J. 2011, 30:2805-2816.
72. Ross J.A., et al. Tn10/IS10 transposition is downregulated at the level of transposase expression by the RNA-binding protein Hfq. Mol. Microbiol. 2010, 78:607-621.
73. Vecerek B., et al. Translational autocontrol of the Escherichia coli hfq RNA chaperone gene. RNA 2005, 11:976-984.
74. Yanofsky C., et al. The complete nucleotide sequence of the tryptophan operon of Escherichia coli. Nucleic Acids Res. 1981, 9:6647-6668.
75. Lynn S.P., et al. Attenuation regulation in the thr operon of Escherichia coli K-12: molecular cloning and transcription of the controlling region. J. Bacteriol. 1982, 152:363-371.
76. Naville M., Gautheret D. Transcription attenuation in bacteria: theme and variations. Brief. Funct. Genomics 2010, 9:178-189.
77. Draper D.E., Reynaldo L.P. RNA binding strategies of ribosomal proteins. Nucleic Acids Res. 1999, 27:381-388.
78. Subramanian A.R. Structure and functions of ribosomal protein S1. Prog. Nucleic Acid Res. Mol. Biol. 1983, 28:101-142.
79. Tzareva N.V., et al. Ribosome-messenger recognition in the absence of the Shine-Dalgarno interactions. FEBS Lett. 1994, 337:189-194.
80. Sengupta J., et al. Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:11991-11996.
81. Sorensen M.A., et al. Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J. Mol. Biol. 1998, 280:561-569.
82. Tedin K., et al. Requirements for ribosomal protein S1 for translation initiation of mRNAs with and without a 5' leader sequence. Mol. Microbiol. 1997, 25:189-199.