1887

Abstract

The importance of Csr post-transcriptional systems is gradually emerging; these systems control a variety of virulence-linked physiological traits in many pathogenic bacteria. This review focuses on the central role that Csr systems play in the pathogenesis of certain bacteria and in the establishment of successful infections in animal hosts. Csr systems appear to control the ‘switch’ between different physiological states in the infection process; for example switching pathogens from a colonization state to a persistence state. Csr systems are controlled by two-component sensor/regulator systems and by non-coding RNAs. In addition, recent findings suggest that the RNA chaperone Hfq may play an integral role in Csr-mediated bacterial adaptation to the host environment.

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2008-01-01
2019-11-14
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References

  1. Agladze, K., Wang, X. & Romeo, T. ( 2005; ). Spatial periodicity of Escherichia coli K-12 biofilm microstructure initiates during a reversible, polar attachment phase of development and requires the polysaccharide adhesin PGA. J Bacteriol 187, 8237–8246.[CrossRef]
    [Google Scholar]
  2. Albus, A. M., Pesci, E. C., Runyen-Janecky, L. J., West, S. E. & Iglewski, B. H. ( 1997; ). Vfr controls quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179, 3928–3935.
    [Google Scholar]
  3. Altier, C., Suyemoto, M. & Lawhon, S. D. ( 2000; ). Regulation of Salmonella enterica serovar Typhimurium invasion genes by csrA. Infect Immun 68, 6790–6797.[CrossRef]
    [Google Scholar]
  4. Anantharaman, V. & Aravind, L. ( 2003; ). Application of comparative genomics in the identification and analysis of novel families of membrane-associated receptors in bacteria. BMC Genomics 4, 34 [CrossRef]
    [Google Scholar]
  5. Ang, S., Horng, Y. T., Shu, J. C., Soo, P. C., Liu, J. H., Yi, W. C., Lai, H. C., Luh, K. T., Ho, S. W. & other authors ( 2001; ). The role of RsmA in the regulation of swarming motility in Serratia marcescens. J Biomed Sci 8, 160–169.
    [Google Scholar]
  6. Babitzke, P. & Romeo, T. ( 2007; ). CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10, 156–163.[CrossRef]
    [Google Scholar]
  7. Bachman, M. A. & Swanson, M. S. ( 2001; ). RpoS co-operates with other factors to induce Legionella pneumophila virulence in the stationary phase. Mol Microbiol 40, 1201–1214.[CrossRef]
    [Google Scholar]
  8. Bachman, M. A. & Swanson, M. S. ( 2004a; ). Genetic evidence that Legionella pneumophila RpoS modulates expression of the transmission phenotype in both the exponential phase and the stationary phase. Infect Immun 72, 2468–2476.[CrossRef]
    [Google Scholar]
  9. Bachman, M. A. & Swanson, M. S. ( 2004b; ). The LetE protein enhances expression of multiple LetA/LetS-dependent transmission traits by Legionella pneumophila. Infect Immun 72, 3284–3293.[CrossRef]
    [Google Scholar]
  10. Baker, C. S., Morozov, I., Suzuki, K., Romeo, T. & Babitzke, P. ( 2002; ). CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 44, 1599–1610.[CrossRef]
    [Google Scholar]
  11. Baker, C. S., Eory, L. A., Yakhnin, H., Mercante, J., Romeo, T. & Babitzke, P. ( 2007; ). CsrA inhibits translation initiation of Escherichia coli hfq by binding to a single site overlapping the Shine-Dalgarno sequence. J Bacteriol 189, 5472–5481.[CrossRef]
    [Google Scholar]
  12. Barnard, F. M., Loughlin, M. F., Fainberg, H. P., Messenger, M. P., Ussery, D. W., Williams, P. & Jenks, P. J. ( 2004; ). Global regulation of virulence and the stress response by CsrA in the highly adapted human gastric pathogen Helicobacter pylori. Mol Microbiol 51, 15–32.
