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EcoSal Plus

Domain 5:

Responding to the Environment

Envelope Stress Responses

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  • Authors: Dawn M. Macritchie1, and Tracy L. Raivio2
  • Editor: James M. Slauch3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada.; 2: Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada.; 3: The Schoold of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL
  • Received 07 January 2009 Accepted 16 March 2009 Published 29 July 2009
  • Address correspondence to Tracy L. Raivio traivio@ualberta.ca.
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  • Abstract:

    The gram-negative bacterial envelope is a complex extracytoplasmic compartment responsible for numerous cellular processes. Among its most important functions is its service as the protective layer separating the cytoplasmic space from the ever-changing external environment. To adapt to the diverse conditions encountered both in the environment and within the mammalian host, and species have evolved six independent envelope stress response systems . This review reviews the sE response, the CpxAR and BaeSR two-component systems (TCS) , the phage shock protein response, and the Rcs phosphorelay system. These five signal transduction pathways represent the most studied of the six known stress responses. The signal for adhesion to abiotic surfaces enters the pathway through the novel outer membrane lipoprotein NlpE, and activation on entry into the exponential phase of growth occurs independently of CpxA . Adhesion could disrupt NlpE causing unfolding of its unstable N-terminal domain, leading to activation of the Cpx response. The most recent class of genes added to the Cpx regulon includes those involved in copper homeostasis. Two separate microarray experiments revealed that exposure of cells to high levels of external copper leads to upregulation of several Cpx regulon members. The BaeSR TCS has also been shown to mediate drug resistance in . Similar to , the Bae pathway of mediates resistance to oxacillin, novobiocin, deoxycholate, β-lactams, and indole.

  • Citation: Macritchie D, Raivio T. 2009. Envelope Stress Responses, EcoSal Plus 2009; doi:10.1128/ecosalplus.5.4.7

Key Concept Ranking

Two-Component Signal Transduction Systems
0.550291
Rcs Phosphorelay System
0.42153695
Stress Response Systems
0.38953868
Outer Membrane Proteins
0.38545704
0.550291

