Regulatory roles for small RNAs in bacteria

Current Opinion in Microbiology

Volumn 6, Issue 2, 2003, Pages 120-124

  Massé, Eric ^a   Majdalani, Nadim ^a   Gottesman, Susan ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; COMPLEMENTARY RNA; DNA; MESSENGER RNA; PROTEIN; RNA; RNA BINDING PROTEIN; RNA DIRECTED RNA POLYMERASE;

BINDING SITE; ESCHERICHIA COLI; GENE EXPRESSION; NONHUMAN; OPEN READING FRAME; OPERON; REVIEW; RNA STABILITY; RNA TRANSCRIPTION; RNA TRANSLATION; TRANSCRIPTION TERMINATION; UNTRANSLATED REGION;

ESCHERICHIA COLI;

EID: 0038352109     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(03)00027-4     Document Type: Review

References (56)

1. Brantl S: Antisense-RNA regulation and RNA interference. Biochim Biophys Acta 2002, 1575:15-25.
2. Zeiler BN, Simons RW: Control by Antisense RNA. In Regulation of Gene Expression in Escherichia coli. Edited by Lin ECC, Lynch AS. R.G. Landes Company; 1996:67-83.
3. Gerdes K, Gultyaev AP, Franch T, Pedersen K, Mikkelsen ND: Antisense RNA-regulated programmed cell death. Annu Rev Genet 1997, 31:1-31.
4. Wassarman KM, Zhang A, Storz G: Small RNAs in Escherichia coli. Trends Microbiol 1999, 7:37-45.
5. Gottesman S: Stealth regulation: biological circuits with small RNA switches. Genes Dev 2002, 16:2829-2842.
6. Wassarman KM: Small RNAs in bacteria: diverse regulators of gene expression in response to environmental changes. Cell 2002, 109:141-144.
7. Storz G: An expanding universe of noncoding RNAs. Science 2002, 296:1260-1263.
8. 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. Using conservation determined by BLAST comparisons of intergenic regions of Escherichia coli to Salmonella and Klebsiella, as well as microarray expression data, candidates for new small RNAs were selected. From 60 regions tested by northern blot, 17 new small RNAs and six novel small open reading frames were identified. Many of these bind the RNA chaperone Hfq.
9. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EGH, Margalit H, Altuvia S: Novel small RNA-encoding genes in the intergenic region of Escherichia coli. Curr Biol 2001, 11:941-950. Orphan promoters and Rho-independent terminators within intergenic regions of E. coli were identified; conservation was used as a second criterion to find new small RNAs. Fourteen out of 23 tested candidates were found to encode small RNAs and were found to be expressed under specific growth conditions.
10. Rivas E, Klein RJ, Jones TA, Eddy SR: Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol 2001, 11:1369-1373. A generally applicable computational method for identifying secondary structure elements (co-variance in related organisms of secondary structure elements such as stems) was developed and applied to the intergenic regions of the E. coli chromosome. Of 275 predicted structures, 11 out of 49 predicted candidates tested by northern blot were found to express small RNA species.
11. Chen S, Lesnik EA, Hall TA, Sampath R, Griffey RH, Ecker DJ, Blyn LB: A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome. Biosystems 2002, 65:157-177. Sigma 70 promoters and nearby Rho-independent terminators within intergenic regions suggest 227 possible candidates for small RNAs; these include known small RNAs and some tRNAs, as well as new short ORFs. Of the remaining candidates, northern blots confirmed the presence of small RNAs in seven of the eight tested. This is the only E. coli genomic search that does not require conservation as one criterion.
12. 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. The small RNA RyhB has at least six target mRNAs that all encode iron-containing proteins or iron metabolism proteins. High expression of RyhB in low-iron medium rapidly down-regulates these specific mRNAs. This allows the cell to react extremely fast to new environmental conditions and re-orient use of an essential nutrient (iron) to more critical components. This might prove to be an important pathway in the regulation of virulence in pathogenic organisms, in which iron acquisition and use in vivo is critical.
13. Hantke K: Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K12: fur not only affects iron metabolism. Mol Gen Genet 1987, 210:135-139.