    [Google Scholar]
  13. Beatson, S. A., Whitchurch, C. B., Sargent, J. L., Levesque, R. C. & Mattick, J. S. ( 2002; ). Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. J Bacteriol 184, 3605–3613.[CrossRef]
    [Google Scholar]
  14. Beier, D. & Gross, R. ( 2006; ). Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9, 143–152.[CrossRef]
    [Google Scholar]
  15. Bejerano-Sagie, M. & Xavier, K. B. ( 2007; ). The role of small RNAs in quorum sensing. Curr Opin Microbiol 10, 189–198.[CrossRef]
    [Google Scholar]
  16. Brennan, R. G. & Link, T. M. ( 2007; ). Hfq structure, function and ligand binding. Curr Opin Microbiol 10, 125–133.[CrossRef]
    [Google Scholar]
  17. Burrowes, E., Abbas, A., O'Neill, A., Adams, C. & O'Gara, F. ( 2005; ). Characterisation of the regulatory RNA RsmB from Pseudomonas aeruginosa PAO1. Res Microbiol 156, 7–16.[CrossRef]
    [Google Scholar]
  18. Burrowes, E., Baysse, C., Adams, C. & O'Gara, F. ( 2006; ). Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152, 405–418.[CrossRef]
    [Google Scholar]
  19. Chien, M., Morozova, I., Shi, S., Sheng, H., Chen, J., Gomez, S. M., Asamani, G., Hill, K., Nuara, J. & other authors ( 2004; ). The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305, 1966–1968.[CrossRef]
    [Google Scholar]
  20. Clegg, S. & Hughes, K. T. ( 2002; ). FimZ is a molecular link between sticking and swimming in Salmonella enterica serovar Typhimurium. J Bacteriol 184, 1209–1213.[CrossRef]
    [Google Scholar]
  21. Cui, Y., Chatterjee, A., Liu, Y., Dumenyo, C. K. & Chatterjee, A. K. ( 1995; ). 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, 5108–5115.
    [Google Scholar]
  22. D'Argenio, D. A. & Miller, S. I. ( 2004; ). Cyclic di-GMP as a bacterial second messenger. Microbiology 150, 2497–2502.[CrossRef]
    [Google Scholar]
  23. Dasgupta, N., Ferrell, E. P., Kanack, K. J., West, S. E. & Ramphal, R. ( 2002; ). fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is σ 70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein. J Bacteriol 184, 5240–5250.[CrossRef]
    [Google Scholar]
  24. Diggle, S. P., Winzer, K., Chhabra, S. R., Worrall, K. E., Camara, M. & Williams, P. ( 2003; ). The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50, 29–43.[CrossRef]
    [Google Scholar]
  25. Ding, Y., Davis, B. M. & Waldor, M. K. ( 2004; ). Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol Microbiol 53, 345–354.[CrossRef]
    [Google Scholar]
  26. Dubey, A. K., Baker, C. S., Suzuki, K., Jones, A. D., Pandit, P., Romeo, T. & Babitzke, P. ( 2003; ). CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript. J Bacteriol 185, 4450–4460.[CrossRef]
    [Google Scholar]
  27. Dubey, A. K., Baker, C. S., Romeo, T. & Babitzke, P. ( 2005; ). RNA sequence and secondary structure participate in high-affinity CsrA–RNA interaction. RNA 11, 1579–1587.[CrossRef]
    [Google Scholar]
  28. Fettes, P. S., Forsbach-Birk, V., Lynch, D. & Marre, R. ( 2001; ). Overexpresssion of a Legionella pneumophila homologue of the E. coli regulator csrA affects cell size, flagellation, and pigmentation. Int J Med Microbiol 291, 353–360.[CrossRef]
    [Google Scholar]
  29. Folichon, M., Arluison, V., Pellegrini, O., Huntzinger, E., Regnier, P. & Hajnsdorf, E. ( 2003; ). The poly(A) binding protein Hfq protects RNA from RNase E and exoribonucleolytic degradation. Nucleic Acids Res 31, 7302–7310.[CrossRef]
    [Google Scholar]
  30. Forsbach-Birk, V., McNealy, T., Shi, C., Lynch, D. & Marre, R. ( 2004; ). Reduced expression of the global regulator protein CsrA in Legionella pneumophila affects virulence-associated regulators and growth in Acanthamoeba castellanii. Int J Med Microbiol 294, 15–25.[CrossRef]
    [Google Scholar]
  31. Fortune, D. R., Suyemoto, M. & Altier, C. ( 2006; ). Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect Immun 74, 331–339.[CrossRef]
    [Google Scholar]
  32. Gomez, M. I. & Prince, A. ( 2007; ). Opportunistic infections in lung disease: Pseudomonas infections in cystic fibrosis. Curr Opin Pharmacol 7, 244–251.[CrossRef]
    [Google Scholar]