References

1. McBroom AJ, Kuehn MJ. 12 May 2005, posting date. Outer membrane vesicles. In R Curtiss III (Editor in Chief), EcoSal—Escherichia coli and Salmonella: Cellular and Molecular Biology. [Online] http://www.ecosal.org. ASM Press, Washington, DC.
2. Erickson JW, Gross CA. 1989. Identification of the sigma E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression. Genes Dev 3:1462–1471. [PubMed][CrossRef]
3. Wang QP, Kaguni JM. 1989. A novel sigma factor is involved in expression of the rpoH gene of Escherichia coli. J Bacteriol 171:4248–4253.[PubMed]
4. Erickson JW, Vaughn V, Walter WA, Neidhardt FC, Gross CA. 1987. Regulation of the promoters and transcripts of rpoH, the Escherichia coli heat shock regulatory gene. Genes Dev 1:419–432. [PubMed][CrossRef]
5. Mecsas J, Rouviere PE, Erickson JW, Donohue TJ, Gross CA. 1993. The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev 7:2618–2628. [PubMed][CrossRef]
6. Raina S, Missiakas D, Georgopoulos C. 1995. The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli. EMBO J 14:1043–1055.[PubMed]
7. De Las Penas A, Connolly L, Gross CA. 1997. SigmaE is an essential sigma factor in Escherichia coli. J Bacteriol 179:6862–6864.[PubMed]
8. Missiakas D, Betton JM, Raina S. 1996. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol 21:871–884. [PubMed][CrossRef]
9. Rouviere PE, Gross CA. 1996. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev 10:3170–3182. [PubMed][CrossRef]
10. De Las Penas A, Connolly L, Gross CA. 1997. The sigmaE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigmaE. Mol Microbiol 24:373–385. [PubMed][CrossRef]
11. Missiakas D, Mayer MP, Lemaire M, Georgopoulos C, Raina S. 1997. Modulation of the Escherichia coli sigmaE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol Microbiol 24:355–371. [PubMed][CrossRef]
12. Ades SE, Connolly LE, Alba BM, Gross CA. 1999. The Escherichia coli sigma(E)-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Genes Dev 13:2449–2461. [PubMed][CrossRef]
13. Collinet B, Yuzawa H, Chen T, Herrera C, Missiakas D. 2000. RseB binding to the periplasmic domain of RseA modulates the RseA:sigmaE interaction in the cytoplasm and the availability of sigmaE-RNA polymerase. J Biol Chem 275:33898–33904. [PubMed][CrossRef]
14. Alba BM, Zhong HJ, Pelayo JC, Gross CA. 2001. degS (hhoB) is an essential Escherichia coli gene whose indispensable function is to provide sigma (E) activity. Mol Microbiol 40:1323–1333. [PubMed][CrossRef]
15. Alba BM, Leeds JA, Onufryk C, Lu CZ, Gross CA. 2002. DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes Dev 16:2156–2168. [PubMed][CrossRef]
16. Dartigalongue C, Missiakas D, Raina S. 2001. Characterization of the Escherichia coli sigma E regulon. J Biol Chem 276:20866–20875. [PubMed][CrossRef]
17. Kanehara K, Akiyama Y, Ito K. 2001. Characterization of the yaeL gene product and its S2P-protease motifs in Escherichia coli. Gene 281:71–79. [PubMed][CrossRef]
18. Kanehara K, Ito K, Akiyama Y. 2002. YaeL (EcfE) activates the sigma(E) pathway of stress response through a site-2 cleavage of anti-sigma(E), RseA. Genes Dev 16:2147–2155. [PubMed][CrossRef]
19. Harris BZ, Lim WA. 2001. Mechanism and role of PDZ domains in signaling complex assembly. J Cell Sci 114:3219–3231.[PubMed]
20. Walsh NP, Alba BM, Bose B, Gross CA, Sauer RT. 2003. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113:61–71. [PubMed][CrossRef]
21. Sohn J, Grant RA, Sauer RT. 2007. Allosteric activation of DegS, a stress sensor PDZ protease. Cell 131:572–583. [PubMed][CrossRef]
22. Wilken C, Kitzing K, Kurzbauer R, Ehrmann M, Clausen T. 2004. Crystal structure of the DegS stress sensor: How a PDZ domain recognizes misfolded protein and activates a protease. Cell 117:483–494. [PubMed][CrossRef]
23. Zeth K. 2004. Structural analysis of DegS, a stress sensor of the bacterial periplasm. FEBS Lett 569:351–358. [PubMed][CrossRef]
24. Hasselblatt H, Kurzbauer R, Wilken C, Krojer T, Sawa J, Kurt J, Kirk R, Hasenbein S, Ehrmann M, Clausen T. 2007. Regulation of the sigmaE stress response by DegS: how the PDZ domain keeps the protease inactive in the resting state and allows integration of different OMP-derived stress signals upon folding stress. Genes Dev 21:2659–2670. [PubMed][CrossRef]
25. Kanehara K, Ito K, Akiyama Y. 2003. YaeL proteolysis of RseA is controlled by the PDZ domain of YaeL and a Gln-rich region of RseA. EMBO J 22:6389–6398. [PubMed][CrossRef]
26. Ades SE. 2004. Control of the alternative sigma factor sigmaE in Escherichia coli. Curr Opin Microbiol 7:157–162. [PubMed][CrossRef]
27. Campbell EA, Tupy JL, Gruber TM, Wang S, Sharp MM, Gross CA, Darst SA. 2003. Crystal structure of Escherichia coli sigmaE with the cytoplasmic domain of its anti-sigma RseA. Mol Cell 11:1067–1078. [PubMed][CrossRef]
28. Flynn JM, Levchenko I, Sauer RT, Baker TA. 2004. Modulating substrate choice: the SspB adaptor delivers a regulator of the extracytoplasmic-stress response to the AAA+ protease ClpXP for degradation. Genes Dev 18:2292–2301. [PubMed][CrossRef]
29. Chaba R, Grigorova IL, Flynn JM, Baker TA, Gross CA. 2007. Design principles of the proteolytic cascade governing the sigmaE-mediated envelope stress response in Escherichia coli: keys to graded, buffered, and rapid signal transduction. Genes Dev 21:124–136. [PubMed][CrossRef]
30. Ades SE, Grigorova IL, Gross CA. 2003. Regulation of the alternative sigma factor sigma(E) during initiation, adaptation, and shutoff of the extracytoplasmic heat shock response in Escherichia coli. J Bacteriol 185:2512–2519. [PubMed][CrossRef]
31. Cezairliyan BO, Sauer RT. 2007. Inhibition of regulated proteolysis by RseB. Proc Natl Acad Sci USA 104:3771–3776. [PubMed][CrossRef]
32. Grigorova IL, Chaba R, Zhong HJ, Alba BM, Rhodius V, Herman C, Gross CA. 2004. Fine-tuning of the Escherichia coli sigmaE envelope stress response relies on multiple mechanisms to inhibit signal-independent proteolysis of the transmembrane anti-sigma factor, RseA. Genes Dev 18:2686–2697. [PubMed][CrossRef]
33. Kim DY, Jin KS, Kwon E, Ree M, Kim KK. 2007. Crystal structure of RseB and a model of its binding mode to RseA. Proc Natl Acad Sci USA 104:8779–8784.[PubMed]
34. Button JE, Silhavy TJ, Ruiz N. 2007. A suppressor of cell death caused by the loss of sigmaE downregulates extracytoplasmic stress responses and outer membrane vesicle production in Escherichia coli. J Bacteriol 189:1523–1530. [PubMed][CrossRef]