14. Hantke K: Iron and metal regulation in bacteria. Curr Opin Microbiol 2001, 4:172-177.
15. Escolar L, Pérez-Martin J, de Lorenzo V: Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 1999, 181:6223-6229.
16. Sahagan B, Dahlberg JE: A small, unstable RNA molecule of Escherichia coli: Spot 42 RNA. J Mol Biol 1979, 131:593-605.
17. Polayes DA, Rice PW, Garner MM, Dahlberg JE: Cyclic AMP-cyclic AMP receptor protein as a repressor of transcription of the spf gene of Escherichia coli. J Bacteriol 1988, 170:3110-3114.
18. Møller T, Franch T, Udesen C, Gerdes K, Valentin-Hansen P: Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 2002, 16:1696-1706. This important paper has resolved the long mysterious role of Spot 42 RNA. It is responsible for the discoordinate regulation of the galactose operon. The regulatory RNA is expressed in conditions of low cAMP when glucose is present and galactose is not utilized. Spot 42 is able to repress the translation of a specific gene in the operon by RNA-RNA interactions close to the ribosome-binding site of galK.
19. Brown L, Elliott T: Mutations that increase expression of the rpoS gene and decrease its dependence on hfq function in Salmonella typhimurium. J Bacteriol 1997, 179:656-662.
20. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S: DsrA RNA regulates translation of RpoS message by an antiantisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci USA 1998, 95:12462-12467.
21. Majdalani N, Hernandez D, Gottesman S: Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 2002, 46:813-826. RprA RNA stimulates RpoS translation by pairing to the same region of the RpoS leader as DsrA. However, RprA synthesis is regulated by the capsule phospho-relay system, whereas DsrA synthesis is regulated by temperature. The existence of two different small RNA regulators allows multiple environmental signals to be transduced to regulate RpoS translation.
22. Zhang A, Altuvia S, Tiwari A, Argaman L, Hengge-Aronis R, Storz G: The oxyS regulatory RNA represses rpoS translation by binding Hfq (HF-1) protein. EMBO J 1998, 17:6061-6068.
23. Sledjeski D, Gottesman S: A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc Natl Acad Sci USA 1995, 92:2003-2007.
24. Repoila F, Gottesman S: Signal transduction cascade for regulation of RpoS: temperature regulation of DsrA. J Bacteriol 2001, 183:4012-4023. RpoS translation at low temperature is dependent upon the small RNA DsrA. Temperature regulation was found to reside in both the stability and synthesis of DsrA. A minimal DsrA promoter of 36 bp is sufficient to confer temperature regulation on a reporter.
25. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G: A small stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 1997, 90:43-53.
26. Lease RA, Cusick M, Belfort M: Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci USA 1998, 95:12456-12461.
27. Altuvia S, Zhang A, Argaman L, Tiwari A, Storz G: The Escherichia coli oxyS regulatory RNA represses fhlA translation by blocking ribosome binding. EMBO J 1998, 17:6069-6075.
28. 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.
29. Sledjeski DD, Whitman C, Zhang A: Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 2001, 183:1997-2005.
30. Majdalani N, Chen S, Murrow J, St. John K, Gottesman S: Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol 2001, 39:1382-1394.
31. Møller T, Franch T, Hojrup P, Keene DR, Bachinger HP, Brennan R, Valentin-Hansen P: Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 2002, 9:23-30. A sequence motif shared by the Hfq protein and the archeal and eukaryotic Sm proteins suggests that Hfq is a close relative. Hfq promotes RNA-RNA interactions between Spot 42 and its cognate mRNA.
32. Kajitani M, Kato A, Wada A, Inokuchi Y, Ishihama A: Regulation of the Escherichia coli hfq gene encoding the host factor for phage Q beta. J Bacteriol 1994, 176:531-534.
33. Sun X, Zhulin I, Wartell RM: Predicted structure and phyletic distribution of the RNA-binding protein Hfq. Nucleic Acids Res 2002, 30:3662-3671.
