Chapter 8 : Envelope Stress

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This chapter focuses on envelope stress responses of gram-negative and gram-positive bacteria. To date, five major cell envelope stress responses have been identified in : the s, Cpx, Rcs, phage-shock protein (Psp), and Bae responses. Many of stress responses in gram-positive bacteria fall into two major categories: those that are activated by directly binding the antibiotic and those that are induced by a signal generated by antibiotic action. In general, responses in the first class have small regulon encoding genes that detoxify the antibiotic by pumping it out of the cell or modifying it. This review focuses on the second class because they can be clearly defined as envelope stress responses, sensing defects in the envelope and regulating genes that alter envelope physiology to enhance survival. Even though the LiaRS system is induced by many envelope stresses, liaRS mutants are not more susceptible to inducing stresses. σ of , one of the founding members of the extracytoplasmic function (ECF) σ factor family, is one of approximately 50 putative ECF σ factors in the bacterium. Cell envelope stress responses are widespread throughout the bacterial world, but have been investigated most intensively in , , and their close relatives. The regulatory interactions among the key players in the response; that is, the σ/anti-σ factor and sensor kinase/response regulator pairs are highly conserved.

Citation: Ades S, Hayden J, Laubacher M. 2011. Envelope Stress, p 115-131. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch8

Key Concept Ranking

Envelope Stress Response
Gene Expression and Regulation
Type III Secretion System
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Image of Figure 1.
Figure 1.

Overview of the gram-positive and gram-negative cell envelopes. For the gram-negative cell envelope, the phospholipid bilayer of the inner membrane (IM) and the asymmetric bilayer with phospholipids and LPS of the outer membrane (OM) are shown with associated integral and peripheral membrane proteins and lipoproteins. The periplasm lies between the two membranes and contains the thin layer of peptidoglycan (PG). For the gram-positive cell envelope, the cytoplasmic membrane (CM) with associated proteins is shown. A thick layer of peptidoglycan (PG) lies outside of the cytoplasmic membrane. Teichoic acids (TA) are covalently attached to the peptidoglycan and lipoteichoic acids (LTA) are covalently attached to the cytoplasmic membrane. A new peptidoglycan subunit is depicted as it is being flipped across the cytoplasmic membrane prior to insertion in the mature peptidoglycan layer.

Citation: Ades S, Hayden J, Laubacher M. 2011. Envelope Stress, p 115-131. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch8
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Image of Figure 2.
Figure 2.

Gram-negative envelope stress responses. The key regulators, accessory proteins, and physiological inducers of the five major envelope stress responses of are shown. The flow of phosphate through the Cpx, Rcs, and Bae phosphorelay systems is indicated (P). Protease activity is indicated by scissors.

Citation: Ades S, Hayden J, Laubacher M. 2011. Envelope Stress, p 115-131. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch8
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Image of Figure 3.
Figure 3.

Gram-positive envelope stress responses. The key regulators and accessory proteins of the major envelope stress responses are shown. The flow of phosphate through the LiaRS and CseBC phosphorelay systems is indicated (P). Protease activity is indicated by scissors. The mechanisms that release σ and σ from their respective anti-σ factors are not known.

Citation: Ades S, Hayden J, Laubacher M. 2011. Envelope Stress, p 115-131. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch8
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1. Adams, H.,, W. Teertstra,, J. Demmers,, R. Boesten, and, J. Tommassen. 2003. Interactions between phage-shock proteins in Escherichia coli. J. Bacteriol. 185:11741180.
2. Ahuja,, N., D. Korkin,, R. Chaba,, B. O. Cezairliyan,, R. T. Sauer,, K. K. Kim, and, C. A. Gross. 2009. Analyzing the interaction of RseA and RseB, the two negative regulators of the sigmaE envelope stress response, using a combined bioinformatic and experimental strategy. J. Biol. Chem. 284:54035413.
3. Arricau,, N., D. Hermant,, H. Waxin,, C. Ecobichon,, P. S. Duffey, and, M. Y. Popoff. 1998. The RcsB-RcsC regulatory system of Salmonella typhi differentially modulates the expression of invasion proteins, flagellin and Vi antigen in response to osmolarity. Mol. Microbiol. 29:835850.
4. Baranova, N., and, H. Nikaido. 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. 184:41684176.
5. Becker,, L. A.,, I. S. Bang,, M. L. Crouch, and, F. C. Fang. 2005. Compensatory role of PspA, a member of the phage shock protein operon, in rpoE mutant Salmonella enterica serovar Typhimurium. Mol. Microbiol. 56:10041016.
6. Belcheva, A., and, D. Golemi-Kotra. 2008. A close-up view of the VraSR two-component system. A mediator of Staphylococcus aureus response to cell wall damage. J. Biol. Chem. 283:1235412364.
7. Boulanger,, A., A. Francez-Charlot,, A. Conter,, M. P. Castanie-Cornet,, K. Cam, and, C. Gutierrez. 2005. Multistress regulation in Escherichia coli: expression of osmB involves two independent promoters responding either to sigmaS or to the RcsCDB His-Asp phosphorelay. J. Bacteriol. 187:32823286.