35. Rezuchova B, Kormanec J. 2001. A two-plasmid system for identification of promoters recognized by RNA polymerase containing extracytoplasmic stress response sigma(E) in Escherichia coli. J Microbiol Methods 45:103–111. [PubMed][CrossRef]
36. Rezuchova B, Miticka H, Homerova D, Roberts M, Kormanec J. 2003. New members of the Escherichia coli sigmaE regulon identified by a two-plasmid system. FEMS Microbiol Lett 225:1–7. [PubMed][CrossRef]
37. Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. 2006. Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 4:e2. [PubMed][CrossRef]
38. Skovierova H, Rowley G, Rezuchova B, Homerova D, Lewis C, Roberts M, Kormanec J. 2006. Identification of the sigmaE regulon of Salmonella enterica serovar Typhimurium. Microbiology 152:1347–1359. [PubMed][CrossRef]
39. Humphreys S, Stevenson A, Bacon A, Weinhardt AB, Roberts M. 1999. The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect Immun 67:1560–1568.[PubMed]
40. Johnson K, Charles I, Dougan G, Pickard D, O'Gaora P, Costa G, Ali T, Miller I, Hormaeche C. 1991. The role of a stress-response protein in Salmonella typhimurium virulence. Mol Microbiol 5:401–407. [PubMed][CrossRef]
41. Raivio TL. 2005. Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol 56:1119–1128. [PubMed][CrossRef]
42. Redford P, Roesch PL, Welch RA. 2003. DegS is necessary for virulence and is among extraintestinal Escherichia coli genes induced in murine peritonitis. Infect Immun 71:3088–3096. [PubMed][CrossRef]
43. Rowley G, Spector M, Kormanec J, Roberts M. 2006. Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat Rev Microbiol 4:383–394. [PubMed][CrossRef]
44. Sydenham M, Douce G, Bowe F, Ahmed S, Chatfield S, Dougan G. 2000. Salmonella enterica serovar Typhimurium surA mutants are attenuated and effective live oral vaccines. Infect Immun 68:1109–1115. [PubMed][CrossRef]
45. Testerman TL, Vazquez-Torres A, Xu Y, Jones-Carson J, Libby SJ, Fang FC. 2002. The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol Microbiol 43:771–782. [PubMed][CrossRef]
46. Hayden JD, Ades SE. 2008. The extracytoplasmic stress factor, sigmaE, is required to maintain cell envelope integrity in Escherichia coli. PLoS ONE 3:e1573. [PubMed][CrossRef]
47. Kabir MS, Yamashita D, Koyama S, Oshima T, Kurokawa K, Maeda M, Tsunedomi R, Murata M, Wada C, Mori H, Yamada M. 2005. Cell lysis directed by sigmaE in early stationary phase and effect of induction of the rpoE gene on global gene expression in Escherichia coli. Microbiology 151:2721–2735. [PubMed][CrossRef]
48. Douchin V, Bohn C, Bouloc P. 2006. Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. J Biol Chem 281:12253–12259. [PubMed][CrossRef]
49. Figueroa-Bossi N, Lemire S, Maloriol D, Balbontin R, Casadesus J, Bossi L. 2006. Loss of Hfq activates the sigmaE-dependent envelope stress response in Salmonella enterica. Mol Microbiol 62:838–852. [PubMed][CrossRef]
50. Johansen J, Rasmussen AA, Overgaard M, Valentin-Hansen P. 2006. Conserved small non-coding RNAs that belong to the sigmaE regulon: role in down-regulation of outer membrane proteins. J Mol Biol 364:1–8. [PubMed][CrossRef]
51. Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton JC, Vogel J. 2006. SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global Omp mRNA decay. Mol Microbiol 62:1674–1688. [PubMed][CrossRef]
52. Thompson KM, Rhodius VA, Gottesman S. 2007. SigmaE regulates and is regulated by a small RNA in Escherichia coli. J Bacteriol 189:4243–4256. [PubMed][CrossRef]
53. Udekwu KI, Darfeuille F, Vogel J, Reimegard J, Holmqvist E, Wagner EG. 2005. Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 19:2355–2366. [PubMed][CrossRef]
54. Udekwu KI, Wagner EG. 2007. Sigma E controls biogenesis of the antisense RNA MicA. Nucleic Acids Res 35:1279–1288. [PubMed][CrossRef]
55. Aiba H, Matsuyama S, Mizuno T, Mizushima S. 1987. Function of micF as an antisense RNA in osmoregulatory expression of the ompF gene in Escherichia coli. J Bacteriol 169:3007–3012.[PubMed]
56. Andersen J, Delihas N. 1990. micF RNA binds to the 5′ end of ompF mRNA and to a protein from Escherichia coli. Biochemistry 29:9249–9256. [PubMed][CrossRef]
57. Guisbert E, Rhodius VA, Ahuja N, Witkin E, Gross CA. 2007. Hfq modulates the sigmaE-mediated envelope stress response and the sigma32-mediated cytoplasmic stress response in Escherichia coli. J Bacteriol 189:1963–1973. [PubMed][CrossRef]
58. McEwen J, Silverman P. 1980. Chromosomal mutations of Escherichia coli that alter expression of conjugative plasmid functions. Proc Natl Acad Sci USA 77:513–517. [PubMed][CrossRef]
59. McEwen J, Silverman P. 1980. Genetic analysis of Escherichia coli K-12 chromosomal mutants defective in expression of F-plasmid functions: identification of genes cpxA and cpxB. J Bacteriol 144:60–67.[PubMed]
60. McEwen J, Silverman P. 1980. Mutations in genes cpxA and cpxB of Escherichia coli K-12 cause a defect in isoleucine and valine syntheses. J Bacteriol 144:68–73.[PubMed]
61. McEwen J, Silverman PM. 1982. Mutations in genes cpxA and cpxB alter the protein composition of Escherichia coli inner and outer membranes. J Bacteriol 151:1553–1559.[PubMed]
62. Albin R, Weber R, Silverman PM. 1986. The Cpx proteins of Escherichia coli K12. Immunologic detection of the chromosomal cpxA gene product. J Biol Chem 261:4698–4705.[PubMed]
63. Weber RF, Silverman PM. 1988. The cpx proteins of Escherichia coli K12. Structure of the cpxA polypeptide as an inner membrane component. J Mol Biol 203:467–478. [PubMed][CrossRef]
64. Krikos A, Mutoh N, Boyd A, Simon MI. 1983. Sensory transducers of E. coli are composed of discrete structural and functional domains. Cell 33:615–622. [PubMed][CrossRef]
65. Dong J, Iuchi S, Kwan HS, Lu Z, Lin EC. 1993. The deduced amino-acid sequence of the cloned cpxR gene suggests the protein is the cognate regulator for the membrane sensor, CpxA, in a two-component signal transduction system of Escherichia coli. Gene 136:227–230. [PubMed][CrossRef]
66. Cosma CL, Danese PN, Carlson JH, Silhavy TJ, Snyder WB. 1995. Mutational activation of the Cpx signal transduction pathway of Escherichia coli suppresses the toxicity conferred by certain envelope-associated stresses. Mol Microbiol 18:491–505. [PubMed][CrossRef]
67. Danese PN, Snyder WB, Cosma CL, Davis LJ, Silhavy TJ. 1995. The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9:387–398. [PubMed][CrossRef]
68. Snyder WB, Davis LJ, Danese PN, Cosma CL, Silhavy TJ. 1995. Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J Bacteriol 177:4216–4223.[PubMed]
69. Danese PN, Silhavy TJ. 1997. The sigma(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev 11:1183–1193. [PubMed][CrossRef]