34. Zhang A, Wassarman KM, Ortega J, Steven AC, Storz G: The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 2002, 9:11-22. Hfq increases the RNA-RNA interactions between the regulatory RNA OxyS and the target mRNAs rpoS and fhlA. The preferential binding of Hfq to polyA- or polyU-RNA, with no consensus, is also demonstrated. The authors also note the homology between eukaryotic Sm proteins and Hfq.
35. Tsui HCT, Leung HCE, Winkler ME: Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol 1994, 13:35-49.
36. Schumacher MA, Pearson RF, Møller T, Valentin-Hansen P, Brennan RG: Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J 2002, 21:3546-3556. The crystal structure of Hfq from S. aureus with and without a short RNA was determined. As predicted from electron microscopy studies and sequence homology, Hfq forms a hexameric ring very similar to that seen for Sm proteins. RNA binds around the inside of the ring.
37. Will CL, Luhrmann R: Spliceosomal UsnRNP biogenesis, structure and function. Curr Opin Cell Biol 2001, 13:290-301.
38. Hajndsorf E, Regnier P: Host factor Hfq of Escherichia coli stimulates elongation of poly(A) tails by poly(A) polymerase I. Proc Natl Acad Sci USA 2000, 97:1501-1505.
39. Vytvytska O, Moll I, Kaberdin VR, von Gabain A, Blasi U: Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev 2000, 14:1109-1118.
40. Vytvytska O, Jakobsen J, Balcunaite G, Andersen J, 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.
41. Tsui HCT, Feng G, Winkler M: Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12. J Bacteriol 1997, 179:7476-7487.
42. Wassarman KM, Storz G: 6S RNA regulates E. coli RNA polymerase activity. Cell 2000, 101:613-623.
43. Romeo T: Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 1998, 29:1321-1330.
44. Wei BL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, Romeo T: Positive regulation of motility and fihDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 2001, 40:245-256.
45. Jackson DW, Suzuki K, Oakford L, Simecka JW, Hart ME, Romeo T: Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 2002, 184:290-301.
46. Wei B, Shin S, LaPorte D, Wolfe AJ, Romeo T: Global regulatory mutations in csrA and rpoS cause severe central carbon stress in Escherichia coil in the presence of acetate. J Bacteriol 2000, 182:1632-1640.
47. Baker CS, Morozov I, Suzuki K, Romeo T, Babitzke P: CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 2002, 44:1599-1610. CsrA protein binds to the mRNA glgCAP, involved in carbohydrate metabolism, blocking ribosome binding and thus translation in vivo and in vitro. This binding requires a region near the Shine-Dalgarno sequence and a second sequence further upstream.
48. Gudapaty S, Suzuki K, Wang X, Babitzke P, Romeo T: Regulatory interactions of Csr components: the RNA binding protein CsrA activates csrB transcription in Escherichia coli. J Bacteriol 2001, 183:6017-6027.
49. Suzuki K, Wang X, Weilbacher T, Pernestig AK, Melefors O, Georgellis D, Babitzke P, Romeo T: Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 2002, 184:5130-5140.
50. Weilbacher T, Suzuki K, Dubey AK, Wang X, Gudapaty S, Morozov I, Baker CS, Georgellis D, Babitzke P, Romeo T: A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol. Microbiol. 2003, in press.
51. Altier C, Suyemoto M, Lawhon SD: Regulation of Salmonella enterica serovar typhimurium invasion genes by csrA. Infect Immun 2000, 68:6790-6797.
52. Ma W, Cui Y, Liu Y, Dumenyo CK, Mukherjee A, Chatterjee AK: Molecular characterization of global regulatory RNA species that control pathogenicity factors in Erwinia amylovora and Erwinia herbicola pv gypsophilae. J Bacteriol 2000, 183:1870-1880.
53. Cui Y, Chatterjee A, Liu Y, Dumenyo CK, Chatteriee AK: Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp, carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. J Bacteriol 1995, 177:5108-5115.
54. Withey JH, Friedman DI: The biological roles of trans-translation. Curr Opin Microbiol 2002, 5:154-159.
55. Abo T, Inada T, Ogawa K, Aiba H: SsrA-mediated tagging and proteolysis of Lacl and its role in the regulation of lac operon. EMBO J 2000, 19:3762-3769.
56. Xu F, Gaggero C, Cohen S: Polyadenylation can regulate ColE1 type plasmid copy number independently of any effect on RNA decay by decreasing the interaction of antisense RNAI with its RNAII target. Plasmid 2002, 48:49-58.