  33. Goodman, A. L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R. S. & Lory, S. ( 2004; ). A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7, 745–754.[CrossRef]
    [Google Scholar]
  34. Gottesman, S. ( 2004; ). The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 58, 303–328.[CrossRef]
    [Google Scholar]
  35. Gudapaty, S., Suzuki, K., Wang, X., Babitzke, P. & Romeo, T. ( 2001; ). Regulatory interactions of Csr components: the RNA binding protein CsrA activates csrB transcription in Escherichia coli. J Bacteriol 183, 6017–6027.[CrossRef]
    [Google Scholar]
  36. Gutierrez, P., Li, Y., Osborne, M. J., Pomerantseva, E., Liu, Q. & Gehring, K. ( 2005; ). Solution structure of the carbon storage regulator protein CsrA from Escherichia coli. J Bacteriol 187, 3496–3501.[CrossRef]
    [Google Scholar]
  37. Hammer, B. K. & Bassler, B. L. ( 2003; ). Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50, 101–104.[CrossRef]
    [Google Scholar]
  38. Hammer, B. K., Tateda, E. S. & Swanson, M. S. ( 2002; ). A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol Microbiol 44, 107–118.[CrossRef]
    [Google Scholar]
  39. Heeb, S. & Haas, D. ( 2001; ). Regulatory roles of the GacS/GacA two-component system in plant-associated and other gram-negative bacteria. Mol Plant Microbe Interact 14, 1351–1363.[CrossRef]
    [Google Scholar]
  40. Heurlier, K., Williams, F., Heeb, S., Dormond, C., Pessi, G., Singer, D., Camara, M., Williams, P. & Haas, D. ( 2004; ). Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186, 2936–2945.[CrossRef]
    [Google Scholar]
  41. Hung, D. T., Zhu, J., Sturtevant, D. & Mekalanos, J. J. ( 2006; ). Bile acids stimulate biofilm formation in Vibrio cholerae. Mol Microbiol 59, 193–201.[CrossRef]
    [Google Scholar]
  42. Jackson, D. W., Suzuki, K., Oakford, L., Simecka, J. W., Hart, M. E. & Romeo, T. ( 2002; ). Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 184, 290–301.[CrossRef]
    [Google Scholar]
  43. Jain, V., Kumar, M. & Chatterji, D. ( 2006; ). ppGpp: stringent response and survival. J Microbiol 44, 1–10.
    [Google Scholar]
  44. Kajitani, M., Kato, A., Wada, A., Inokuchi, Y. & Ishihama, A. ( 1994; ). Regulation of the Escherichia coli hfq gene encoding the host factor for phage Qβ. J Bacteriol 176, 531–534.
    [Google Scholar]
  45. Kay, E., Humair, B., Denervaud, V., Riedel, K., Spahr, S., Eberl, L., Valverde, C. & Haas, D. ( 2006; ). Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 188, 6026–6033.[CrossRef]
    [Google Scholar]
  46. Kharazmi, A. ( 1991; ). Mechanisms involved in the evasion of the host defence by Pseudomonas aeruginosa. Immunol Lett 30, 201–205.[CrossRef]
    [Google Scholar]
  47. Kohler, T., van Delden, C., Curty, L. K., Hamzehpour, M. M. & Pechere, J. C. ( 2001; ). Overexpression of the MexEF-OprN multidrug efflux system affects cell-to-cell signaling in Pseudomonas aeruginosa. J Bacteriol 183, 5213–5222.[CrossRef]
    [Google Scholar]
  48. Kulkarni, P. R., Cui, X., Williams, J. W., Stevens, A. M. & Kulkarni, R. V. ( 2006; ). Prediction of CsrA-regulating small RNAs in bacteria and their experimental verification in Vibrio fischeri. Nucleic Acids Res 34, 3361–3369.[CrossRef]
    [Google Scholar]
  49. Laskowski, M. A. & Kazmierczak, B. I. ( 2006; ). Mutational analysis of RetS, an unusual sensor kinase-response regulator hybrid required for Pseudomonas aeruginosa virulence. Infect Immun 74, 4462–4473.[CrossRef]
    [Google Scholar]
  50. Lawhon, S. D., Frye, J. G., Suyemoto, M., Porwollik, S., McClelland, M. & Altier, C. ( 2003; ). Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 48, 1633–1645.[CrossRef]
    [Google Scholar]
  51. Lenz, D. H., Miller, M. B., Zhu, J., Kulkarni, R. V. & Bassler, B. L. ( 2005; ). CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol Microbiol 58, 1186–1202.[CrossRef]
    [Google Scholar]
  52. Liaw, S. J., Lai, H. C., Ho, S. W., Luh, K. T. & Wang, W. B. ( 2003; ). Role of RsmA in the regulation of swarming motility and virulence factor expression in Proteus mirabilis. J Med Microbiol 52, 19–28.[CrossRef]
    [Google Scholar]
  53. Liu, M. Y. & Romeo, T. ( 1997; ). The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein. J Bacteriol 179, 4639–4642.