70. Pogliano J, Lynch AS, Belin D, Lin EC, Beckwith J. 1997. Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev 11:1169–1182. [PubMed][CrossRef]
71. Raivio TL, Silhavy TJ. 1997. Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J Bacteriol 179:7724–7733.[PubMed]
72. Danese PN, Silhavy TJ. 1998. CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180:831–839.[PubMed]
73. Raivio TL, Popkin DL, Silhavy TJ. 1999. The Cpx envelope stress response is controlled by amplification and feedback inhibition. J Bacteriol 181:5263–5272.[PubMed]
74. Fleischer R, Heermann R, Jung K, Hunke S. 2007. Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli. J Biol Chem 282:8583–8593. [PubMed][CrossRef]
75. Buelow DR, Raivio TL. 2005. Cpx signal transduction is influenced by a conserved N-terminal domain in the novel inhibitor CpxP and the periplasmic protease DegP. J Bacteriol 187:6622–6630. [PubMed][CrossRef]
76. Isaac DD, Pinkner JS, Hultgren SJ, Silhavy TJ. 2005. The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. Proc Natl Acad Sci USA 102:17775–17779. [PubMed][CrossRef]
77. Miot M, Betton JM. 2007. Optimization of the inefficient translation initiation region of the cpxP gene from Escherichia coli. Protein Sci 16:2445–2453. [PubMed][CrossRef]
78. Otto K, Silhavy TJ. 2002. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci USA 99:2287–2292. [PubMed][CrossRef]
79. De Wulf P, Kwon O, Lin EC. 1999. The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J Bacteriol 181:6772–6778.[PubMed]
80. DiGiuseppe PA, Silhavy TJ. 2003. Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol 185:2432–2440. [PubMed][CrossRef]
81. Miyadai H, Tanaka-Masuda K, Matsuyama S, Tokuda H. 2004. Effects of lipoprotein overproduction on the induction of DegP (HtrA) involved in quality control in the Escherichia coli periplasm. J Biol Chem 279:39807–39813. [PubMed][CrossRef]
82. Hirano Y, Hossain MM, Takeda K, Tokuda H, Miki K. 2007. Structural studies of the Cpx pathway activator NlpE on the outer membrane of Escherichia coli. Structure 15:963–976. [PubMed][CrossRef]
83. Jones CH, Danese PN, Pinkner JS, Silhavy TJ, Hultgren SJ. 1997. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J 16:6394–6406. [PubMed][CrossRef]
84. Lee YM, DiGiuseppe PA, Silhavy TJ, Hultgren SJ. 2004. P pilus assembly motif necessary for activation of the CpxRA pathway by PapE in Escherichia coli. J Bacteriol 186:4326–4337. [PubMed][CrossRef]
85. Sauer FG, Futterer K, Pinkner JS, Dodson KW, Hultgren SJ, Waksman G. 1999. Structural basis of chaperone function and pilus biogenesis. Science 285:1058–1061. [PubMed][CrossRef]
86. Yamamoto K, Ishihama A. 2005. Transcriptional response of Escherichia coli to external copper. Mol Microbiol 56:215–227. [PubMed][CrossRef]
87. Gupta SD, Lee BT, Camakaris J, Wu HC. 1995. Identification of cutC and cutF (nlpE) genes involved in copper tolerance in Escherichia coli. J Bacteriol 177:4207–4215.[PubMed]
88. Yamamoto K, Ishihama A. 2006. Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci Biotechnol Biochem 70:1688–1695. [PubMed][CrossRef]
89. Danese PN, Oliver GR, Barr K, Bowman GD, Rick PD, Silhavy TJ. 1998. Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J Bacteriol 180:5875–5884.[PubMed]
90. Langen GR, Harper JR, Silhavy TJ, Howard SP. 2001. Absence of the outer membrane phospholipase A suppresses the temperature-sensitive phenotype of Escherichia coli degP mutants and induces the Cpx and sigma(E) extracytoplasmic stress responses. J Bacteriol 183:5230–5238. [PubMed][CrossRef]
91. Mileykovskaya E, Dowhan W. 1997. The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine. J Bacteriol 179:1029–1034.[PubMed]
92. Dorel C, Vidal O, Prigent-Combaret C, Vallet I, Lejeune P. 1999. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol Lett 178:169–175. [PubMed][CrossRef]
93. De Wulf P, McGuire AM, Liu X, Lin EC. 2002. Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J Biol Chem 277:26652–26661. [PubMed][CrossRef]
94. Connolly L, De Las Penas A, Alba BM, Gross CA. 1997. The response to extracytoplasmic stress in Escherichia coli is controlled by partially overlapping pathways. Genes Dev 11:2012–2021. [PubMed][CrossRef]
95. Raffa RG, Raivio TL. 2002. A third envelope stress signal transduction pathway in Escherichia coli. Mol Microbiol 45:1599–1611. [PubMed][CrossRef]
96. Hirakawa H, Inazumi Y, Masaki T, Hirata T, Yamaguchi A. 2005. Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol Microbiol 55:1113–1126. [PubMed][CrossRef]
97. Batchelor E, Walthers D, Kenney LJ, Goulian M. 2005. The Escherichia coli CpxA-CpxR envelope stress response system regulates expression of the porins ompF and ompC. J Bacteriol 187:5723–5731. [PubMed][CrossRef]
98. Jubelin G, Vianney A, Beloin C, Ghigo JM, Lazzaroni JC, Lejeune P, Dorel C. 2005. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187:2038–2049. [PubMed][CrossRef]
99. Kershaw CJ, Brown NL, Constantinidou C, Patel MD, Hobman JL. 2005. The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151:1187–1198. [PubMed][CrossRef]
100. Cao J, Woodhall MR, Alvarez J, Cartron ML, Andrews SC. 2007. EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe(2+) transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol Microbiol 66:827. [PubMed][CrossRef]
101. De Wulf P, Akerley BJ, Lin EC. 2000. Presence of the Cpx system in bacteria. Microbiology 146(Pt 2):247–248.[PubMed]
102. Humphreys S, Rowley G, Stevenson A, Anjum MF, Woodward MJ, Gilbert S, Kormanec J, Roberts M. 2004. Role of the two-component regulator CpxAR in the virulence of Salmonella enterica serotype Typhimurium. Infect Immun 72:4654–4661. [PubMed][CrossRef]
103. Suntharalingam P, Spencer H, Gallant CV, Martin NL. 2003. Salmonella enterica serovar Typhimurium rdoA is growth phase regulated and involved in relaying Cpx-induced signals. J Bacteriol 185:432–443. [PubMed][CrossRef]
104. Hung DL, Raivio TL, Jones CH, Silhavy TJ, Hultgren SJ. 2001. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J 20:1508–1518. [PubMed][CrossRef]
105. Hernday AD, Braaten BA, Broitman-Maduro G, Engelberts P, Low DA. 2004. Regulation of the pap epigenetic switch by CpxAR: phosphorylated CpxR inhibits transition to the phase ON state by competition with Lrp. Mol Cell 16:537–547. [PubMed][CrossRef]
106. Nevesinjac AZ, Raivio TL. 2005. The Cpx envelope stress response affects expression of the type IV bundle-forming pili of enteropathogenic Escherichia coli. J Bacteriol 187:672–686. [PubMed][CrossRef]
