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The Two-Component Network and the General Stress Sigma Factor RpoS (σS) in Escherichia coli

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Bacterial Signal Transduction: Networks and Drug Targets

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 631))

Abstract

The general stress sigma factor RpoS (σs) is induced buring entry into stationary phase and in response to multiple stress conditions. RpoS is regulated at the levels of transcription, translation, proteolysis and protein activity. A key factor in RpoS control is the two-component response regulator RssB, which acts as a direct recognition and targeting factor for ClpXP-mediated RpoS proteolysis. A major, but not the only phosphodonor for RssB is the complex histidine sensor kinase ArcB. ArcB coordinates RpoS proteolysis with rpoS transcription by also phosphorylating the response regulator ArcA, which besides controlling a large regulon, also acts as a transcriptional repressor for rpoS. ArcB activity depends, on the redox state of the respiratory chain, which links RpoS control to the balance between energy supply and available respiratory electron acceptor. In addition, the BarA/UvrY and Rcs phosphorelay systems can activate rpoS transcription and translation respectively. These systems are involved in the control of motility, biofilm formation and/or virulence, suggesting that further studying a potential role of RpoS in these physiological functions may be rewarding.

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References

  1. Hengge-Aronis R. The general stress response in Escherichia coli. In: Storz G, Hengge-Aronis R, eds. Bacterial Stress Responses. Washington, D.C. ASM Press, 2000: 161–178.

    Google Scholar 

  2. Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the σs subunit of RNA polymerase in Escherichia coli. Microbiol Molec Biol Rev 2002; 66:373–395.

    Article  CAS  Google Scholar 

  3. Hengge-Aronis R. Stationary phase gene regulation: what makes an, Escherichia coli promoter σs-dependent? Curr Op Microbiol 2002; 5:591–595.

    Article  CAS  Google Scholar 

  4. Typas A, Hengge R. The molecular basis of selectivity of stress-regulated promoters of σ-containing RNA polymerase. Mol Microbiol 2007; 63:1296–1306.

    Article  PubMed  CAS  Google Scholar 

  5. Lacour S, Landini P. σs-dependent gene expression at the onset of stationary phase in Escherichia coli: function of σs-dependent genes and identification of their promoter, sequences. J Bacteriol 2004; 186:7186–7195.

    Article  PubMed  CAS  Google Scholar 

  6. Patten CL, Kirchhhof MG, Schertzberg MR et al. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12 Mol Genet Genomics 2004; 272:580–591.

    Article  PubMed  CAS  Google Scholar 

  7. Weber H, Polen T, Heuveling J et al. Genome-wide analysis of the general stress response network in Escherichia coli: σs-dependent genes, promoters and sigma factor selectivity. J Bacteriol 2005; 187:1591–1603.

    Article  PubMed  CAS  Google Scholar 

  8. Gentry DR, Hernandez VJ, Nguyen LH et al. Synthesis of the stationary-phase sigma factor σs is positively regulated by ppGpp. J Bacteriol 1993; 175:7982–7989.

    PubMed  CAS  Google Scholar 

  9. Lange R, Hengge-Aronis R. The cellular concentration of the σs subunit of RNA-polymerase in Escherichia coli is controlled at the levels of transcription, translation and protein stability. Genes Dev 1994; 8:1600–1612.

    Article  PubMed  CAS  Google Scholar 

  10. Lange R, Hengge-Aronis R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 1991; 5:49–59.

    Article  PubMed  CAS  Google Scholar 

  11. Fischer D, Teich A, Neubauer P et al. The general stress sigma factor σs of Escherichia coli is induced during diauxic shift from glucose to lactose. J Bacteriol 1998; 180:6203–6206.

    PubMed  CAS  Google Scholar 

  12. Muffler A, Traulsen DD, Lange R et al. Posttranscriptional osmotic regulation of the σs subunit of RNA polymerase in Escherichia coli. J Bacteriol 1996; 178:1607–1613.

