CsrB sRNA family: sequestration of RNA-binding regulatory proteins

Current Opinion in Microbiology

Volumn 10, Issue 2, 2007, Pages 156-163

  Babitzke, Paul ^a   Romeo, Tony ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON STORAGE REGULATOR B PROTEIN; REGULATOR PROTEIN; RNA; RNA BINDING PROTEIN; SMALL RNA; UNCLASSIFIED DRUG;

BINDING SITE; BIOFILM; CELL MOTILITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; NONHUMAN; PROTEIN FUNCTION; QUORUM SENSING; REGULATORY MECHANISM; REGULATORY RNA SEQUENCE; REVIEW; RIBOSOME; RNA BINDING; RNA STABILITY; SEQUENCE HOMOLOGY;

BACTERIA; BACTERIAL PROTEINS; BASE SEQUENCE; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; QUORUM SENSING; REPRESSOR PROTEINS; RNA, BACTERIAL; RNA, UNTRANSLATED; RNA-BINDING PROTEINS;

BACTERIA (MICROORGANISMS);

EID: 34247169597     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2007.03.007     Document Type: Review

References (50)

1. Storz G., Altuvia S., and Wassarman K.M. An abundance of RNA regulators. Annu Rev Biochem 74 (2005) 199-217
2. Liu M.Y., Gui G., Wei B., Preston III J.F., Oakford L., Yuksel U., Giedroc D.P., and Romeo T. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem 272 (1997) 17502-17510
3. Baker C.S., Morozov I., Suzuki K., Romeo T., and Babitzke P. CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 44 (2002) 1599-1610
4. Romeo T. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29 (1998) 1321-1330
5. Blumer C., Heeb S., Pessi G., and Haas D. Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc Natl Acad Sci USA 96 (1999) 14073-14078
6. Ecc. Mol Plant Microbe Interact 14 (2001) 516-526
7. Toledo-Arana A., Repoila F., and Cossart P. Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol 10 (2007) 182-188
8. Bejerano-Sagie M., and Xavier K.B. The role of small RNAs in quorum sensing. Curr Opin Microbiol 10 (2007) 189-198
9. Romeo T., Gong M., Liu M.Y., and Brun-Zinkernagel A.M. Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol 175 (1993) 4744-4755
10. Sabnis N.A., Yang H., and Romeo T. Pleiotropic regulation of central carbohydrate metabolism in Escherichia coli via the gene csrA. J Biol Chem 270 (1995) 29096-29104
11. Liu M.Y., Yang H., and Romeo T. The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. J Bacteriol 177 (1995) 2663-2672
12. Liu M.Y., and Romeo T. The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein. J Bacteriol 179 (1997) 4639-4642
13. Chatterjee A., Cui Y., Liu Y., Dumenyo C.K., and Chatterjee A.K. Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-l-homoserine lactone. Appl Environ Microbiol 61 (1995) 1959-1967
14. Cui Y., Chatterjee A., Liu Y., Dumenyo C.K., and Chatterjee A.K. 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 177 (1995) 5108-5115
15. Mukherjee A., Cui Y., Liu Y., Dumenyo C.K., and Chatterjee A.K. Global regulation in Erwinia species by Erwinia carotovora rsmA, a homologue of Escherichia coli csrA: repression of secondary metabolites, pathogenicity and hypersensitive reaction. Microbiol 142 (1996) 427-434
16. Reimmann C., Valverde C., Kay E., and Haas D. Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHA0. J Bacteriol 187 (2005) 276-285. The authors of this paper demonstrated that two RsmA proteins exist in P. fluorescens. This was the first demonstration of CsrA or RsmA paralogs in the same species.
17. Weilbacher T., Suzuki K., Dubey A.K., Wang X., Gudapaty S., Morozov I., Baker C.S., Georgellis D., Babitzke P., and Romeo T. A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 48 (2003) 657-670
18. Liu Y., Cui Y., Mukherjee A., and Chatterjee A.K. Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Mol Microbiol 29 (1998) 219-234
19. Heeb S., Blumer C., and Haas D. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J Bacteriol 184 (2002) 1046-1056
