A novel sRNA component of the carbon storage regulatory system of Escherichia coli

Molecular Microbiology

Volumn 48, Issue 3, 2003, Pages 657-670

  Weilbacher, Thomas ^a   Suzuki, Kazushi ^b   Dubey, Ashok K ^c   Wang, Xin ^b   Gudapaty, Seshigirao ^a,e   Morozov, Igor ^c,f   Baker, Carol S ^c   Georgellis, Dimitris ^d   Babitzke, Paul ^c   Romeo, Tony ^b  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^e ANDHRA UNIVERSITY   (India)

^f UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; GLYCOGEN; PROTEIN CSRA; PROTEIN CSRB; PROTEIN CSRC; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BIOFILM; CARBON STORAGE; ENTEROBACTERIACEAE; ESCHERICHIA COLI; EVOLUTION; GENETIC TRANSCRIPTION; GLYCOGEN SYNTHESIS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; TRANSCRIPTION REGULATION;

BASE SEQUENCE; BIOFILMS; CARBON; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GLYCOGEN; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; RNA STABILITY; RNA, BACTERIAL; RNA-BINDING PROTEINS;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0037899184     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03459.x     Document Type: Article

References (51)

1. Altier, C., Suyemoto, M., and Lawhon, S. (2000) Regulation of Salmonella enterica serovar typhimurium invasion genes by csrA. Infect Immun 68: 6790-6797.
2. Altschul, S.F., Gish, W., Miller, W., Meyers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Altuvia, S., Zhang, A., Argaman, L., Tiwari, A., and Storz, G. (1998) The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding. EMBO J 17: 6069-6075.
4. Argaman, L., Hershberg, R., Vogel, J., Bejerano, G., Wagner, E.G., Margalit, H., and Altuvia, S. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 11: 941-950.
5. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1989) Current Protocols in Molecular Biology. New York: John Wiley & Sons.
6. Babitzke, P., Stults, J.T., Shire, S.J., and Yanofsky, C. (1994) TRAP, the trp RNA-binding attenuation protein of Bacillus subtilis, is a multisubunit complex that appears to recognize G/UAG repeats in the trpEDCFBA and trpG transcripts. J Biol Chem 269: 16597-16604.
7. Baker, C.S., Morozov, I., Suzuki, K., Romeo, T., and Babitzke, P. (2002) CsrA regulates glycogen biosynthesis by preventing translation of glgC. Escherichia coli. Mol Microbiol 44: 1599-1610.
8. Blattner, F.R., Plunkett, G., III, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
9. Boyd, D., Weiss, S.D., Chen, J.C., and Beckwith, J. (2000) Towards single copy gene expression systems making gene cloning physiologically relevant: lambda InCh, a simple Escherichia coli plasmid-chromosome shuttle system. J Bacteriol 182: 842-847.
10. Chamberlain, J.P. (1979) Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble flour, sodium salicylate. Anal Biochem 98: 132-135.
11. Chatterjee, A., Cui, Y.Y., Liu, Y., Dumenyo, C.K., and Chatterjee, A.K. (1995) Inactivation of rsmA leads to over-production of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl Environ Microbiol 61: 1959-1967.
12. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
13. Eraso, J.M., and Weinstock, G.M. (1992) Anaerobic control of colicin E1 production. J Bacteriol 174: 5101-5109.
14. Evans, D.G., Evans, D.J., Jr, and Tjoa, W. (1997) Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun 18: 330-337.
15. Gottesman, S. (1984) Bacterial regulation: global regulatory networks. Annu Rev Genet 18: 415-441.
16. Gudapaty, S., Suzuki, K., Wang, X., Babitzke, P., and Romeo, T. (2001) Regulatory interactions of Csr components: the RNA binding protein CsrA activates csrB transcription in Escherichia coli. J Bacteriol 183: 6017-6027.
17. Heeb, S., Blumer, C., and Haas, D. (2002) Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHAO. J Bacteriol 184: 1046-1056.
18. Hengge-Aronis, R. (1996) Regulation of gene expression during entry into stationary phase. In Escherichia coli and Salmonella: Cellular and Molecular Biology, Vol. 1, 2nd edn. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 1497-1512.
19. Huisman, G.W., Siegele, D.A., Zambrano, M.M., and Kolter, R. (1996) Morphological and physiological changes during the stationary phase. In Escherichia coli and Salmonella: Cellular and Molecular Biology, Vol. 1, 2nd edn. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 1672-1682.
20. Jackson, D.W., Suzuki, K., Oakford, L., Simecka, J.W., Hart, M.E., and Romeo, T. (2002) Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 184: 290-301.
21. Lease, R., and Belfort, M. (2000) A trans-acting RNA as a control switch in Escherichia coli. DsrA modulates function by forming alternative structures. Proc Natl Acad Sci USA 97: 9919-9924.
22. Liu, M., and Romeo, T. (1997) The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein. J Bacteriol 179: 4639-4642.