    PubMed  CAS  Google Scholar 

  13. Lee IS, Lin J, Hall HK et al. The stationary-phase sigma factor σs (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium. Mol Microbiol 1995; 17:155–167.

    Article  PubMed  CAS  Google Scholar 

  14. Bearson SMD, Benjamin Jr. WH, Swords WE et al. Acid shock induction of RpoS is mediated by the mouse virulence gene mviA, of Salmonella typhimurium. J Bacteriol 1996; 178:2572–2579.

    PubMed  CAS  Google Scholar 

  15. Muffler A, Barth M, Marschall C et al. Heat shock regulation of σs turnover: a role for DnaK and relationship between stress responses mediated by σs and σ32 in Escherichia coli. J Bacteriol 1997; 179:445–452.

    PubMed  CAS  Google Scholar 

  16. Sledjeski DD, Gupta A, Gottesman S. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in E. coli. EMBO J 1996; 15:3993–4000.

    PubMed  CAS  Google Scholar 

  17. Lange R, Fischer D, Hengge-Aronis R. Identification, of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the σs subunit of RNA-polymerase in Escherichia coli. J Bacteriol 1995; 177:4676–4680.

    PubMed  CAS  Google Scholar 

  18. Teich A, Meyer S, Lin HY et al. Growth rate related concentration changes of the starvation response regulators σs and ppGpp in glucose-limited fed-batch and continuous cultures of Escherichia coli. Biotechnol Progr 1999; 15:123–129.

    Article  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  20. Majdalani N, Cunning C, Sledjeski D et al. DsrA, RNA regulates translation of RpoS message by an antiantisense mechanisms independent of its action as an antisilencer of transcription. Proc Natl Acad Sci USA 1998; 95:12462–12467.

    Article  PubMed  CAS  Google Scholar 

  21. Majdalani N, Hermandez D, Gottesman S. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 2002; 46:813–826.

    Article  PubMed  CAS  Google Scholar 

  22. Muffler A, Fischer D, Hengge-Aronis R. The RNA-binding protein HF-I, known as a host factor for phage Qβ RNA replication, is essential for the translational regulation of rpoS in Escherichia coli. Genes Dev 1996; 10:1143–1151.

    Article  PubMed  CAS  Google Scholar 

  23. Repoila F, Majdalani N, Gottesman S. Small noncoding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol Microbiol 2003; 48:855–862.

    Article  PubMed  CAS  Google Scholar 

  24. Worhunsky DJ, Godek K, Litsch S et al. Interactions of the noncoding RNA DsrA and RpoS mRNA with the 30 S ribosomal subunit. J Biol Chem 2003; 278:15815–15824.

    Article  PubMed  CAS  Google Scholar 

  25. Becker G, Klauek E, Hengge-Aronis R. Regulation of RpoS proteolysis in Escherichia coli: The response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc Natl Acad Sci USA 1999; 96:6439–6444.

    Article  PubMed  CAS  Google Scholar 

  26. Klauck E, Lingnau M, Hengge-Aronis R. Role of the response regulator RssB in σs recognition and initiation of σs proteolysis in Escherichia coli. Mol Microbiol 2001; 40:1381–1390.

    Article  PubMed  CAS  Google Scholar 

  27. Muffler A, Fischer D, Altuvia S et al. The response regulator RssB controls stability of the σs subunit of RNA polymerase in Escherichia coli. EMBO J 1996; 15:1333–1339.

    PubMed  CAS  Google Scholar 

  28. Pratt LA, Silhavy TJ. The response regulator, SprE, controls the stability of RpoS. Proc Natl Acad Sci USA 1996; 93:2488–2492.

    Article  PubMed  CAS  Google Scholar 

  29. Schweder T, Lee K-H, Lomovskaya O et al. Regulation of Escherichia coli starvation sigma factor (σs) by ClpXP protease. J Bacteriol 1996; 178:470–476.