8. Brissette, J. L.,, M. Russel,, L. Weiner, and, P. Model. 1990. Phage shock protein, a stress protein of Escherichia coli. Proc. Natl. Acad. Sci. USA 87:862866.
9. Brutsche, S., and, V. Braun. 1997. SigX of Bacillus subtilis replaces the ECF sigma factor fecI of Escherichia coli and is inhibited by RsiX. Mol. Gen. Genet. 256:416425.
10. Bury-Mone,, S., Y. Nomane,, N. Reymond,, R. Barbet,, E. Jacquet,, S. Imbeaud,, A. Jacq, and, P. Bouloc. 2009. Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet. 5:e1000651.
11. Butcher, B. G., and, J. D. Helmann. 2006. Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by Bacilli. Mol. Microbiol. 60:765782.
12. Callewaert, L.,, K. G. Vanoirbeek,, I. Lurquin,, C. W. Michiels, and, A. Aertsen. 2009. The Rcs two-component system regulates expression of lysozyme inhibitors and is induced by exposure to lysozyme. J. Bacteriol. 191:19791981.
13. Campbell,, E. A.,, J. L. Tupy,, T. M. Gruber,, S. Wang,, M. M. Sharp,, C. A. Gross, and, S. A. Darst. 2003. Crystal structure of Escherichia coli sigmaE with the cytoplasmic domain of its anti-sigma RseA. Mol. Cell 11:10671078.
14. Cano,, D. A.,, G. Dominguez-Bernal,, A. Tierrez,, F. Garcia-Del Portillo, and, J. Casadesus. 2002. Regulation of capsule synthesis and cell motility in Salmonella enterica by the essential gene igaA. Genetics 162:15131523.
15. Cao, M., and, J. D. Helmann. 2002. Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function sigma factors. J. Bacteriol. 184:61236129.
16. Cao, M., and, J. D. Helmann. 2004. The Bacillus subtilis extracytoplasmic-function sigmaX factor regulates modification of the cell envelope and resistance to cationic antimicrobial peptides. J. Bacteriol. 186:11361146.
17. Cao,, M.,, P. A. Kobel,, M. M. Morshedi,, M. F. Wu,, C. Paddon, and, J. D. Helmann. 2002a. Defining the Bacillus subtilis sigma(W) regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J. Mol. Biol. 316:443457.
18. Cao,, M., T. Wang,, R. Ye, and, J. D. Helmann. 2002b. Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis sigma(W) and sigma(M) regulons. Mol. Microbiol. 45:12671276.
19. Carlsson, K. E.,, J. Liu,, P. J. Edqvist, and, M. S. Francis. 2007. Extracytoplasmic-stress-responsive pathways modulate type III secretion in Yersinia pseudotuberculosis. Infect. Immun. 75:39133924.
20. Castanie-Cornet, M. P.,, K. Cam, and, A. Jacq. 2006. RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli. J. Bacteriol. 188:42644270.
21. Cezairliyan, B. O., and, R. T. Sauer. 2007. Inhibition of regulated proteolysis by RseB. Proc. Natl. Acad. Sci. USA 104:37713776.
22. Chaba,, R.,, I. L. Grigorova,, J. M. Flynn,, T. A. Baker, and, C. A. Gross. 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. 21:124136.
23. Clarke, D. J.,, I. B. Holland, and, A. Jacq. 1997. Point mutations in the transmembrane domain of DjlA, a membrane-linked DnaJ-like protein, abolish its function in promoting colanic acid production via the Rcs signal transduction pathway. Mol. Microbiol. 25:933944.
24. Clavel, T.,, J. C. Lazzaroni,, A. Vianney, and, R. Portalier. 1996. Expression of the tolQRA genes of Escherichia coli K-12 is controlled by the RcsC sensor protein involved in capsule synthesis. Mol. Microbiol. 19:1925.
25. Collinet, B.,, H. Yuzawa,, T. Chen,, C. Herrera, and, D. Missiakas. 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. 275:3389833904.
26. Cosma,, C. L.,, P. N. Danese,, J. H. Carlson,, T. J. Silhavy, and, W. B. Snyder. 1995. Mutational activation of the Cpx signal transduction pathway of Escherichia coli suppresses the toxicity conferred by certain envelope-associated stresses. Mol. Microbiol. 18:491505.
27. Costanzo, A., and, S. E. Ades. 2006. Growth phase-dependent regulation of the extracytoplasmic stress factor, sigmaE, by guanosine 3',5'-bispyrophosphate (ppGpp). J. Bacteriol. 188:46274634.
28. Craig, J. E.,, A. Nobbs, and, N. J. High. 2002. The extracytoplasmic sigma factor, final sigma(E), is required for intracellular survival of nontypeable Haemophilus influenzae in J774 macrophages. Infect. Immun. 70:708715.
29. Crouch,, M. L.,, L. A. Becker,, I. S. Bang,, H. Tanabe,, A. J. Ouellette, and, F. C. Fang. 2005. The alternative sigma factor sigma is required for resistance of Salmonella enterica serovar Typhimurium to anti-microbial peptides. Mol. Microbiol. 56:789799.