    [Google Scholar]
  54. Liu, M. Y., Gui, G., Wei, B., Preston, J. F., III, Oakford, L., Yuksel, U., Giedroc, D. P. & Romeo, T. ( 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.[CrossRef]
    [Google Scholar]
  55. Liu, Z., Hsiao, A., Joelsson, A. & Zhu, J. ( 2006; ). The transcriptional regulator VqmA increases expression of the quorum-sensing activator HapR in Vibrio cholerae. J Bacteriol 188, 2446–2453.[CrossRef]
    [Google Scholar]
  56. Liu, Z., Stirling, F. R. & Zhu, J. ( 2007; ). Temporal quorum-sensing induction regulates Vibrio cholerae biofilm architecture. Infect Immun 75, 122–126.[CrossRef]
    [Google Scholar]
  57. Livny, J. & Waldor, M. K. ( 2007; ). Identification of small RNAs in diverse bacterial species. Curr Opin Microbiol 10, 96–101.[CrossRef]
    [Google Scholar]
  58. Majdalani, N., Vanderpool, C. K. & Gottesman, S. ( 2005; ). Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40, 93–113.[CrossRef]
    [Google Scholar]
  59. Marshall, B. ( 2006; ). Helicobacter connections. ChemMedChem 1, 783–802.[CrossRef]
    [Google Scholar]
  60. McNealy, T. L., Forsbach-Birk, V., Shi, C. & Marre, R. ( 2005; ). The Hfq homolog in Legionella pneumophila demonstrates regulation by LetA and RpoS and interacts with the global regulator CsrA. J Bacteriol 187, 1527–1532.[CrossRef]
    [Google Scholar]
  61. Mercante, J., Suzuki, K., Cheng, X., Babitzke, P. & Romeo, T. ( 2006; ). Comprehensive alanine-scanning mutagenesis of Escherichia coli CsrA defines two subdomains of critical functional importance. J Biol Chem 281, 31832–31842.[CrossRef]
    [Google Scholar]
  62. Moll, I., Afonyushkin, T., Vytvytska, O., Kaberdin, V. R. & Blasi, U. ( 2003; ). Coincident Hfq binding and RNase E cleavage sites on mRNA and small regulatory RNAs. RNA 9, 1308–1314.[CrossRef]
    [Google Scholar]
  63. Molofsky, A. B. & Swanson, M. S. ( 2003; ). Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol Microbiol 50, 445–461.[CrossRef]
    [Google Scholar]
  64. Molofsky, A. B. & Swanson, M. S. ( 2004; ). Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol 53, 29–40.[CrossRef]
    [Google Scholar]
  65. Morita, T., Maki, K. & Aiba, H. ( 2005; ). RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev 19, 2176–2186.[CrossRef]
    [Google Scholar]
  66. Mukherjee, A., Cui, Y., Liu, Y., Dumenyo, C. K. & Chatterjee, A. K. ( 1996; ). Global regulation in Erwinia species by Erwinia carotovora rsmA, a homologue of Escherichia coli csrA: repression of secondary metabolites, pathogenicity and hypersensitive reaction. Microbiology 142, 427–434.[CrossRef]
    [Google Scholar]
  67. Mulcahy, H., O'Callaghan, J., O'Grady, E. P., Adams, C. & O'Gara, F. ( 2006; ). The posttranscriptional regulator RsmA plays a role in the interaction between Pseudomonas aeruginosa and human airway epithelial cells by positively regulating the type III secretion system. Infect Immun 74, 3012–3015.[CrossRef]
    [Google Scholar]
  68. Nakao, H., Watanabe, H., Nakayama, S. & Takeda, T. ( 1995; ). yst gene expression in Yersinia enterocolitica is positively regulated by a chromosomal region that is highly homologous to Escherichia coli host factor 1 gene (hfq). Mol Microbiol 18, 859–865.[CrossRef]
    [Google Scholar]
