Envelope stress responses and Gram-negative bacterial pathogenesis

Molecular Microbiology

Volumn 56, Issue 5, 2005, Pages 1119-1128

  Raivio, Tracy L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DSBA PROTEIN; MEMBRANE PROTEIN; PROTEASE DEGP; PROTEIN BAE; PROTEIN CPX; PROTEINASE; SIGMA FACTOR; SIGMA FACTOR E; UNCLASSIFIED DRUG;

BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; CATALYSIS; CATALYST; DISULFIDE BOND; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; GRAM NEGATIVE INFECTION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; SECRETION; SHORT SURVEY; STRESS; SURVIVAL;

ANIMALS; BACTERIAL PROTEINS; CELL MEMBRANE; CELL WALL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-NEGATIVE BACTERIA; HUMANS; PROTEIN KINASES; SIGMA FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VIRULENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 19944402536     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04625.x     Document Type: Short Survey

References (90)

1. E in Escherichia coli. Curr Opin Microbiol 7: 157-162.
2. E-dependent envelope stress response. Mol Microbiol 52: 613-619.
3. E-dependent extracytoplasmic stress response. Genes Dev 16: 2156-2168.
4. Baranova, N., and Nikaido, H. (2002) The BaeSR two-component regulatory system activates transcription of the yeg-MNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J Bacteriol 184: 4168-4176.
5. Baumler, A.J., Kusters, J.G., Stojiljkovic, I., and Heffron, F. (1994) Salmonella typhimurium loci involved in survival within macrophages. Infect Immun 62: 1623-1630.
6. Bouwman, C.W., Kohli, M., Killoran, A., Touchie, G.A., Kadner, R.J., and Martin, N.L. (2003) Characterization of SrgA, a Salmonella enterica serovar Typhimurium virulence plasmid-encoded paralogue of the disulfide oxidoreductase DsbA, essential for biogenesis of plasmid-encoded fimbriae. J Bacteriol 185: 991-1000.
7. Braun, P., Ockhuijsen, C., Eppens, E., Koster, M., Bitter, W., and Tommassen, J. (2001) Maturation of Pseudomonas aeruginosa elastase. Formation of the disulfide bonds. J Biol Chem 276: 26030-26035.
8. Chatfield, S.N., Strahan, K., Pickard, D., Charles, I.G., Hormaeche, C.E., and Dougan, G. (1992) Evaluation of Salmonella typhimurium strains harbouring defined mutations in htrA and aroA in the murine salmonellosis model. Microb Pathog 12: 145-151.
9. Cortes, G., de Astorza, B., Benedi, V.J., and Alberti, S. (2002) Role of the htrA gene in Klebsiella pneumoniae virulence. Infect Immun 70: 4772-4776.
10. E, is required for intracellular survival of nontypeable Haemophilus influenzae in J774 macrophages. Infect Immun 70: 708-715.
11. E and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli Genes Dev 11: 1183-1193.
12. Danese, P.N., and Silhavy, T.J. (1998) CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180: 831-839.
13. Danese, P.N., Snyder, W.B., Cosma, C.L., Davis, L.J., and Silhavy, T.J. (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.
14. Danese, P.N., Oliver, G.R., Barr, K., Bowman, G.D., Rick, P.D., and Silhavy, T.J. (1998) Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J Bacteriol 180: 5875-5884.
15. Dartigalongue, C., and Raina, S. (1998) A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J 17: 3968-3980.
16. E regulon. J Biol Chem 276: 20866-20875.
17. E is an essential sigma factor in Escherichia coli. J Bacteriol 179: 6862-6864.
18. De Wulf, P., Akerley, B., and Lin, E.C.C. (2000) Presence of the Cpx system in bacteria. Microbiol 146: 247-248.
19. De Wulf, P., McGuire, A.M., Liu, X., and Lin, E.C. (2002) Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J Biol Chem 277: 26652-26661.
20. DiGiuseppe, P.A., and Silhavy, T.J. (2003) Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol 185: 2432-2440.
21. Donnenberg, M.S., Zhang, H.-Z., and Stone, K.D. (1997) Biogenesis of 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.