30. Danese,, P. N.,, G. R. Oliver,, K. Barr,, G. D. Bowman,, P. D. Rick, and, T. J. Silhavy. 1998. Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J. Bacteriol. 180:58755884.
31. Danese, P. N.,, L. A. Pratt, and, R. Kolter. 2000. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol. 182:35933596.
32. Danese, P. N., and, T. J. Silhavy. 1998. CpxP, a stress-combative member of the Cpx regulon. J. Bacteriol. 180:831839.
33. Danese,, P. N.,, W. B. Snyder,, C. L. Cosma,, L. J. Davis, and, T. J. Silhavy. 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. 9:387398.
34. Dartigalongue,, C., D. Missiakas, and, S. Raina. 2001. Characterization of the Escherichia coli sigma E regulon. J. Biol. Chem. 276:2086620875.
35. Darwin, A. J. 2005. The phage-shock-protein response. Mol. Microbiol. 57:621628.
36. Darwin, A. J. 2007. Regulation of the phage-shock-protein stress response in Yersinia enterocolitica. Adv. Exp. Med. Biol. 603:167177.
37. Darwin, A. J., and, V. L. Miller. 2001. The psp locus of Yersinia enterocolitica is required for virulence and for growth in vitro when the Ysc type III secretion system is produced. Mol. Microbiol. 39:429444.
38. Davalos-Garcia, M.,, A. Conter,, I. Toesca,, C. Gutierrez, and, K. Cam. 2001. Regulation of osmC gene expression by the two-component system rcsB-rcsC in Escherichia coli. J. Bacteriol. 183:58705876.
39. Davis, B. M., and, M. K. Waldor. 2009. High-throughput sequencing reveals suppressors of Vibrio cholerae rpoE mutations: one fewer porin is enough. Nucleic Acids Res. 37:57575767.
40. De Las Penas, A., L. Connolly, and, C. A. Gross. 1997a. SigmaE is an essential sigma factor in Escherichia coli. J. Bacteriol. 179:68626864.
41. De Las Penas, A., L. Connolly, and, C. A. Gross. 1997b. The sigmaE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigmaE. Mol. Microbiol. 24:373385.
42. Detweiler,, C. S.,, D. M. Monack,, I. E. Brodsky,, H. Mathew, and, S. Falkow. 2003. virK, somA and rcsC are important for systemic Salmonella enterica serovar Typhimurium infection and cationic peptide resistance. Mol. Microbiol. 48:385400.
43. De Wulf, P., O. Kwon, and, E. C. Lin. 1999. The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J. Bacteriol. 181:67726778.
44. De Wulf,, P.,, A. M. McGuire,, X. Liu, and, E. C. Lin. 2002. Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P Escherichia coli in. J. Biol. Chem. 277:2665226661.
45. DiGiuseppe, P. A., and, T. J. Silhavy. 2003. Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185:24322440.
46. Dominguez-Bernal,, G.,, M. G. Pucciarelli,, F. Ramos-Morales,, M. Garcia-Quintanilla,, D. A. Cano,, J. Casadesus, and, F. Garcia-del Portillo. 2004. Repression of the RcsC-YojN-RcsB phosphorelay by the IgaA protein is a requisite for Salmonella virulence. Mol. Microbiol. 53:14371449.
47. Dorel,, C., P. Lejeune, and, A. Rodrigue. 2006. The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Res. Microbiol. 157:306314.
48. Dorel, C.,, O. Vidal,, C. Prigent-Combaret,, I. Vallet, and, P. Lejeune. 1999. Involvement of the Cpx signal transduction pathway of E. Coli in biofilm formation. FEMS Microbiol. Lett. 178:169175.
49. Dworkin,, J., G. Jovanovic, and, P. Model. 2000. The PspA protein of Escherichia coli is a negative regulator of sigma(54)-dependent transcription. J. Bacteriol. 182:311319.
50. Ebel,, W.,, G. J. Vaughn,, H. K. Peters, 3rd, and, J. E. Trempy. 1997. Inactivation of mdoH leads to increased expression of colanic acid capsular polysaccharide in Escherichia coli. J. Bacteriol. 179:68586861.
51. Eiamphungporn, W., and, J. D. Helmann. 2008. The Bacillus subtilis sigma(M) regulon and its contribution to cell envelope stress responses. Mol. Microbiol. 67:830848.
52. Elderkin, S.,, P. Bordes,, S. Jones,, M. Rappas, and, M. Buck. 2005. Molecular determinants for PspA-mediated repression of the AAA transcriptional activator PspF. J. Bacteriol. 187:32383248.
53. Ellermeier, C. D., and, R. Losick. 2006. Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis. Genes Dev. 20:19111922.
54. Erickson, J. W., and, C. A. Gross. 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. 3:14621471.
55. Erickson, K. D., and, C. S. Detweiler. 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. 62:883894.
56. Ferrieres, L., and, D. J. Clarke. 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. 50:16651682.
57. Ferrieres, L., A. Thompson, and, D. J. Clarke. 2009. Elevated levels of {sigma}S inhibit biofilm formation in Escherichia coli: a role for the Rcs phosphorelay. Microbiology. 155:35443553.