  69. Patel, R. ( 2005; ). Biofilms and antimicrobial resistance. Clin Orthop Relat Res 437, 41–47.
    [Google Scholar]
  70. Pernestig, A. K., Georgellis, D., Romeo, T., Suzuki, K., Tomenius, H., Normark, S. & Melefors, O. ( 2003; ). The Escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J Bacteriol 185, 843–853.[CrossRef]
    [Google Scholar]
  71. Pessi, G., Williams, F., Hindle, Z., Heurlier, K., Holden, M. T., Camara, M., Haas, D. & Williams, P. ( 2001; ). The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183, 6676–6683.[CrossRef]
    [Google Scholar]
  72. Richter-Dahlfors, A., Buchan, A. M. & Finlay, B. B. ( 1997; ). Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 186, 569–580.[CrossRef]
    [Google Scholar]
  73. Rife, C., Schwarzenbacher, R., McMullan, D., Abdubek, P., Ambing, E., Axelrod, H., Biorac, T., Canaves, J. M., Chiu, H. J. & other authors ( 2005; ). Crystal structure of the global regulatory protein CsrA from Pseudomonas putida at 2.05 Å resolution reveals a new fold. Proteins 61, 449–453.[CrossRef]
    [Google Scholar]
  74. Rodrigue, A., Quentin, Y., Lazdunski, A., Mejean, V. & Foglino, M. ( 2000; ). Two-component systems in Pseudomonas aeruginosa: why so many? Trends Microbiol 8, 498–504.[CrossRef]
    [Google Scholar]
  75. Romeo, T. ( 1998; ). Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29, 1321–1330.[CrossRef]
    [Google Scholar]
  76. Romeo, T., Gong, M., Liu, M. Y. & 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.
    [Google Scholar]
  77. Ryan, R. P., Fouhy, Y., Lucey, J. F., Crossman, L. C., Spiro, S., He, Y. W., Zhang, L. H., Heeb, S., Camara, M. & other authors ( 2006; ). Cell–cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103, 6712–6717.[CrossRef]
    [Google Scholar]
  78. Schubert, M., Lapouge, K., Duss, O., Oberstrass, F. C., Jelesarov, I., Haas, D. & Allain, F. H. ( 2007; ). Molecular basis of messenger RNA recognition by the specific bacterial repressing clamp RsmA/CsrA. Nat Struct Mol Biol 14, 807–813.[CrossRef]
    [Google Scholar]
  79. Sledjeski, D. D., Whitman, C. & Zhang, A. ( 2001; ). Hfq is necessary for regulation by the untranslated RNA DsrA. J Bacteriol 183, 1997–2005.[CrossRef]
    [Google Scholar]
  80. Sonnleitner, E., Hagens, S., Rosenau, F., Wilhelm, S., Habel, A., Jager, K. E. & Blasi, U. ( 2003; ). Reduced virulence of a hfq mutant of Pseudomonas aeruginosa O1. Microb Pathog 35, 217–228.[CrossRef]
    [Google Scholar]
  81. Sonnleitner, E., Schuster, M., Sorger-Domenigg, T., Greenberg, E. P. & Blasi, U. ( 2006; ). Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aeruginosa. Mol Microbiol 59, 1542–1558.[CrossRef]
    [Google Scholar]
  82. Sorger-Domenigg, T., Sonnleitner, E., Kaberdin, V. R. & Blasi, U. ( 2007; ). Distinct and overlapping binding sites of Pseudomonas aeruginosa Hfq and RsmA proteins on the non-coding RNA RsmY. Biochem Biophys Res Commun 352, 769–773.[CrossRef]
    [Google Scholar]
  83. Storz, G. & Haas, D. ( 2007; ). A guide to small RNAs in microorganisms. Curr Opin Microbiol 10, 93–95.[CrossRef]
    [Google Scholar]
  84. Stover, C. K., Pham, X. Q., Erwin, A. L., Mizoguchi, S. D., Warrener, P., Hickey, M. J., Brinkman, F. S., Hufnagle, W. O., Kowalik, D. J. & other authors ( 2000; ). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959–964.[CrossRef]
    [Google Scholar]
  85. Suzuki, K., Wang, X., Weilbacher, T., Pernestig, A. K., Melefors, O., Georgellis, D., Babitzke, P. & Romeo, T. ( 2002; ). Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 184, 5130–5140.[CrossRef]