22. E subunit of Escherichia coli RNA polymerase: a second alternate σ factor involved in high-temperature gene expression. Genes Dev 3: 1462-1471.
23. Flynn, J.M., Levchenko, I., Sauer, R.T., and Baker, T.A. (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.
24. Foreman, D.T., Martinez, Y., Coombs, G., Torres, A., and Kupersztoch, Y.M. (1995) TolC and DsbA are needed for the secretion of STB, a heat-stable enterotoxin of Escherichia coli. Mol Microbiol 18: 237-245.
25. Gal-Mor, O., and Segal, G. (2003) Identification of CpxR as a positive regulator of icm and dot virulence genes of Legionella pneumophila. J Bacteriol 185: 4908-4919.
26. Gonzalez, M.D., Lichtensteiger, C.A., and Vimr, E.R. (2001) Adaptation of signature-tagged mutagenesis to Escherichia coli K1 and the infant-rat model of invasive disease. FEMS Microbiol Lett 198: 125-128.
27. Graham, J.E., and Clark-Curtiss, J.E. (1999) identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proc Natl Acad Sci USA 96: 11554-11559.
28. E envelope stress response relies on multiple mechanisms to inhibit signal-independent proteolysis of the transmembrane anti-sigma factor, RseA. Genes Dev 18: 2686-2697.
29. Ha, U.H., Wang, Y., and Jin, S. (2003) DsbA of Pseudomonas aeruginosa is essential for multiple virulence factors. Infect Immun 71: 1590-1595.
30. Hayashi, S., Abe, M., Kimoto, M., Furukawa, S., and Nakazawa, T. (2000) The dsbA-dsbB disulfide bond formation system of Burkholderia cepacia is involved in the production of protease and alkaline phosphatase, motility, metal resistance, and multi-drug resistance. Microbiol Immunol 44: 41-50.
31. Hernday, A.D., Braaten, B.A., Broitman-Maduro, G., Engelberts, P., and Low, D.A. (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.
32. Heusipp, G., Schmidt, M.A., and Miller, V.L. (2003) Identification of rpoE and nadB as host responsive elements of Yersinia enterocolitica. FEMS Microbiol Lett 226: 291-298.
33. Heusipp, G., Nelson, K.M., Schmidt, M.A., and Miller, V.L. (2004) Regulation of htrA expression in Yersinia enterocolitica. FEMS Microbiol Lett 231: 227-235.
34. Hicks, S., Frankel, G., Kaper, J.B., Dougan, G., and Phillips, A.D. (1998) Role of intimin and bundle-forming pili in enteropathogenic Escherichia coli adhesion to pediatric intestinal tissue in vitro. Infect Immun 66: 1570-1578.
35. Hirakawa, H., Nishino, K., Yamada, J., Hirata, T., and 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.
36. E, is critically important for the virulence of Salmonella typhimurium. Infect Immun 67: 1560-1568.
37. Humphreys, S., Rowley, G., Stevenson, A., Anjum, M.F., Woodward, M.J., Gilbert, S. et al. (2004) Role of the two-component regulator CpxAR in the virulence of Salmonella enterica serotype Typhimurium. Infect Immun 72: 4654-4661.
38. Hung, D.L., Raivio, T.L., Jones, C.H., Silhavy, T.J., and Hultgren, S.J. (2001) Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J 20: 1508-1518.
39. Jackson, M.W., and Piano, G.V. (1999) DsbA is required for stable expression of outer membrane protein YscC and for efficient Yop secretion in Yersinia pestis. J Bacteriol 181: 5126-5130.
40. Johnson, K., Charles, I., Dougan, G., Pickard, D., O'Gaora, P., Costa, G. et al. (1991) The role of a stress-response protein in Salmonella typhimurium virulence. Mol Microbiol 5: 401-407.
41. Jones, C.H., Danese, P.M., Pinkner, J.S., Silhavy, T.J., and Hultgren, S.J. (1997) The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J 21: 6394-6406.
42. E, RseA. Genes Dev 16: 2147-2155.
43. E plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect Immun 70: 5355-5362.
44. Leong, J.M., Morrissey, P.E., and Isberg, R.R. (1993) A 76-amino acid disulfide loop in the Yersinia pseudotuberculosis invasin protein is required for integrin receptor recognition. J Biol Chem 268: 20524-20532.