58. Flannagan, R. S., and, M. A. Valvano. 2008. Burkholderia cenocepacia requires RpoE for growth under stress conditions and delay of phagolysosomal fusion in macrophages. Microbiology 154:643653.
59. Fleischer, R.,, R. Heermann,, K. Jung, and, S. Hunke. 2007. Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli. J. Biol. Chem. 282:85838593.
60. Francez-Charlot,, A., B. Laugel,, A. Van Gemert,, N. Dubarry,, F. Wiorowski,, M. P. Castanie-Cornet,, C. Gutierrez, and, K. Cam. 2003. RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol. Microbiol. 49:823832.
61. Genevaux,, P., A. Wawrzynow,, M. Zylicz,, C. Georgopoulos, and, W. L. Kelley. 2001. DjlA is a third DnaK co-chaperone of Escherichia coli, and DjlA-mediated induction of colanic acid capsule requires DjlA-DnaK interaction. J. Biol. Chem. 276:79067912.
62. Genin, S., and, C. A. Boucher. 1994. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol. Gen. Genet. 243:112118.
63. Gottesman,, S., P. Trisler, and, A. Torres-Cabassa. 1985. Regulation of capsular polysaccharide synthesis in Escherichia coli K-12: characterization of three regulatory genes. J. Bacteriol. 162:11111119.
64. Green, R. C., and, A. J. Darwin. 2004. PspG, a new member of the Yersinia enterocolitica phage shock protein regulon. J. Bacteriol. 186:49104920.
65. Grigorova,, I. L.,, R. Chaba,, H. J. Zhong,, B. M. Alba,, V. Rhodius,, C. Herman, and, C. A. Gross. 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. 18:26862697.
66. Guilvout, I.,, M. Chami,, A. Engel,, A. P. Pugsley, and, N. Bayan. 2006. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J. 25:52415249.
67. Hagiwara,, D., M. Sugiura,, T. Oshima,, H. Mori,, H. Aiba,, T. Yamashino, and, T. Mizuno. 2003. Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phospho-relay system in Escherichia coli. J. Bacteriol. 185:57355746.
68. Hardie, K. R.,, S. Lory, and, A. P. Pugsley. 1996. Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 15:978988.
69. Hayden, J. D., and, S. E. Ades. 2008. The extracytoplasmic stress factor, sigmaE, is required to maintain cell envelope integrity in Escherichia coli. PLoS One 3:e1573.
70. Heusipp,, G.,, M. A. Schmidt, and, V. L. Miller. 2003. Identification of rpoE and nadB as host responsive elements of Yersinia enterocolitica. FEMS Microbiol. Lett. 226:291298.
71. Hinchliffe,, S. J.,, S. L. Howard,, Y. H. Huang,, D. J. Clarke, and, B. W. Wren. 2008. The importance of the Rcs phosphorelay in the survival and pathogenesis of the enteropathogenic yersiniae. Microbiology 154:11171131.
72. Hirakawa, H.,, Y. Inazumi,, T. Masaki,, T. Hirata, and, A. Yamaguchi. 2005. Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol. Microbiol. 55:11131126.
73. Hirano, Y.,, M. M. Hossain,, K. Takeda,, H. Tokuda, and, K. Miki. 2007. Structural studies of the Cpx pathway activator NlpE on the outer membrane of Escherichia coli. Structure 15:963976.
74. Hong, H. J.,, M. S. Paget, and, M. J. Buttner. 2002. A signal transduction system in Streptomyces coelicolor that activates the expression of a putative cell wall glycan operon in response to vancomycin and other cell wall-specific antibiotics. Mol. Microbiol. 44:11991211.
75. Horsburgh, M. J., and, A. Moir. 1999. Sigma M, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Mol. Microbiol. 32:4150.
76. Humphreys,, S., G. Rowley,, A. Stevenson,, M. F. Anjum,, M. J. Woodward,, S. Gilbert,, J. Kormanec, and, M. Roberts. 2004. Role of the two-component regulator CpxAR in the virulence of Salmonella enterica serotype Typhimurium. Infect. Immun. 72:46544661.
77. Hung,, D. L.,, T. L. Raivio,, C. H. Jones,, T. J. Silhavy, and, S. J. Hultgren. 2001. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J. 20:15081518.
78. Hunke, S., and, J. M. Betton. 2003. Temperature effect on inclusion body formation and stress response in the periplasm of Escherichia coli. Mol. Microbiol. 50:15791589.
79. Hutchings,, M. I.,, H. J. Hong,, E. Leibovitz,, I. C. Sutcliffe, and, M. J. Buttner. 2006. The sigma(E) cell envelope stress response of Streptomyces coelicolor is influenced by a novel lipoprotein, CseA. J. Bacteriol. 188:72227229.