    PubMed  CAS  Google Scholar 

  30. Zhou Y, Gottesman S, Hoskins JR et al. The RssB response regulator directly targets σs for degradation by ClpXP. Genes Dev 2001; 15:627–637.

    Article  PubMed  CAS  Google Scholar 

  31. Jishage M, Ishihama A. Transcriptional organization and in vivo role of the Escherichia coli rsd gene, encoding the regulator of RNA polymerase sigma D. J Bacteriol 1999; 181:3768–3776.

    PubMed  CAS  Google Scholar 

  32. Jishage M, Kvint K, Shingler V et al. Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev 2002; 16:1260–1270.

    Article  PubMed  CAS  Google Scholar 

  33. Pratt LA, Silhavy TJ. Crl stimulates RpoS activity during stationary phase. Mol Microbiol 1998; 29:1225–1236.

    Article  PubMed  CAS  Google Scholar 

  34. Typas A, Barembruch C, Hengge R. Stationary phase reorganisation of the E. coli transcription machinery by Crl protein, a fine-tuner of σs activity and levels. EMBO J 2007; 26:1569–1578.

    Article  PubMed  CAS  Google Scholar 

  35. Pruteanu M, Hengge-Aronis R. The cellular level of the recognition factor RssB is rate-limiting for σs proteolysis: Implications for RssB regulation and signal transduction in σs turnover in Escherichia coli. Mol Microbiol 2002; 45:1701–1714.

    Article  PubMed  CAS  Google Scholar 

  36. Stüdemann A, Noirelere-Savoye M, Klauck E et al. Sequential recognition of two distinct sites in σs by the proteolytic targeting factor RssB and ClpX. EMBO J 2003; 22:4111–4120.

    Article  PubMed  Google Scholar 

  37. Mika F, Hengge R. A two-component phosphotransfer network involving ArcB, ArcA and RssB coordinates synthesis and proteolysis of σs in E. coli. Genes Dev 2005; 19:2770–2781.

    Article  PubMed  CAS  Google Scholar 

  38. Becker G, Klauck E, Hengge-Aronis R. The response regulator RssB, a recognition factor for σs proteolysis in Escherichia coli, can act like an antiσs factor. Mol Microbiol 2000; 35:657–666.

    Article  PubMed  CAS  Google Scholar 

  39. Galperin MY. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 2006: 188:4169–4182.

    Article  PubMed  CAS  Google Scholar 

  40. Becker G, Hengge-Aronis R. What makes an Escherichia coli promoter σs-dependent? Role of the −13/−14 nucleotide promoter positions and region 2.5 of σs. Mol Microbiol 2001; 39:1153–1165.

    Article  PubMed  CAS  Google Scholar 

  41. Dougan DA, Weber-Ban E, Bukau B. Targeted delivery of an ssrA-tagged, substrate by the adaptor protein SspB to its cognate AAA+ protein ClpX. Mol Cell 2003; 12:373–380.

    Article  PubMed  CAS  Google Scholar 

  42. Flynn JM, Levehenko I, Seidel M et al. Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis. Proc Natl Acad Sci 2001; 98:10584–10589.

    Article  PubMed  CAS  Google Scholar 

  43. Wah DA, Levchenko I, Baker TA et al. Characterization of a specificity factor for an AAA+ATPase. Assembly of SspB dimers with ssrA-tagged proteins and the ClpX hexamer. Chem Biol 2002; 9:1237–1245.

    Article  PubMed  CAS  Google Scholar 

  44. Kirstein J, Schlothauer T, Dougan DAd et al. Adaptor protein controlled oligomerization activates the AAA+ protein ClpC. EMBO J 2006; 25:1481–1491.

    Article  PubMed  CAS  Google Scholar 

  45. Jenal U, Hengge-Aronis R. Regulation by proteolysis in bacterial cells. Curr Opin Microbiol 2003; 6:163–172.

    Article  PubMed  CAS  Google Scholar 

  46. Bouché S, Klauck E, Fischer D et al. Regulation of RssB-dependent proteolysis in Escherichia coli: a role for acetyl phosphate in a response regulator-controlled process. Mol Microbiol 1998; 27:787–795.