45. Li, S.R., Dorrell, N., Everest, P.H., Dougan, G., and Wren, B.W. (1996) Construction and characterization of a Yersinia enterocolitica O:8 high-temperature requirement (htrA) isogenic mutant. Infect Immun 64: 2088-2094.
46. Malhotra, S., Silo-Suh, L.A., Mathee, K., and Ohman, D.E. (2000) Proteome analysis of the effect of mucoid conversion on global protein expression in Pseudomonas aeruginosa strain PAO1 shows induction of the disulfide bond isomerase. Dsba J Bacteriol 182: 6999-7006.
47. E: role in global gene expression and survival in macrophages. Mol Microbiol 41: 423-437.
48. E, an Escherichia coli heat-inducible σ-factor, is modulated by expression of outer membrane proteins. Genes Dev 7: 2618-2628.
49. Miki, T., Okada, N., and Danbara, H. (2004) Two periplasmic disulfide oxidoreductases, DsbA and SrgA, target outer membrane protein SpiA, a component of the Salmonella pathogenicity island 2 type III secretion system. J Biol Chem 279: 34631-34642.
50. Mileykovskaya, E., and Dowhan, W. (1997) The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine. J Bacteriol 179: 1029-1034.
51. E in Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett 226: 307-314.
52. Mitobe, J., Arakawa, E., and Watanabe, H. (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: 107-113.
53. Mutunga, M., Graham, S., De Hormaeche, R.D., Musson, J.A., Robinson, J.H., Mastroeni, P. et al. (2004) Attenuated Salmonella typhimurium htrA mutants cause fatal infections in mice deficient in NADPH oxidase and destroy NADPH oxidase-deficient macrophage monolayers. Vaccine 22:4124-4131.
54. Nagakubo, S., Nishino, K., Hirata, T., and 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.
55. Nakayama, S., Kushiro, A., Asahara, T., Tanaka, R., Hu, L., Kopecko, D.J., and 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. Microbiol 149: 2809-2817.
56. Nakayama, S.-I., and Watanabe, H. (1995) Involvement of cpxA, a sensor of a two-component regulatory system, in the pH-dependent regulation of expression of Shigella sonnei virF gene. J Bacteriol 177: 5062-5069.
57. Nakayama, S.-I., and Watanabe, H. (1998) Identification of cpxR as a positive regulator essential for expression of the Shigella sonnei virF gene. J Bacteriol 180: 3522-3528.
58. Nevesinjac, A.Z., and Raivio, T.L. (2005) The Cpx Envelope Stress Response Affects Expression of the Type IV Bundle-Forming Pili of Enteropathogenic Escherichia coli. J Bacteriol 187: 672-686.
59. Okamoto, K., Baba, T., Yamanaka, H., Akashi, N., and Fujii, Y. (1995) Disulfide bond formation and secretion of Escherichia coli heat-stable enterotoxin II. J Bacteriol 177: 4579-4586.
60. Otto, K., and Silhavy, T.J. (2002) Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci USA 99: 2287-2292.
61. Peek, J.A., and Taylor, R.K. (1992) Characterization of a periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proc Natl Acad Sci USA 89: 6210-6214.
62. Phillips, R.W., and Roop, R.M., 2nd (2001) Brucella abortus HtrA functions as an authentic stress response protease but is not required for wild-type virulence in BALB/c mice. Infect Immun 69: 5911-5913.
63. Pogliano, J.A., Lynch, S., Belin, D., Lin, E.C.C., and 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.
64. Pugsley, A.P., Bayan, N., and Sauvonnet, N. (2001) Disulfide bond formation in secreton component PulK provides a possible explanation for the role of DsbA in pullulanase secretion. J Bacteriol 183: 1312-1319.
65. Purdy, G.E., Hong, M., and Payne, S.M. (2002) Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread. Infect Immun 70: 6355-6364.
66. Raffa, R.G., and Raivio, T.L. (2002) A third envelope stress signal transduction pathway in Escherichia coli. Mol Microbiol 45: 1599-1611.
67. Raivio, T.L., and Silhavy, T.J. (1997) Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J Bacteriol 179: 7724-7733.
68. E and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr Opin Microbiol 2: 159-165.