80. Hyyrylainen, H. L.,, M. Sarvas, and, V. P. Kontinen. 2005. Transcriptome analysis of the secretion stress response of Bacillus subtilis. Appl. Microbiol. Biotechnol. 67:389396.
81. Ionescu, M., and, S. Belkin. 2009. Overproduction of exopolysaccharides by an Escherichia coli K-12 rpoS mutant in response to osmotic stress. Appl. Environ. Microbiol. 75:483492.
82. Ize,, B., I. Porcelli,, S. Lucchini,, J. C. Hinton,, B. C. Berks, and, T. Palmer. 2004. Novel phenotypes of Escherichia coli tat mutants revealed by global gene expression and phenotypic analysis. J. Biol. Chem. 279:4754347554.
83. Jervis,, A. J.,, P. D. Thackray,, C. W. Houston,, M. J. Horsburgh, and, A. Moir. 2007. SigM-responsive genes of Bacillus subtilis and their promoters. J. Bacteriol. 189:45344538.
84. Johansen, J.,, A. A. Rasmussen,, M. Overgaard, and, P. Valentin-Hansen. 2006. Conserved small non-coding RNAs that belong to the sigmaE regulon: role in down-regulation of outer membrane proteins. J. Mol. Biol. 364:18.
85. Jones,, C. H.,, P. N. Danese,, J. S. Pinkner,, T. J. Silhavy, and, S. J. Hultgren. 1997. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J. 16:63946406.
86. Jordan, S.,, M. I. Hutchings, and, T. Mascher. 2008. Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol. Rev. 32:107146.
87. Jordan,, S., A. Junker,, J. D. Helmann, and, T. Mascher. 2006. Regulation of LiaRS-dependent gene expression in Bacillus subtilis: identification of inhibitor proteins, regulator binding sites, and target genes of a conserved cell envelope stress-sensing two-component system. J. Bacteriol. 188:51535166.
88. Jordan,, S., E. Rietkotter,, M. A. Strauch,, F. Kalamorz,, B. G. Butcher,, J. D. Helmann, and, T. Mascher. 2007. LiaRS-dependent gene expression is embedded in transition state regulation in Bacillus subtilis. Microbiology 153:25302540.
89. Kabir,, M. S.,, D. Yamashita,, S. Koyama,, T. Oshima,, K. Kurokawa,, M. Maeda,, R. Tsunedomi,, M. Murata,, C. Wada,, H. Mori, and, M. Yamada. 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 151:27212735.
90. Kaldalu,, N., R. Mei, and, K. Lewis. 2004. Killing by ampicillin and ofloxacin induces overlapping changes in Escherichia coli transcription profile. Antimicrob. Agents Chemother. 48:890896.
91. Kleerebezem,, M., W. Crielaard, and, J. Tommassen. 1996. Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J. 15:162171.
92. Klein, G.,, B. Lindner,, W. Brabetz,, H. Brade, and, S. Raina. 2009. Escherichia coli K-12 suppressor-free mutants lacking early glycosyltransferases and late acyltransferases: minimal lipopolysaccharide structure and induction of envelope stress response. J. Biol. Chem. 284:1536915389.
93. Kobayashi,, R., T. Suzuki, and, M. Yoshida. 2007. Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol. Microbiol. 66:100109.
94. Kovacikova, G., and, K. Skorupski. 2002. The alternative sigma factor sigma(E) plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect. Immun. 70:53555362.
95. Kuroda,, M., H. Kuroda,, T. Oshima,, F. Takeuchi,, H. Mori, and, K. Hiramatsu. 2003. Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol. Microbiol. 49:807821.
96. Laubacher, M. E., and, S. E. Ades. 2008. The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J. Bacteriol. 190:20652074.
97. Lee,, Y. M.,, P. A. DiGiuseppe,, T. J. Silhavy, and, S. J. Hultgren. 2004. P pilus assembly motif necessary for activation of the CpxRA pathway by PapE in Escherichia coli. J. Bacteriol. 186:43264337.
98. Lloyd,, L. J.,, S. E. Jones,, G. Jovanovic,, P. Gyaneshwar,, M. D. Rolfe,, A. Thompson,, J. C. Hinton, and, M. Buck. 2004. Identification of a new member of the phage shock protein response in Escherichia coli, the phage shock protein G (PspG). J. Biol. Chem. 279:5570755714.
99. Lonetto,, M. A.,, K. L. Brown,, K. E. Rudd, and, M. J. Buttner. 1994. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc. Natl. Acad. Sci. USA 91:75737577.
100. Macritchie,, D. M.,, J. D. Ward,, A. Z. Nevesinjac, and, T. L. Raivio. 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. 76:14651475.
101. Majdalani, N., and, S. Gottesman. 2005. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59:379405.
102. Majdalani, N.,, M. Heck,, V. Stout, and, S. Gottesman. 2005. Role of RcsF in signaling to the Rcs phosphorelay pathway in Escherichia coli. J. Bacteriol. 187:67706778.
103. Majdalani,, N., D. Hernandez, and, S. Gottesman. 2002. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol. Microbiol. 46:813826.