20. Valverde C., Heeb S., Keel C., and Haas D. RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0. Mol Microbiol 50 (2003) 1361-1379
21. Kay E., Dubuis C., and Haas D. Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci USA 102 (2005) 17136-17141
22. Suzuki K., Wang X., Weilbacher T., Pernestig A., Melefors O., Georgellis D., Babitzke P., and Romeo T. Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 184 (2002) 5130-5140
23. Wei B.L., Brun-Zinkernagel A.M., Simecka J.W., Pruss B.M., Babitzke P., and Romeo T. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40 (2001) 245-256
24. Dubey A.K., Baker C.S., Romeo T., and Babitzke P. RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 11 (2005) 1579-1587. This study identified the characteristics of high-affinity CsrA binding sites using SELEX, and confirmed the importance of GGA motif-containing RNA hairpins for CsrA binding.
25. Gutierrez P., Li Y., Osborne M.J., Pomerantseva E., Liu Q., and Gehring K. Solution structure of the carbon storage regulator protein CsrA from Escherichia coli. J Bacteriol 187 (2005) 3496-3501. The nuclear magnetic resonance (NMR) structure of CsrA, along with the crystal structure of the Pseudomonas putida protein, provided the first structural information for this protein and confirmed that CsrA functions as a dimer.
26. Mercante J., Suzuki K., Cheng X., Babitzke P., and Romeo T. Comprehensive alanine-scanning mutagenesis of Escherichia coli CsrA defines two subdomains of critical functional importance. J Biol Chem 281 (2006) 31832-31842. This study identified two symmetrical surfaces on CsrA that probably function as RNA binding domains.
27. Dubey A.K., Baker C.S., Suzuki K., Jones A.D., Pandit P., Romeo T., and Babitzke P. CsrA regulates translation of the Escherichia coli starvation gene, cstA, by blocking ribosome access to the cstA transcript. J Bacteriol 185 (2003) 4450-4460
28. Wang X., Dubey A.K., Suzuki K., Baker C.S., Babitzke P., and Romeo T. CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol 56 (2005) 1648-1663
29. Wei B., Shin S., LaPorte D., Wolfe A.J., and Romeo T. Global regulatory mutations in csrA and rpoS cause severe central carbon stress in Escherichia coli in the presence of acetate. J Bacteriol 182 (2000) 1632-1640
30. Gudapaty S., Suzuki K., Wang X., Babitzke P., and Romeo T. Regulatory interactions of Csr components: The RNA binding protein CsrA activates csrB transcription in Escherichia coli. J Bacteriol 183 (2001) 6017-6027
31. Mondragon V., Franco B., Jonas K., Suzuki K., Romeo T., Melefors O., and Georgellis D. pH dependent activation of the BarA-UvrY two-component system in Escherichia coli. J Bacteriol 188 (2006) 8303-8306
32. Suzuki K., Babitzke P., Kushner S.R., and Romeo T. Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20 (2006) 2605-2617. This study identified a protein that targets CsrB and CsrC for degradation by the endoribonuclease RNase E. This was the first report of a GGDEF-EAL domain protein that does not participate in cyclic di-GMP metabolism.
33. Valverde C., Lindell M., Wagner E.G.H., and Haas D. A repeated GGA motif is critical for the activity and stability of the riboregulator RsmY of Pseudomonas fluorescens. J Biol Chem 279 (2004) 25066-25074
34. Heeb S., Valverde C., Gigot-Bonnefoy C., and Haas D. Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. FEMS Microbiol Lett 243 (2005) 251-258. This study provided evidence that RsmA regulates expression of rpoS, a gene encoding a stationary phase and stress response sigma factor. Although it is not known whether this regulation is direct or indirect, this finding suggests that the Rsm regulon is considerably larger than was previously thought.
35. Kõiv V., and Mäe A. Quorum sensing controls the synthesis of virulence factors by modulating rsmA gene expression in Erwinia carotovora subsp. carotovora. Mol Genet Genomics 265 (2001) 287-292