107. Donnenberg MS, Zhang HZ, Stone KD. 1997. Biogenesis of the bundle-forming pilus of enteropathogenic Escherichia coli: reconstitution of fimbriae in recombinant E. coli and role of DsbA in pilin stability—a review. Gene 192:33–38. [PubMed][CrossRef]
108. MacRitchie DM, Ward JD, Nevesinjac AZ, Raivio TL. 2008. Activation of the Cpx envelope stress response down-regulates expression of several locus of enterocyte effacement-encoded genes in enteropathogenic Escherichia coli. Infect Immun 76:1465–1475. [PubMed][CrossRef]
109. Carlsson KE, Liu J, Edqvist PJ, Francis MS. 2007. Extracytoplasmic-stress-responsive pathways modulate type III secretion in Yersinia pseudotuberculosis. Infect Immun 75:3913–3924. [PubMed][CrossRef]
110. Carlsson KE, Liu J, Edqvist PJ, Francis MS. 2007. Influence of the Cpx extracytoplasmic-stress-responsive pathway on Yersinia sp.-eukaryotic cell contact. Infect Immun 75:4386–4399. [PubMed][CrossRef]
111. Nakayama S, Kushiro A, Asahara T, Tanaka R, Hu L, Kopecko DJ, Watanabe H. 2003. Activation of hilA expression at low pH requires the signal sensor CpxA, but not the cognate response regulator CpxR, in Salmonella enterica serovar Typhimurium. Microbiology 149:2809–2817. [PubMed][CrossRef]
112. Nagasawa S, Ishige K, Mizuno T. 1993. Novel members of the two-component signal transduction genes in Escherichia coli. J Biochem 114:350–357.[PubMed]
113. Hagenmaier S, Stierhof YD, Henning U. 1997. A new periplasmic protein of Escherichia coli which is synthesized in spheroplasts but not in intact cells. J Bacteriol 179:2073–2076.[PubMed]
114. Raivio TL, Laird MW, Joly JC, Silhavy TJ. 2000. Tethering of CpxP to the inner membrane prevents spheroplast induction of the Cpx envelope stress response. Mol Microbiol 37:1186–1197. [PubMed][CrossRef]
115. Baranova N, Nikaido H. 2002. The baeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J Bacteriol 184:4168–4176. [PubMed][CrossRef]
116. Nagakubo S, Nishino K, Hirata T, Yamaguchi A. 2002. The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. J Bacteriol 184:4161–4167. [PubMed][CrossRef]
117. Hirakawa H, Nishino K, Hirata T, Yamaguchi A. 2003. Comprehensive studies of drug resistance mediated by overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Bacteriol 185:1851–1856. [PubMed][CrossRef]
118. Hirakawa H, Nishino K, Yamada J, Hirata T, Yamaguchi A. 2003. Beta-lactam resistance modulated by the overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Antimicrob Chemother 52:576–582. [PubMed][CrossRef]
119. Hu WS, Li PC, Cheng CY. 2005. Correlation between ceftriaxone resistance of Salmonella enterica serovar Typhimurium and expression of outer membrane proteins OmpW and Ail/OmpX-like protein, which are regulated by BaeR of a two-component system. Antimicrob Agents Chemother 49:3955–3958. [PubMed][CrossRef]
120. Nishino K, Nikaido E, Yamaguchi A. 2007. Regulation of multidrug efflux systems involved in multidrug and metal resistance of Salmonella enterica serovar Typhimurium. J Bacteriol 189:9066–9075. [PubMed][CrossRef]
121. Pilsl H, Smajs D, Braun V. 1999. Characterization of colicin S4 and its receptor, OmpW, a minor protein of the Escherichia coli outer membrane. J Bacteriol 181:3578–3581.[PubMed]
122. Gil F, Ipinza F, Fuentes J, Fumeron R, Villarreal JM, Aspee A, Mora GC, Vasquez CC, Saavedra C. 2007. The ompW (porin) gene mediates methyl viologen (paraquat) efflux in Salmonella enterica serovar typhimurium. Res Microbiol 158:529–536. [PubMed][CrossRef]
123. Lee LJ, Barrett JA, Poole RK. 2005. Genome-wide transcriptional response of chemostat-cultured Escherichia coli to zinc. J Bacteriol 187:1124–1134. [PubMed][CrossRef]
124. Yamamoto K, Ogasawara H, Ishihama A. 2008. Involvement of multiple transcription factors for metal-induced spy gene expression in Escherichia coli. J Biotechnol 133:196–200. [PubMed][CrossRef]
125. Zhou L, Lei XH, Bochner BR, Wanner BL. 2003. Phenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems. J Bacteriol 185:4956–4972. [PubMed][CrossRef]
126. Zoetendal EG, Smith AH, Sundset MA, Mackie RI. 2008. The BaeSR two-component regulatory system mediates resistance to condensed tannins in Escherichia coli. Appl Environ Microbiol 74:535–539. [PubMed][CrossRef]
127. Nishino K, Honda T, Yamaguchi A. 2005. Genome-wide analyses of Escherichia coli gene expression responsive to the BaeSR two-component regulatory system. J Bacteriol 187:1763–1772. [PubMed][CrossRef]
128. Brissette JL, Russel M, Weiner L, Model P. 1990. Phage shock protein, a stress protein of Escherichia coli. Proc Natl Acad Sci USA 87:862–866. [PubMed][CrossRef]
129. Brissette JL, Russel M. 1990. Secretion and membrane integration of a filamentous phage-encoded morphogenetic protein. J Mol Biol 211:565–580. [PubMed][CrossRef]
130. Russel M, Kazmierczak B. 1993. Analysis of the structure and subcellular location of filamentous phage pIV. J Bacteriol 175:3998–4007.[PubMed]
131. Brissette JL, Weiner L, Ripmaster TL, Model P. 1991. Characterization and sequence of the Escherichia coli stress-induced psp operon. J Mol Biol 220:35–48. [PubMed][CrossRef]
132. Weiner L, Brissette JL, Model P. 1991. Stress-induced expression of the Escherichia coli phage shock protein operon is dependent on sigma 54 and modulated by positive and negative feedback mechanisms. Genes Dev 5:1912–1923. [PubMed][CrossRef]
133. Kleerebezem M, Crielaard W, Tommassen J. 1996. Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the proton motive force under stress conditions. EMBO J 15:162–171.[PubMed]
134. Adams H, Teertstra W, Demmers J, Boesten R, Tommassen J. 2003. Interactions between phage-shock proteins in Escherichia coli. J Bacteriol 185:1174–1180. [PubMed][CrossRef]
135. Adams H, Teertstra W, Koster M, Tommassen J. 2002. PspE (phage-shock protein E) of Escherichia coli is a rhodanese. FEBS Lett 518:173–176. [PubMed][CrossRef]
136. Rappas M, Bose D, Zhang X. 2007. Bacterial enhancer-binding proteins: unlocking sigma54-dependent gene transcription. Curr Opin Struct Biol 17:110–116. [PubMed][CrossRef]
137. Weiner L, Brissette JL, Ramani N, Model P. 1995. Analysis of the proteins and cis-acting elements regulating the stress-induced phage shock protein operon. Nucleic Acids Res 23:2030–2036. [PubMed][CrossRef]
138. Jovanovic G, Weiner L, Model P. 1996. Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. J Bacteriol 178:1936–1945.[PubMed]
139. Dworkin J, Jovanovic G, Model P. 2000. The PspA protein of Escherichia coli is a negative regulator of sigma(54)-dependent transcription. J Bacteriol 182:311–319. [PubMed][CrossRef]