23. Liu, M., Yang, H., and Romeo, T. (1995) The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. J Bacteriol 177: 2663-2672.
24. Liu, M., Gui, G., Wei, B., Preston, J.F., Oakford, L., Yuksel, U., 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.
25. Majdalani, N., Cunning, C., Sledjeski, D., Elliot, T., and 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.
26. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
27. Neidhardt, F., and Savageau, M.A. (1996) Regulation beyond the operon. In Escherichia coli and Salmonella: Cellular and Molecular Biology, Vol. 1. 2nd edn. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.L., Magasanik, B., et al. (eds) Washington, DC: American Society for Microbiology Press, pp. 1310-1324.
28. Pernestig, A.-K., Melefors, Ö., and Georgellis, D. (2001) Identification of UvrY as the cognate response regulator for the BarA sensor kinase in Escherichia coli. J Biol Chem 276: 225-231.
29. Rivas, E., Klein, R.J., Jones, T.A., and Eddy, S.R. (2001) Computational identification of noncoding RNAs in E. coli by comparative genomics. Curr Biol 11: 1369-1373.
30. Romeo, T. (1998) Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29: 1321-1330.
31. Romeo, T., and Preiss, J. (1989) Genetic regulation of glycogen biosynthesis in Escherichia coli: in vitro effects of cyclic AMP and guanosine 5′-diphosphate 3′-diphosphate and analysis of in vivo transcripts. J Bacteriol 171: 2773-2782.
32. Romeo, T., Black, J., and Preiss, J. (1990) Genetic regulation of glycogen biosynthesis in Escherichia coli: in vivo effects of the catabolite repression and stringent response systems in glg gene expression. Curr Microbiol 21: 131-137.
33. Romeo, T., Moore, J., and Smith, J. (1991) A simple method for cloning genes involved in glucan biosynthesis: isolation of structural and regulatory genes for glycogen synthesis in Escherichia coli. Gene 108: 23-29.
34. Romeo, T., Gong, M., Liu, M.Y., and Brun-Zinkernagel, A.-M. (1993) 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: 4744-4755.
35. Sabnis, N.A., Yang, H., and Romeo, T. (1995) Pleiotropic regulation of central carbohydrate metabolism in Escherichia coli via the gene csrA. J Biol Chem 270: 29096-29104.
36. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
37. Sledjeski, D., Whitman, C., and Zhang, A. (2001) Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183: 1997-2005.
38. Smith, P.K., Krohn, R.H., Hermanson, G.T., Mallie, A.K., Gartner, F.H., Provensano, J.D., et al, (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85.
39. Stoker, N.G., Fairweather, N.F., and Spratt, B.G. (1982) Versatile low-copy-number plasmid vectors for cloning in Escherichia coli. Gene 18: 335-341.
40. Suzuki, K., Wang, X., Weilbacher, T., Pernestig, A.-K., Melefors, O., Georgellis, D., et al. (2002) Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 184: 5130-5140.
41. Tatarko, M., and Romeo, T. (2001) Disruption of a global regulatory gene to enhance central carbon flux into phenylalanine biosynthesis in Escherichia coli. Curr Microbiol 43: 26-32.
42. Wassarman, K.M. (2002) SmallRNAs in bacteria: diverse regulators of gene expression in response to environmental change. Cell 109: 141-144.
43. Wassarman, K.M., and Storz, G. (2000) 6S RNA regulates E. coli RNA polymerase activity. Cell 101: 613-623.
44. Wassarman, K.M., Zhang, A., and Storz, G. (1999) Small RNAs in Escherichia coli. Trends Microbiol 7: 37-44.
45. Wassarman, K.M., Repoila, F., Rosenow, C., Storz, G., and Gottesman, S. (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 15: 1637-1651.
46. Wei, B., Shin, S., Laporte, D., Wolfe, A., and Romeo, T. (2000) Global regulatory mutations in csrA and rpoS cause severe central carbon stress in Escherichia coli. the presence of acetate. J Bacteriol 182: 1632-1640.
47. Wei, B., Brun-Zinkernagel, A., Simecka, J.W., Prub, BM., Babitzke, P., and Romeo, T. (2001) Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40: 245-256.
48. Yakhnin, A.V., Trimble, J.J., Chiaro, C.R., and Babitzke, P. (2000) Effects of mutations in the L-tryptophan binding pocket of the Trp RNA-binding attenuation protein of Bacillus subtilis. J Biol Chem 275: 4519-4524.
49. Yang, H., Liu, M., and Romeo, T. (1996) Coordinate regulation of glycogen catabolism and biosynthesis in Escherichia coli via the CsrA gene product. J Bacteriol 178: 1012-1017.
50. Zhang, A., Wassarman, K.M., Ortega, J., Steven, A.C., and Storz, G. (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9: 11-22.
51. Zuker, M., Mathews, D.H., and Turner, D.H. (1999) Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In RNA Biochemistry and Biotechnology. Barciszewski, J., and Clark, B.F.C. (eds). Dordrecht: Kluwer Academic Publishers, pp. 11-43.