    Article  PubMed  Google Scholar 

  47. Bougdour A, Wickner S, Gottesman S. Modulating RssB activity: IraP, a novel regulator of σs stability in Escherichia coli. Genes Dev 2006; 20:884–897.

    Article  PubMed  CAS  Google Scholar 

  48. Bougdour A, Lelong C, Geiselmann J. Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J Biol Chem 2004; 279:19540–19550

    Article  PubMed  CAS  Google Scholar 

  49. Gonzalez-Barrios AF, Zuo R, Hashimoto Y et al. Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 2006; 188:305–316.

    Article  PubMed  Google Scholar 

  50. Peterson CN, Ruiz N, Silhavy TJ. RpoS proteolysis is regulated by a mechanism that does not require the SprE (RssB) response regulator phosphorylation site. J Bacteriol 2004; 186:7403–7410.

    Article  PubMed  CAS  Google Scholar 

  51. Ruiz N, Peterson CN, Silhavy TJ. RpoS-dependent transcriptional control of sprE: regulatory feedback loop. J Bacteriol 2001; 183:5974–5981.

    Article  PubMed  CAS  Google Scholar 

  52. McCleary WR, Stock JB. Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 1994; 269:31567–31572.

    PubMed  CAS  Google Scholar 

  53. Oshima T, Aiba H, Masuda Y et al. Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli. Mol Microbiol 2002; 46:281–291.

    Article  PubMed  CAS  Google Scholar 

  54. Sugiura M, Aiba H, Mizuno T. Identification and classification of two-component systems that affect rpoS expression in Escherichia coli. Biosci Biotechnol Biochem 2003; 67:1612–1615.

    Article  PubMed  CAS  Google Scholar 

  55. Yamamoto K, Hirao K, Oshima T et al. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 2005; 208:1448–1456.

    Google Scholar 

  56. Malpica R, Sandoval GR, Rodriguez C et al. Signaling by the are two-component system provides a link between the redox state of the quinone pool and gene expression. Antioxid Redox Signal 2006; 8:781–795.

    Article  PubMed  CAS  Google Scholar 

  57. Georgellis D, Kwon O, Lin ECC. Quinones as the redox signal for the Arc Two-component system of bacteria. Science 2001; 292:2314–2315.

    Article  PubMed  CAS  Google Scholar 

  58. Malpica R, Franco B, Rodriguez C et al. Identification of quinone-sensitive redox switch in, the ArcB sensor kinase. Proc Natl Acad Sci USA 2004; 101:13318–13323.

    Article  PubMed  CAS  Google Scholar 

  59. Georgellis D, Kwon O, De Wulf P et al. Signal decay through a reverse phosphorelay in the Arc two-component signal transduction system. J Biol Chem 1998; 273:32864–32869.

    Article  PubMed  CAS  Google Scholar 

  60. Wright JS, Olekhnovich IN, Touchie G et al. The histidine kinase domain of UhpB inhibits UhpA action at the Escherichia coli uhpT promoter. J Bacteriol 2000; 182:6279–6286.

    Article  PubMed  CAS  Google Scholar 

  61. Sourjik V. Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol 2005; 12:569–576.

    Article  Google Scholar 

  62. Backfisch T, Pruteanu M, Hengge R et al. Mathematical modeling of RpoS regulation in E. coli. Found Systems Biol Engineer 2005:239–242.

    Google Scholar 

  63. Mukhopadhyay S, Audia JP, Roy RN et al. Transcriptional induction of the conserved alternative sigma factor RpoS in Escherichia coli is dependent on BarA, a probable two-component regulator. Mol Microbiol 2000; 37:371–381.

    Article  PubMed  CAS  Google Scholar 

  64. Pernestig A-K, Melefors Ö, Georgellis D. Identification of UvrY as the cognate response regulator for the BarA sensor kinase in Eschrichia coli. J Biol Chem 2001; 276:225–231.