104. Mariscotti, J. F., and, F. Garcia-Del Portillo. 2008. Instability of the Salmonella RcsCDB signalling system in the absence of the attenuator IgaA. Microbiology 154:13721383.
105. Mariscotti, J. F., and, F. Garcia-del Portillo. 2009. Genome expression analyses revealing the modulation of the Salmonella Rcs regulon by the attenuator IgaA. J. Bacteriol. 191:18551867.
106. Martin, D. W.,, B. W. Holloway, and, V. Deretic. 1993. Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor. J. Bacteriol. 175:11531164.
107. Martinez,, B.,, A. L. Zomer,, A. Rodriguez,, J. Kok, and, O. P. Kuipers. 2007. Cell envelope stress induced by the bacteriocin Lcn972 is sensed by the Lactococcal two-component system CesSR. Mol. Microbiol. 64:473486.
108. Mascher,, T.,, A. B. Hachmann, and, J. D. Helmann. 2007. Regulatory overlap and functional redundancy among Bacillus subtilis extracytoplasmic function sigma factors. J. Bacteriol. 189:69196927.
109. Mascher,, T.,, N. G. Margulis,, T. Wang,, R. W. Ye, and, J. D. Helmann. 2003. Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol. Microbiol. 50:15911604.
110. Mascher,, T.,, S. L. Zimmer,, T. A. Smith, and, J. D. Helmann. 2004. Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. Antimicrob. Agents Chemother. 48:28882896.
111. Mathur,, J.,, B. M. Davis, and, M. K. Waldor. 2007. Antimicrobial peptides activate the Vibrio cholerae sigmaE regulon through an OmpU-dependent signalling pathway. Mol. Microbiol. 63:848858.
112. Maxson, M. E., and, A. J. Darwin. 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. 186:41994208.
113. Maxson, M. E., and, A. J. Darwin. 2006a. Multiple promoters control expression of the Yersinia enterocolitica phage-shock-protein A (pspA) operon. Microbiology 152:10011010.
114. Maxson, M. E., and, A. J. Darwin. 2006b. PspB and PspC of Yersinia enterocolitica are dual function proteins: regulators and effectors of the phage-shock-protein response. Mol. Microbiol. 59:16101623.
115. McBroom, A. J., and, M. J. Kuehn. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 63:545558.
116. Mecsas,, J.,, P. E. Rouviere,, J. W. Erickson,, T. J. Donohue, and, C. A. Gross. 1993. The activity of sigma E, an Escherichia coli heatinducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev. 7:26182628.
117. Mileykovskaya, E., and, W. Dowhan. 1997. The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine. J. Bacteriol. 179:10291034.
118. Missiakas, D.,, J. M. Betton, and, S. Raina. 1996. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol. Microbiol. 21:871884.
119. Missiakas, D.,, M. P. Mayer,, M. Lemaire,, C. Georgopoulos, and, S. Raina. 1997. Modulation of the Escherichia coli sigmaE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol. Microbiol. 24:355371.
120. Mitobe,, J., E. Arakawa, and, H. Watanabe. 2005. A sensor of the two-component system CpxA affects expression of the type III secretion system through posttranscriptional processing of InvE. J. Bacteriol. 187:107113.
121. Nakayama, S., and, H. Watanabe. 1998. Identification of cpxR as a positive regulator essential for expression of the Shigella sonnei virF gene. J. Bacteriol. 180:35223528.
122. Nassif,, X., N. Honore,, T. Vasselon,, S. T. Cole, and, P. J. Sansonetti. 1989. Positive control of colanic acid synthesis in Escherichia coli by rmpA and rmpB, two virulence-plasmid genes of Klebsiella pneumoniae. Mol. Microbiol. 3:13491359.
123. Nevesinjac, A. Z., and, T. L. Raivio. 2005. The Cpx envelope stress response affects expression of the type IV bundle-forming pili of enteropathogenic Escherichia coli. J. Bacteriol. 187:672686.
124. Nishino,, K., E. Nikaido, and, A. Yamaguchi. 2007. Regulation of multidrug efflux systems involved in multidrug and metal resistance of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189:90669075.
125. Ophir, T., and, D. L. Gutnick. 1994. A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl. Environ. Microbiol. 60:740745.
126. Otto, K., and, T. J. Silhavy. 2002. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl. Acad. Sci. USA 99:22872292.
127. Paget,, M. S.,, L. Chamberlin,, A. Atrih,, S. J. Foster, and, M. J. Buttner. 1999a. Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J. Bacteriol. 181:204211.
128. Paget, M. S.,, E. Leibovitz, and, M. J. Buttner. 1999b. A putative two-component signal transduction system regulates sigmaE, a sigma factor required for normal cell wall integrity in Streptomyces coelicolor A3(2). Mol. Microbiol. 33:97107.
129. Papenfort,, K., V. Pfeiffer,, F. Mika,, S. Lucchini,, J. C. Hinton, and, J. Vogel. 2006. SigmaE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol. Microbiol. 62:16741688.
130. Parker,, C. T.,, A. W. Kloser,, C. A. Schnaitman,, M. A. Stein,, S. Gottesman, and, B. W. Gibson. 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. 174:25252538.