140. Elderkin S, Jones S, Schumacher J, Studholme D, Buck M. 2002. Mechanism of action of the Escherichia coli phage shock protein PspA in repression of the AAA family transcription factor PspF. J Mol Biol 320:23–37. [PubMed][CrossRef]
141. Elderkin S, Bordes P, Jones S, Rappas M, Buck M. 2005. Molecular determinants for PspA-mediated repression of the AAA transcriptional activator PspF. J Bacteriol 187:3238–3248. [PubMed][CrossRef]
142. Kleerebezem M, Tommassen J. 1993. Expression of the pspA gene stimulates efficient protein export in Escherichia coli. Mol Microbiol 7:947–956. [PubMed][CrossRef]
143. Jones SE, Lloyd LJ, Tan KK, Buck M. 2003. Secretion defects that activate the phage shock response of Escherichia coli. J Bacteriol 185:6707–6711. [PubMed][CrossRef]
144. DeLisa MP, Lee P, Palmer T, Georgiou G. 2004. Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J Bacteriol 186:366–373. [PubMed][CrossRef]
145. Carlson JH, Silhavy TJ. 1993. Signal sequence processing is required for the assembly of LamB trimers in the outer membrane of Escherichia coli. J Bacteriol 175:3327–3334.[PubMed]
146. Maxson ME, Darwin AJ. 2004. Identification of inducers of the Yersinia enterocolitica phage shock protein system and comparison to the regulation of the RpoE and Cpx extracytoplasmic stress responses. J Bacteriol 186:4199–4208. [PubMed][CrossRef]
147. Robichon C, Bonhivers M, Pugsley AP. 2003. An intramolecular disulphide bond reduces the efficacy of a lipoprotein plasma membrane sorting signal. Mol Microbiol 49:1145–1154. [PubMed][CrossRef]
148. Weiner L, Model P. 1994. Role of an Escherichia coli stress-response operon in stationary-phase survival. Proc Natl Acad Sci USA 91:2191–2195. [PubMed][CrossRef]
149. Guilvout I, Chami M, Engel A, Pugsley AP, Bayan N. 2006. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J 25:5241–5249. [PubMed][CrossRef]
150. Becker LA, Bang IS, Crouch ML, Fang FC. 2005. Compensatory role of PspA, a member of the phage shock protein operon, in rpoE mutant Salmonella enterica serovar Typhimurium. Mol Microbiol 56:1004–1016. [PubMed][CrossRef]
151. Lloyd LJ, Jones SE, Jovanovic G, Gyaneshwar P, Rolfe MD, Thompson A, Hinton JC, Buck M. 2004. Identification of a new member of the phage shock protein response in Escherichia coli, the phage shock protein G (PspG). J Biol Chem 279:55707–55714. [PubMed][CrossRef]
152. Seo J, Savitzky DC, Ford E, Darwin AJ. 2007. Global analysis of tolerance to secretin-induced stress in Yersinia enterocolitica suggests that the phage-shock-protein system may be a remarkably self-contained stress response. Mol Microbiol 65:714–727. [PubMed][CrossRef]
153. Jovanovic G, Lloyd LJ, Stumpf MP, Mayhew AJ, Buck M. 2006. Induction and function of the phage shock protein extracytoplasmic stress response in Escherichia coli. J Biol Chem 281:21147–21161. [PubMed][CrossRef]
154. Whitfield C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75:39–68. [PubMed][CrossRef]
155. Gottesman S, Trisler P, Torres-Cabassa A. 1985. Regulation of capsular polysaccharide synthesis in Escherichia coli K-12: characterization of three regulatory genes. J Bacteriol 162:1111–1119.[PubMed]
156. Stout V, Gottesman S. 1990. RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli. J Bacteriol 172:659–669.[PubMed]
157. Stout V, Torres-Cabassa A, Maurizi MR, Gutnick D, Gottesman S. 1991. RcsA, an unstable positive regulator of capsular polysaccharide synthesis. J Bacteriol 173:1738–1747.[PubMed]
158. Trisler P, Gottesman S. 1984. lon transcriptional regulation of genes necessary for capsular polysaccharide synthesis in Escherichia coli K-12. J Bacteriol 160:184–191.[PubMed]
159. Torres-Cabassa AS, Gottesman S. 1987. Capsule synthesis in Escherichia coli K-12 is regulated by proteolysis. J Bacteriol 169:981–989.[PubMed]
160. Brill JA, Quinlan-Walshe C, Gottesman S. 1988. Fine-structure mapping and identification of two regulators of capsule synthesis in Escherichia coli K-12. J Bacteriol 170:2599–25611.[PubMed]
161. Sledjeski D, Gottesman S. 1995. A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc Natl Acad Sci USA 92:2003–2007. [PubMed][CrossRef]
162. Ebel W, Trempy JE. 1999. Escherichia coli RcsA, a positive activator of colanic acid capsular polysaccharide synthesis, functions to activate its own expression. J Bacteriol 181:577–584.[PubMed]
163. Takeda S, Fujisawa Y, Matsubara M, Aiba H, Mizuno T. 2001. A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC → YojN → RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol Microbiol 40:440–450. [PubMed][CrossRef]
164. Clarke DJ, Joyce SA, Toutain CM, Jacq A, Holland IB. 2002. Genetic analysis of the RcsC sensor kinase from Escherichia coli K-12. J Bacteriol 184:1204–1208. [PubMed][CrossRef]
165. Fredericks CE, Shibata S, Aizawa S, Reimann SA, Wolfe AJ. 2006. Acetyl phosphate-sensitive regulation of flagellar biogenesis and capsular biosynthesis depends on the Rcs phosphorelay. Mol Microbiol 61:734–747. [PubMed][CrossRef]
166. Gervais FG, Drapeau GR. 1992. Identification, cloning, and characterization of rcsF, a new regulator gene for exopolysaccharide synthesis that suppresses the division mutation ftsZ84 in Escherichia coli K-12. J Bacteriol 174:8016–8022.[PubMed]
167. Majdalani N, Heck M, Stout V, Gottesman S. 2005. Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli. J Bacteriol 187:6770–6778. [PubMed][CrossRef]
168. Castanie-Cornet MP, Cam K, Jacq A. 2006. RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli. J Bacteriol 188:4264–4270. [PubMed][CrossRef]
169. Hagiwara D, Sugiura M, Oshima T, Mori H, Aiba H, Yamashino T, Mizuno T. 2003. Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli. J Bacteriol 185:5735–5746. [PubMed][CrossRef]
170. Shiba Y, Matsumoto K, Hara H. 2006. DjlA negatively regulates the Rcs signal transduction system in Escherichia coli. Genes Genet Syst 81:51–56. [PubMed][CrossRef]
171. Kelm O, Kiecker C, Geider K, Bernhard F. 1997. Interaction of the regulator proteins RcsA and RcsB with the promoter of the operon for amylovoran biosynthesis in Erwinia amylovora. Mol Gen Genet 256:72–83. [PubMed][CrossRef]
172. Wehland M, Bernhard F. 2000. The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J Biol Chem 275:7013–7020. [PubMed][CrossRef]
173. Carballes F, Bertrand C, Bouche JP, Cam K. 1999. Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB. Mol Microbiol 34:442–450. [PubMed][CrossRef]