36. Chatterjee A., Cui Y., and Chatterjee A.K. RsmA and the Quorum-sensing signal, N-[3-oxohexanoyl]-l-homoserine lactone, control the levels of rsmB RNA in Erwinia carotovora subsp. carotovora by affecting its stability. J Bacteriol 184 (2002) 4089-4095
37. Hyytiäinen H., Montesano M., and Palvo E.T. Global regulators ExpA (GacA) and KgdR modulate extracellular enzyme gene expression through the RsmA-rsmB system in Erwinia carotovora subsp. carotovora. Mol Plant Microbe Interact 14 (2001) 931-938
38. Ecc production and virulence by modulating levels of regulatory RNA (rsmB) and RNA-binding protein (RsmA). J Bacteriol 181 (1999) 6042-6052
39. Liu Y., Jiang G., Cui Y., Mukherjee A., Ma W.L., and Chatterjee A.K. kdgREcc negatively regulates genes for pectinases, cellulase, protease, HarpinEcc, and a global regulator in Erwinia carotovora subsp. carotovora. J Bacteriol 181 (1999) 2411-2422
40. Asita M., Cui Y., Ma W., Liu Y., and Chatterjee A.K. hexA of Erwinia carotovora ssp. carotovora strain Ecc71 negatively regulates production of RpoS and rsmB RNA, a global regulator of extracellular proteins, plant virulence and the quorum-sensing signal, N-(3-oxohexanoyl)-l-homoserine lactone. Environ Microbiol 2 (2000) 203-215
41. Mukherjee A., Cui Y., Ma W., Liu Y., Ishihama A., Eisenstark A., and Chatterjee A.K. RpoS (Sigma-S) controls expression of rsmA, a global regulator of secondary metabolites, Harpin, and extracellular proteins in Erwinia carotovora. J Bacteriol 180 (1998) 3629-3634
42. Cui Y., Chatterjee A., Hasegawa H., Dixit V., Leigh N., and Chatterjee A.K. ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein. J Bacteriol 187 (2005) 4792-4803
43. Cui Y., Chatterjee A., Hasegawa H., and Chatterjee A.K. Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with N-acylhomoserine lactone signals. J Bacteriol 188 (2005) 4715-4726. This study provided the first compelling evidence for a regulator that directly controls the expression of rsmA. Moreover, this work substantiated the link between Rsm control and quorum sensing in Erwinia.
44. Rife C., Schwarzenbacher R., McMullan D., Abdubek P., Ambing E., Axelrod H., Biorac T., Canaves J.M., Chiu H.J., Deacon A.M., et al. Crystal structure of the global regulatory protein CsrA from Pseudomonas putida at 2.05 A resolution reveals a new fold. Proteins 61 (2005) 449-453. The crystal structure of CsrA, along with the NMR structure of the E. coli protein, provided the first structural information for this protein and confirmed that CsrA functions as a dimer.
45. Heeb S., Kuehne S.A., Bycroft M., Crivii S., Allen M.D., Haas D., Camara M., and Williams P. Functional analysis of the post-transcriptional regulator RsmA reveals a novel RNA-binding site. J. Mol Biol 355 (2006) 1026-1036
46. Kulkarni P.R., Cui X., Williams J.W., Stevens A.M., and Kulkarni R.V. Prediction of CsrA-regulating small RNAs in bacteria and their experimental verification in Vibrio fischeri. Nucleic Acids Res 34 (2006) 3361-3369. The authors of this publication describe a bioinformatic approach for identifying genes encoding sRNA antagonists of CsrA (RsmA). Prior to this approach, identification of the sRNA genes was considerably more difficult.
47. Kay E., Humair B., Denervaud V., Riedel K., Spahr S., Eberl L., Valverde C.V., and Haas D. Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 188 (2006) 6026-6033
48. Teplitski M., Al-Agely A., and Ahmer B.M.M. Contribution of the SirA regulon to biofilm formation in Salmonella enterica serovar Typhimurium. Microbiol 152 (2006) 3411-3424
49. Fortune D.R., Suyemoto M., and Altier C. Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect Immun 74 (2006) 331-339
50. Lenz D.H., Miller M.B., Zhu J., Kulkarni R.V., and Bassler B.L. CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol Microbiol 58 (2005) 1186-1202