131. Peschel, A. 2002. How do bacteria resist human antimicrobial peptides? Trends Microbiol. 10:179186.
132. Petersohn,, A., M. Brigulla,, S. Haas,, J. D. Hoheisel,, U. Volker, and, M. Hecker. 2001. Global analysis of the general stress response of Bacillus subtilis. J. Bacteriol. 183:56175631.
133. Pietiainen,, M., M. Gardemeister,, M. Mecklin,, S. Leskela,, M. Sarvas, and, V. P. Kontinen. 2005. Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems. Microbiology 151:15771592.
134. Potrykus, J., and, G. Wegrzyn. 2004. The ypdI gene codes for a putative lipoprotein involved in the synthesis of colanic acid in Escherichia coli. FEMS Microbiol. Lett. 235:265271.
135. Price, N. L., and, T. L. Raivio. 2009. Characterization of the Cpx regulon in Escherichia coli strain MC4100. J. Bacteriol. 191:17981815.
136. Raffa, R. G., and, T. L. Raivio. 2002. A third envelope stress signal transduction pathway in Escherichia coli. Mol. Microbiol. 45:15991611.
137. Raivio,, T. L.,, M. W. Laird,, J. C. Joly, and, T. J. Silhavy. 2000. Tethering of CpxP to the inner membrane prevents spheroplast induction of the cpx envelope stress response. Mol. Microbiol. 37:11861197.
138. Raivio, T. L.,, D. L. Popkin, and, T. J. Silhavy. 1999. The Cpx envelope stress response is controlled by amplification and feedback inhibition. J. Bacteriol. 181:52635272.
139. Raivio, T. L., and, T. J. Silhavy. 1997. Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J. Bacteriol. 179:77247733.
140. Rezuchova, B.,, H. Miticka,, D. Homerova,, M. Roberts, and, J. Kormanec. 2003. New members of the Escherichia coli sigmaE regulon identified by a two-plasmid system. FEMS Microbiol. Lett. 225:17.
141. Rhodius,, V. A.,, W. C. Suh,, G. Nonaka,, J. West, and, C. A. Gross. 2006. Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol. 4:e2.
142. Rouviere,, P. E.,, A. De Las Penas,, J. Mecsas,, C. Z. Lu,, K. E. Rudd, and, C. A. Gross. 1995. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli. EMBO J. 14:10321042.
143. Ruiz, N., D. Kahne, and, T. J. Silhavy. 2006. Advances in understanding bacterial outer-membrane biogenesis. Nat. Rev. Microbiol. 4:5766.
144. Ruiz, N., D. Kahne, and, T. J. Silhavy. 2009. Transport of lipopolysaccharide across the cell envelope: the long road of discovery. Nat. Rev. Microbiol. 7:677683.
145. Ruiz, N., and, T. J. Silhavy. 2005. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol. 8:122126.
146. Sailer, F. C.,, B. M. Meberg, and, K. D. Young. 2003. beta-Lactam induction of colanic acid gene expression in Escherichia coli. FEMS Microbiol. Lett. 226:245249.
147. Sambucetti, L., L. Eoyang, and, P. M. Silverman. 1982. Cellular control of conjugation in Escherichia coli K12. Effect of chromosomal cpx mutations on F-plasmid gene expression. J. Mol. Biol. 161:1331.
148. Schobel, S.,, S. Zellmeier,, W. Schumann, and, T. Wiegert. 2004. The Bacillus subtilis sigmaW anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC. Mol. Microbiol. 52:10911105.
149. Seo,, J.,, D. C. Savitzky,, E. Ford, and, A. J. Darwin. 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. 65:714727.
150. Shiba,, Y., K. Matsumoto, and, H. Hara. 2006. DjlA negatively regulates the Rcs signal transduction system in Escherichia coli. Genes Genet. Syst. 81:5156.
151. Shiba,, Y., Y. Yokoyama,, Y. Aono,, T. Kiuchi,, J. Kusaka,, K. Matsumoto, and, H. Hara. 2004. Activation of the Rcs signal transduction system is responsible for the thermosensitive growth defect of an Escherichia coli mutant lacking phosphatidylglycerol and cardiolipin. J. Bacteriol. 186:65266535.
152. Slamti, L., and, M. K. Waldor. 2009. Genetic analysis of activation of the Vibrio cholerae Cpx pathway. J. Bacteriol. 191:50445056.
153. Sledjeski, D. D., and, S. Gottesman. 1996. Osmotic shock induction of capsule synthesis in Escherichia coli K-12. J. Bacteriol. 178:12041206.
154. Snyder,, W. B.,, L. J. Davis,, P. N. Danese,, C. L. Cosma, and, T. J. Silhavy. 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. 177:42164223.
155. Sohn,, J.,, R. A. Grant, and, R. T. Sauer. 2007. Allosteric activation of DegS, a stress sensor PDZ protease. Cell 131:572583.
156. Sohn, J., and, R. T. Sauer. 2009. OMP peptides modulate the activity of DegS protease by differential binding to active and inactive conformations. Mol. Cell 33:6474.