174. Davalos-Garcia M, Conter A, Toesca I, Gutierrez C, Cam K. 2001. Regulation of osmC gene expression by the two-component system rcsB-rcsC in Escherichia coli. J Bacteriol 183:5870–5876. [PubMed][CrossRef]
175. Sturny R, Cam K, Gutierrez C, Conter A. 2003. NhaR and RcsB independently regulate the osmCp1 promoter of Escherichia coli at overlapping regulatory sites. J Bacteriol 185:4298–4304. [PubMed][CrossRef]
176. Pristovsek P, Sengupta K, Lohr F, Schafer B, von Trebra MW, Ruterjans H, Bernhard F. 2003. Structural analysis of the DNA-binding domain of the Erwinia amylovora RcsB protein and its interaction with the RcsAB box. J Biol Chem 278:17752–17759. [PubMed][CrossRef]
177. Virlogeux I, Waxin H, Ecobichon C, Lee JO, Popoff MY. 1996. Characterization of the rcsA and rcsB genes from Salmonella typhi: rcsB through tviA is involved in regulation of Vi antigen synthesis. J Bacteriol 178:1691–1698.[PubMed]
178. Wacharotayankun R, Arakawa Y, Ohta M, Hasegawa T, Mori M, Horii T, Kato N. 1992. Involvement of rcsB in Klebsiella K2 capsule synthesis in Escherichia coli K-12. J Bacteriol 174:1063–1067.[PubMed]
179. Clavel T, Lazzaroni JC, Vianney A, Portalier R. 1996. Expression of the tolQRA genes of Escherichia coli K-12 is controlled by the RcsC sensor protein involved in capsule synthesis. Mol Microbiol 19:19–25. [PubMed][CrossRef]
180. Ebel W, Vaughn GJ, Peters HK III, Trempy JE. 1997. Inactivation of mdoH leads to increased expression of colanic acid capsular polysaccharide in Escherichia coli. J Bacteriol 179:6858–6861.[PubMed]
181. Mouslim C, Latifi T, Groisman EA. 2003. Signal-dependent requirement for the co-activator protein RcsA in transcription of the RcsB-regulated ugd gene. J Biol Chem 278:50588–50595. [PubMed][CrossRef]
182. Parker CT, Kloser AW, Schnaitman CA, Stein MA, Gottesman S, Gibson BW. 1992. Role of the rfaG and rfaP genes in determining the lipopolysaccharide core structure and cell surface properties of Escherichia coli K-12. J Bacteriol 174:2525–2538.[PubMed]
183. Chen MH, Takeda S, Yamada H, Ishii Y, Yamashino T, Mizuno T. 2001. Characterization of the RcsC→YojN→RcsB phosphorelay signaling pathway involved in capsular synthesis in Escherichia coli. Biosci Biotechnol Biochem 65:2364–2367. [PubMed][CrossRef]
184. Kelley WL, Georgopoulos C. 1997. Positive control of the two-component RcsC/B signal transduction network by DjlA: a member of the DnaJ family of molecular chaperones in Escherichia coli. Mol Microbiol 25:913–931. [PubMed][CrossRef]
185. Conter A, Sturny R, Gutierrez C, Cam K. 2002. The RcsCB His-Asp phosphorelay system is essential to overcome chlorpromazine-induced stress in Escherichia coli. J Bacteriol 184:2850–2853. [PubMed][CrossRef]
186. Ferrieres L, Clarke DJ. 2003. The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol Microbiol 50:1665–1682. [PubMed][CrossRef]
187. Sledjeski DD, Gottesman S. 1996. Osmotic shock induction of capsule synthesis in Escherichia coli K-12. J Bacteriol 178:1204–1206.[PubMed]
188. Laubacher ME, Ades SE. 2008. The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J Bacteriol 190:2065–2074. [PubMed][CrossRef]
189. Sailer FC, Meberg BM, Young KD. 2003. Beta-lactam induction of colanic acid gene expression in Escherichia coli. FEMS Microbiol Lett 226:245–249. [PubMed][CrossRef]
190. Ize B, Porcelli I, Lucchini S, Hinton JC, Berks BC, Palmer T. 2004. Novel phenotypes of Escherichia coli tat mutants revealed by global gene expression and phenotypic analysis. J Biol Chem 279:47543–47554. [PubMed][CrossRef]
191. Mouslim C, Groisman EA. 2003. Control of the Salmonella ugd gene by three two-component regulatory systems. Mol Microbiol 47:335–344. [PubMed][CrossRef]
192. Harold FM. 2007. Bacterial morphogenesis: learning how cells make cells. Curr Opin Microbiol 10:591–595. [PubMed][CrossRef]
193. Danese PN, Pratt LA, Kolter R. 2000. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182:3593–3596. [PubMed][CrossRef]
194. Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejeune P, Dorel C. 2000. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2:450–464. [PubMed][CrossRef]
195. Prigent-Combaret C, Vidal O, Dorel C, Lejeune P. 1999. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol 181:5993–6002.[PubMed]
196. Vianney A, Jubelin G, Renault S, Dorel C, Lejeune P, Lazzaroni JC. 2005. Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis. Microbiology 151:2487–2497. [PubMed][CrossRef]
197. Wang Q, Zhao Y, McClelland M, Harshey RM. 2007. The RcsCDB signaling system and swarming motility in Salmonella enterica serovar Typhimurium: dual regulation of flagellar and SPI-2 virulence genes. J Bacteriol 189:8447–8457. [PubMed][CrossRef]
198. Mouslim C, Delgado M, Groisman EA. 2004. Activation of the RcsC/YojN/RcsB phosphorelay system attenuates Salmonella virulence. Mol Microbiol 54:386–395. [PubMed][CrossRef]
199. Erickson KD, Detweiler CS. 2006. The Rcs phosphorelay system is specific to enteric pathogens/commensals and activates ydeI, a gene important for persistent Salmonella infection of mice. Mol Microbiol 62:883–894. [PubMed][CrossRef]
200. Peterson CN, Carabetta VJ, Chowdhury T, Silhavy TJ. 2006. LrhA regulates rpoS translation in response to the Rcs phosphorelay system in Escherichia coli. J Bacteriol 188:3175–3181. [PubMed][CrossRef]
201. Cano DA, Dominguez-Bernal G, Tierrez A, Garcia-Del Portillo F, Casadesus J. 2002. Regulation of capsule synthesis and cell motility in Salmonella enterica by the essential gene igaA. Genetics 162:1513–1523.[PubMed]
202. Dominguez-Bernal G, Pucciarelli MG, Ramos-Morales F, Garcia-Quintanilla M, Cano DA, Casadesus J, Garcia-del Portillo F. 2004. Repression of the RcsC-YojN-RcsB phosphorelay by the IgaA protein is a requisite for Salmonella virulence. Mol Microbiol 53:1437–1449. [PubMed][CrossRef]
203. McBroom AJ, Kuehn MJ. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol 63:545–558. [PubMed][CrossRef]
204. Kuehn MJ, Kesty NC. 2005. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19:2645–2655. [PubMed][CrossRef]
205. McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. 2006. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 188:5385–5392. [PubMed][CrossRef]
206. Nishino K, Yamaguchi A. 2001. Overexpression of the response regulator evgA of the two-component signal transduction system modulates multidrug resistance conferred by multidrug resistance transporters. J Bacteriol 183:1455–1458. [PubMed][CrossRef]
ecosalplus.5.4.7.citations
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/content/journal/ecosalplus/10.1128/ecosalplus.5.4.7
2009-07-29
2017-07-27