    Article  PubMed  CAS  Google Scholar 

  65. Pernestig A-K, Georgellis D, Romeo T et al. The escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J Bacteriol 2003; 185:843–853.

    Article  PubMed  CAS  Google Scholar 

  66. Teplitski M, Goodier RI, Ahmer BM. Pathways lieading from BarA/SirA to motility and virulence gene expression in Salmonella. J Bacteriol 2003; 185:7257–7265.

    Article  PubMed  CAS  Google Scholar 

  67. Tomenius H, Pernestig AK, Jonas K et al. The Escherichia coli BarA-UvrY two-component system is a virulence determinant in the urinary tract. BMC Microbiol 2006; 6:27-.

    Article  PubMed  Google Scholar 

  68. Suzuki K, Wang X, Weilbacher T et al. Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 2002; 184:5130–5140.

    Article  PubMed  CAS  Google Scholar 

  69. Romeo T. Global regulation by the small RNA-binding protein CsrA and the noncoding RNA molecule CsrB. Mol Microbiol 1998; 29:1321–1330.

    Article  PubMed  CAS  Google Scholar 

  70. Weber H, Pesavento C, Possling A et al. Cyclic-di-GMP-mediated signaling within the σs network of Escherichia coli. Mol Microbiol 2006; 62:1014–1034.

    Article  PubMed  CAS  Google Scholar 

  71. Jenal U. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr Opin Microbiol 2004; 7:185–191.

    Article  PubMed  CAS  Google Scholar 

  72. Simm R, Morr M, Kader A et al. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 2004; 53:1123–1134.

    Article  PubMed  CAS  Google Scholar 

  73. Majdalani N, Gottesman S. The Res phosphorelay: a complex signal transduction system. Annu Rev Microbiol 2005; 599:379–405.

    Article  Google Scholar 

  74. Francez-Charlot A, Laugel B, Van Gemert A et al. ResCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol Microbiol 2003; 49:823–832.

    Article  PubMed  CAS  Google Scholar 

  75. Gottesman S, Trisler P, Torres-Cabassa AS. Regulation of capsular polysaccharide synthesis in Escherichia coli K12: characterization of three regulatory genes. J Bacteriol 1985; 162:1111–1119.

    PubMed  CAS  Google Scholar 

  76. Majdalani N, Chen S, Murrow J et al. Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol 2001; 39:1382–1394.

    Article  PubMed  CAS  Google Scholar 

  77. Peterson CN, Carabetta VJ, Chowdhury T et al. LrhA regulates rpoS translation in response to the Res phosphorelay system in Escherichia coli. J Bacteriol 2006; 188:3175–3181.

    Article  PubMed  CAS  Google Scholar 

  78. Lehnen D, Blumer C, Polen T et al. LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol Microbiol 2002; 45:521–532.

    Article  PubMed  CAS  Google Scholar 

  79. Mangan S, Alon U. Structure and function of the feed-forward loop network motif. Proc. Natl Acad Sci USA 2003; 100:11980–11985.

    Article  PubMed  CAS  Google Scholar 

  80. Froclich JM, Tran K, Wall D. A pmrA constitutive mutant sensitizes Escherichia coli to deoxycholic acid. J Bacteriol 2006; 188:1180–1183.

    Article  Google Scholar 

  81. Hagiwara D, Yamashino T, Mizuno T. A genome-wide view of the Escherichia coli BasS-BasR two-component system implicated in iron-responses. Biosci Biotechnol Biochem 2004; 68:1758–1768.

    Article  PubMed  CAS  Google Scholar 

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Hengge, R. (2008). The Two-Component Network and the General Stress Sigma Factor RpoS (σS) in Escherichia coli . In: Utsumi, R. (eds) Bacterial Signal Transduction: Networks and Drug Targets. Advances in Experimental Medicine and Biology, vol 631. Springer, New York, NY. https://doi.org/10.1007/978-0-387-78885-2_4

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