157. Staron,, A.,, H. J. Sofia,, S. Dietrich,, L. E. Ulrich,, H. Liesegang, and, T. Mascher. 2009. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol. Microbiol. 74:557581.
158. Stone, K. J., and, J. L. Strominger. 1971. Mechanism of action of bacitracin: complexation with metal ion and C 55 -isoprenyl pyrophosphate. Proc. Natl. Acad. Sci. USA 68:32233227.
159. Storm, D. R., and, J. L. Strominger. 1973. Complex formation between bacitracin peptides and isoprenyl pyrophosphates. The specificity of lipid-peptide interactions. J. Biol. Chem. 248:39403945.
160. Stout, V., and, S. Gottesman. 1990. RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli. J. Bacteriol. 172:659669.
161. Suntharalingam,, P.,, M. D. Senadheera,, R. W. Mair,, C. M. Levesque, and, D. G. Cvitkovitch. 2009. The LiaFSR system regulates the cell envelope stress response in Streptococcus mutans. J. Bacteriol. 191:29732984.
162. Takeda, S.,, Y. Fujisawa,, M. Matsubara,, H. Aiba, and, T. Mizuno. 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. 40:440450.
163. Tam le,, T., C. Eymann,, D. Albrecht,, R. Sietmann,, F. Schauer,, M. Hecker, and, H. Antelmann. 2006. Differential gene expression in response to phenol and catechol reveals different metabolic activities for the degradation of aromatic compounds in Bacillus subtilis. Environ. Microbiol. 8:14081427.
164. Testerman,, T. L.,, A. Vazquez-Torres,, Y. Xu,, J. Jones-Carson,, S. J. Libby, and, F. C. Fang. 2002. The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol. Microbiol. 43:771782.
165. Thackray, P. D., and, A. Moir. 2003. SigM, an extracytoplasmic function sigma factor of Bacillus subtilis, is activated in response to cell wall antibiotics, ethanol, heat, acid, and super-oxide stress. J. Bacteriol. 185:34913498.
166. Thompson, K. M.,, V. A. Rhodius, and, S. Gottesman. 2007. SigmaE regulates and is regulated by a small RNA in Escherichia coli. J. Bacteriol. 189:42434256.
167. Tierrez, A., and, F. Garcia-del Portillo. 2004. The Salmonella membrane protein IgaA modulates the activity of the RcsC-YojNRcsB and PhoP-PhoQ regulons. J. Bacteriol. 186:74817489.
168. Turner, M. S., and, J. D. Helmann. 2000. Mutations in multidrug efflux homologs, sugar isomerases, and antimicrobial biosynthesis genes differentially elevate activity of the sigma(X) and sigma(W) factors in Bacillus subtilis. J. Bacteriol. 182:52025210.
169. van Stelten,, J., F. Silva,, D. Belin, and, T. J. Silhavy. 2009. Effects of antibiotics and a proto-oncogene homolog on destruction of protein translocator SecY. Science 325:753756.
170. Virlogeux,, I., H. Waxin,, C. Ecobichon,, J. O. Lee, and, M. Y. Popoff. 1996. Characterization of the rcsA and rcsB genes from Salmonella typhi: rcsB through tviA is involved in regulation of Vi antigen synthesis. J. Bacteriol. 178:16911698.
171. Walsh,, N. P.,, B. M. Alba,, B. Bose,, C. A. Gross, and, R. T. Sauer. 2003. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113:6171.
172. Wang,, Q., Y. Zhao,, M. McClelland, and, R. M. Harshey. 2007. The RcsCDB signaling system and swarming motility in Salmonella enterica serovar Typhimurium: dual regulation of flagellar and SPI-2 virulence genes. J. Bacteriol. 189:84478457.
173. Weber, R. F., and, P. M. Silverman. 1988. The cpx proteins of Escherichia coli K12. Structure of the cpxA polypeptide as an inner membrane component. J. Mol. Biol. 203:467478.
174. Wehland, M., and, F. Bernhard. 2000. The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J. Biol. Chem. 275:70137020.
175. Weiner, L., and, P. Model. 1994. Role of an Escherichia coli stressresponse operon in stationary-phase survival. Proc. Natl. Acad. Sci. USA 91:21912195.
176. Wiegert, T.,, G. Homuth,, S. Versteeg, and, W. Schumann. 2001. Alkaline shock induces the Bacillus subtilis sigma(W) regulon. Mol. Microbiol. 41:5971.
177. Wollmann, P., and, K. Zeth. 2007. The structure of RseB: a sensor in periplasmic stress response of E. coli. J. Mol. Biol. 372:927941.
178. Yen,, M. R.,, C. R. Peabody,, S. M. Partovi,, Y. Zhai,, Y. H. Tseng, and, M. H. Saier. 2002. Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim. Biophys. Acta 1562:631.
179. Zellmeier,, S., W. Schumann, and, T. Wiegert. 2006. Involvement of Clp protease activity in modulating the Bacillus subtilis σW stress response. Mol. Microbiol. 61:15691582.

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