Abstract:

The gram-negative bacterial envelope is a complex extracytoplasmic compartment responsible for numerous cellular processes. Among its most important functions is its service as the protective layer separating the cytoplasmic space from the ever-changing external environment. To adapt to the diverse conditions encountered both in the environment and within the mammalian host, and species have evolved six independent envelope stress response systems . This review reviews the sE response, the CpxAR and BaeSR two-component systems (TCS) , the phage shock protein response, and the Rcs phosphorelay system. These five signal transduction pathways represent the most studied of the six known stress responses. The signal for adhesion to abiotic surfaces enters the pathway through the novel outer membrane lipoprotein NlpE, and activation on entry into the exponential phase of growth occurs independently of CpxA . Adhesion could disrupt NlpE causing unfolding of its unstable N-terminal domain, leading to activation of the Cpx response. The most recent class of genes added to the Cpx regulon includes those involved in copper homeostasis. Two separate microarray experiments revealed that exposure of cells to high levels of external copper leads to upregulation of several Cpx regulon members. The BaeSR TCS has also been shown to mediate drug resistance in . Similar to , the Bae pathway of mediates resistance to oxacillin, novobiocin, deoxycholate, β-lactams, and indole.

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Figures

Image of Figure 1
Figure 1

Under noninducing conditions (Left), RseB binds to the periplasmic domain of RseA and inhibits DegS- and RseP-directed cleavage of RseA. RseA sequesters σ, preventing contact between σ and RNA polymerase. Under inducing conditions (Right), outer membrane proteins become misfolded, exposing an otherwise hidden C-terminal domain. The PDZ domain of DegS recognizes this exposed region and binds the protein. This interaction stabilizes the active form of DegS, which then cleaves the periplasmic domain of RseA (Step 1). Release of the periplasmic domain relieves RseP inhibition allowing RseP to cleave the RseA transmembrane domain (Step 2). The cytoplasmic domain of RseA is released into the cytoplasm where it remains attached to σ. The final fragment of RseA is recognized by the SspB adaptor protein and delivered to ClpXP for degradation (Step 3). Free σ forms a complex with RNA polymerase, which directs the expression of the σ regulon (Step 4).

Citation: Macritchie D, Raivio T. 2009. Envelope Stress Responses, EcoSal Plus 2009; doi:10.1128/ecosalplus.5.4.7
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Figure 2

In the absence of an inducing signal (Left), the histidine sensor kinase CpxA functions as a phosphatase maintaining the response regulator CpxR in an unphosphorylated and inactive state. In the presence of activating signals (Right), which include overexpression of the outer membrane lipoprotein NlpE, misfolded P pilin subunits, and high concentrations of external copper, the inhibitor CpxP becomes degraded, possibly in association with misfolded protein. CpxA becomes autophosphorylated at a conserved histidine residue (H1). The phosphoryl group is subsequently transferred to a conserved aspartate residue (D1) on CpxR. CpxR~P serves as the transcriptional regulator of the Cpx regulon, upregulating the expression of protein folding and degrading factors in an effort to remove misfolded proteins from the envelope. Growth signals also induce the Cpx response, in a CpxA-independent manner.

Citation: Macritchie D, Raivio T. 2009. Envelope Stress Responses, EcoSal Plus 2009; doi:10.1128/ecosalplus.5.4.7
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Figure 3

Upon exposure to a toxic compound (e.g., indole), the BaeS sensor kinase becomes autophosphorylated at a conserved histidine residue (H1). The phosphoryl group is subsequently transferred to the cytoplasmic response regulator BaeR. BaeR~P upregulates expression of multidrug efflux genes that mediate the expulsion of toxic compounds from the cell.

Citation: Macritchie D, Raivio T. 2009. Envelope Stress Responses, EcoSal Plus 2009; doi:10.1128/ecosalplus.5.4.7
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Figure 4

Under normal conditions (Left), the negative regulator PspA binds to the activator protein PspF, preventing it from complexing with σ. Upon introduction of an inducing signal (Right), such as a decrease in membrane potential or expression of a secretin protein (pink ovals) in the absence of its pilot protein (black triangle), PspA is recruited to the inner membrane, where it interacts with PspB and PspC and facilitates relief of the impending stress. PspF is free to interact with σ and drive open complex formation and upregulation of the limited Psp regulon. The role of PspD and PspE in relieving envelope stress is not clear at this time. PspG is believed to be an effector of the Psp stress response.

Citation: Macritchie D, Raivio T. 2009. Envelope Stress Responses, EcoSal Plus 2009; doi:10.1128/ecosalplus.5.4.7
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Figure 5

In the absence of an activating signal (Left), RcsC functions as a phosphatase for the transcriptional activator RcsB. The other activator protein RcsA is subject to proteolysis by the ATP-dependent protease Lon. The pathway becomes activated by disruptions to the outer membrane and peptidoglycan layer. The signals enter the pathway through RcsC or the outer membrane lipoprotein RcsF, which somehow signals RcsC. RcsC becomes autophosphorylated at a conserved histidine residue (H1). The phosphoryl group is transferred to a conserved aspartate residue (D1) in its C-terminal end. The Hpt domain of the inner membrane protein RcsD (H2) mediates transfer of the phosphoryl group from RcsC to RcsB. RcsB~P serves as a transcriptional regulator either alone or in concert with RcsA to drive the expression of capsular polysaccharide synthesis and other genes.

Citation: Macritchie D, Raivio T. 2009. Envelope Stress Responses, EcoSal Plus 2009; doi:10.1128/ecosalplus.5.4.7
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