    [Google Scholar]
  86. Suzuki, K., Babitzke, P., Kushner, S. R. & Romeo, T. ( 2006; ). Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20, 2605–2617.[CrossRef]
    [Google Scholar]
  87. Szalewska-Palasz, A., Wegrzyn, G. & Wegrzyn, A. ( 2007; ). Mechanisms of physiological regulation of RNA synthesis in bacteria: new discoveries breaking old schemes. J Appl Genet 48, 281–294.[CrossRef]
    [Google Scholar]
  88. Tamayo, R., Pratt, J. T. & Camilli, A. ( 2007; ). Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61, 131–148.[CrossRef]
    [Google Scholar]
  89. Teplitski, M., Goodier, R. I. & Ahmer, B. M. ( 2003; ). Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J Bacteriol 185, 7257–7265.[CrossRef]
    [Google Scholar]
  90. Teplitski, M., Goodier, R. I. & Ahmer, B. M. ( 2006; ). Catabolite repression of the SirA regulatory cascade in Salmonella enterica. Int J Med Microbiol 296, 449–466.[CrossRef]
    [Google Scholar]
  91. Toledo-Arana, A., Repoila, F. & Cossart, P. ( 2007; ). Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol 10, 182–188.[CrossRef]
    [Google Scholar]
  92. Tomenius, H., Pernestig, A. K., Jonas, K., Georgellis, D., Mollby, R., Normark, S. & Melefors, O. ( 2006; ). The Escherichia coli BarA-UvrY two-component system is a virulence determinant in the urinary tract. BMC Microbiol 6, 27 [CrossRef]
    [Google Scholar]
  93. Toulokhonov, I. I., Shulgina, I. & Hernandez, V. J. ( 2001; ). Binding of the transcription effector ppGpp to Escherichia coli RNA polymerase is allosteric, modular, and occurs near the N terminus of the β′-subunit. J Biol Chem 276, 1220–1225.[CrossRef]
    [Google Scholar]
  94. Ventre, I., Goodman, A. L., Vallet-Gely, I., Vasseur, P., Soscia, C., Molin, S., Bleves, S., Lazdunski, A., Lory, S. & other authors ( 2006; ). Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci U S A 103, 171–176.[CrossRef]
    [Google Scholar]
  95. Venturi, V. ( 2006; ). Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30, 274–291.[CrossRef]
    [Google Scholar]
  96. Wang, X., Dubey, A. K., Suzuki, K., Baker, C. S., Babitzke, P. & Romeo, T. ( 2005; ). CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol 56, 1648–1663.[CrossRef]
    [Google Scholar]
  97. Wei, B. L., Brun-Zinkernagel, A. M., Simecka, J. W., Pruss, B. M., Babitzke, P. & Romeo, T. ( 2001; ). Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40, 245–256.[CrossRef]
    [Google Scholar]
  98. Weilbacher, T., Suzuki, K., Dubey, A. K., Wang, X., Gudapaty, S., Morozov, I., Baker, C. S., Georgellis, D., Babitzke, P. & other authors ( 2003; ). A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 48, 657–670.[CrossRef]
    [Google Scholar]
  99. West, S. E., Sample, A. K. & Runyen-Janecky, L. J. ( 1994; ). The vfr gene product, required for Pseudomonas aeruginosa exotoxin A and protease production, belongs to the cyclic AMP receptor protein family. J Bacteriol 176, 7532–7542.
    [Google Scholar]
  100. Yakhnin, H., Pandit, P., Petty, T. J., Baker, C. S., Romeo, T. & Babitzke, P. ( 2007; ). CsrA of Bacillus subtilis regulates translation initiation of the gene encoding the flagellin protein (hag) by blocking ribosome binding. Mol Microbiol 64, 1605–1620.[CrossRef]
    [Google Scholar]
  101. Zhu, J. & Mekalanos, J. J. ( 2003; ). Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5, 647–656.[CrossRef]
    [Google Scholar]
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