69. Raivio, T.L., and Silhavy, T.J. (2001) Periplasmic stress and ECF sigma factors. Annu Rev Microbiol 55: 591-624.
70. Raivio, T.L., Popkin, D.L., and Silhavy, T.J. (1999) The Cpx envelope stress response is controlled by amplification and feedback inhibition. J Bacteriol 181: 5263-5272.
71. Raivio, T.L., Laird, M.W., Joly, J.C., and Silhavy, T.J. (2000) Tethering of CpxP to the inner membrane prevents spheroplast induction of the Cpx envelope stress response. Mol Microbiol 37: 1186-1197.
72. Resto-Ruiz, S.I., Sweger, D., Widen, R.H., Valkov, N., and Anderson, B.E. (2000) Transcriptional activation of the htrA (High-temperature requirement A) gene from Bartonella henselae. Infect Immun 68: 5970-5978.
73. Sauvonnet, N., and Pugsley, A.P. (1998) The requirement for DsbA in pullulanase secretion is independent of disulphide bond formation in the enzyme. Mol Microbiol 27: 661-667.
74. Sinha, S., Langford, P.R., and Kroll, J.S. (2004) Functional diversity of three different DsbA proteins from Neisseria meningitidis. Microbiol 150: 2993-3000.
75. Snyder, W.B., Davis, L.J.B., Danese, P.M., Cosma, C.L., and Silhavy, T.J. (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.
76. Spiess, C., Beil, A., and Ehrmann, M. (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97: 339-347.
77. Stenson, T.H., and Weiss, A.A. (2002) DsbA and DsbC are required for secretion of pertussis toxin by Bordetella pertussis. Infect Immun 70: 2297-2303.
78. Suntharalingam, P., Spencer, H., Gallant, C.V., and Martin, N.L. (2003) Salmonella enterica serovar Typhimurium rdoA is growth phase regulated and involved in relaying Cpx-induced signals. J Bacteriol 185: 432-443.
79. Tacket, C.O., Sztein, M.B., Losonsky, G.A., Wasserman, S.S., Nataro, J.P., Edelman, R. et al. (1997) Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans. Infect Immun 65: 452-456.
80. E controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol Microbiol 43:771-782.
81. Tinsley, C.R., Voulhoux, R., Beretti, J.L., Tommassen, J.P., and Massif, X. (2004) Three homologues, including two membrane-bound proteins, of the disulphide oxidoreductase DsbA in Neisseria meningitidis: effects on bacterial growth and biogenesis of functional type IV pili. J Biol Chem 279: 27078-27087.
82. Urban, A., Leipelt, M., Eggert, T., and Jaeger, K.E. (2001) DsbA and DsbC affect extracellular enzyme formation in Pseudomonas aeruginosa. J Bacteriol 183: 587-596.
83. Vincent-Sealy, L.V., Thomas, J.D., Commander, P., and Salmond, G.P.C. (1999) Erwinia carotovora DsbA mutants: evidence for a periplasmic-stress signal transduction system affecting transcription of genes encoding secreted proteins. Microbiol 145: 1945-1958.
84. Walsh, N.P., Alba, B.M., Bose, B., Gross, C.A., and Sauer, R.T. (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.
85. Watarai, M., Tobe, T., Yoshikawa, M., and Sasakawa, C. (1995) Disulfide oxidoreductase activity of Shigella flexneri is required for release of lpa proteins and invasion of epithelial cells. Proc Natl Acad Sci USA 92: 4927-4931.
86. Yamamoto, T., Hanawa, T., Ogata, S., and Kamiya, S. (1996) Identification and characterization of the Yersinia enterocolitica gsrA gene, which protectively responds to intracellular stress induced by macrophage phagocytosis and to extracellular environmental stress. Infect Immun 64: 2980-2987.
87. Yamamoto, T., Hanawa, T., Ogata, S., and Kamiya, S. (1997) The Yersinia enterocolitica GsrA stress protein, involved in intracellular survival, is induced by macrophage phagocytosis. Infect Immun 65: 2190-2196.
88. Yorgey, P., Rahme, L.G., Tan, M.W., and Ausubel, P.M. (2001) The roles of mucD and alginate in the virulence of Pseudomonas aeruginosa in plants, nematodes and mice. Mol Microbiol 41: 1063-1076.
89. Young, G.M., and Miller, V.L. (1997) Identification of novel chromosomal loci affecting Yersinia enterocolitica pathogenesis. Mol Microbiol 25: 319-328.
90. E). Infect Immun 64: 2774-2781.