Just scratching the surface: An expanding view of the Cpx envelope stress response

FEMS Microbiology Letters

Volumn 326, Issue 1, 2012, Pages 2-11

  Vogt, Stefanie L ^a   Raivio, Tracy L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cpx envelope stress response; Escherichia coli; Two component signal transduction

Indexed keywords

BACTERIAL PROTEIN; CPX PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL METABOLISM; BACTERIAL SURVIVAL; BACTERIUM PILUS; CELL ADHESION; CPX ENVELOPE STRESS RESPONSE; CYTOPLASM; GRAM NEGATIVE BACTERIUM; MEMBRANE DAMAGE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REGULON; SHORT SURVEY; SIGNAL TRANSDUCTION; STRESS;

BACTERIAL PROTEINS; CELL MEMBRANE; GRAM-NEGATIVE BACTERIA; PROTEIN FOLDING; PROTEIN KINASES; REGULON; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 83055178971     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2011.02406.x     Document Type: Short Survey

References (82)

1. Altman E & Segal G (2008) The response regulator CpxR directly regulates expression of several Legionella pneumophila icm/dot components as well as new translocated substrates. J Bacteriol 190: 1985-1996.
2. Boehm A, Steiner S, Zaehringer F, Casanova A, Hamburger F, Ritz D, Keck W, Ackermann M, Schirmer T & Jenal U (2009) Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress. Mol Microbiol 72: 1500-1516.
3. 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.
4. Buelow DR & Raivio TL (2010) Three (and more) component regulatory systems - auxiliary regulators of bacterial histidine kinases. Mol Microbiol 75: 547-566.
5. Bury-Moné S, Nomane Y, Reymond N, Barbet R, Jacquet E, Imbeaud S, Jacq A & Bouloc P (2009) Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet 5: e1000651.
6. Carlsson KE, Liu J, Edqvist PJ & Francis MS (2007a) Extracytoplasmic-stress-responsive pathways modulate type III secretion in Yersinia pseudotuberculosis. Infect Immun 75: 3913-3924.
7. Carlsson KE, Liu J, Edqvist PJ & Francis MS (2007b) Influence of the Cpx extracytoplasmic-stress-responsive pathway on Yersinia sp.-eukaryotic cell contact. Infect Immun 75: 4386-4399.
8. Chaston J & Goodrich-Blair H (2010) Common trends in mutualism revealed by model associations between invertebrates and bacteria. FEMS Microbiol Rev 34: 41-58.
9. 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.
10. E and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev 11: 1183-1193.
11. Danese PN & Silhavy TJ (1998) CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180: 831-839.
12. 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.
13. 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.
14. 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.
15. 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.
16. DiGiuseppe PA & Silhavy TJ (2003) Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol 185: 2432-2440.
17. 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.
18. 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.
19. 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.
20. Gal-Mor O & Segal G (2003) Identification of CpxR as a positive regulator of icm and dot virulence genes of Legionella pneumophila. J Bacteriol 185: 4908-4919.
21. Gerken H & Misra R (2010) MzrA-EnvZ interactions in the periplasm influence the EnvZ/OmpR two-component regulon. J Bacteriol 192: 6271-6278.
22. Gerken H, Charlson ES, Cicirelli EM, Kenney LJ & Misra R (2009) MzrA: a novel modulator of the EnvZ/OmpR two-component regulon. Mol Microbiol 72: 1408-1422.
23. Groban ES, Clarke EJ, Salis HM, Miller SM & Voigt CA (2009) Kinetic buffering of cross talk between bacterial two-component sensors. J Mol Biol 390: 380-393.
24. Gubbins MJ, Lau I, Will WR, Manchak JM, Raivio TL & Frost LS (2002) The positive regulator, TraJ, of the Escherichia coli F plasmid is unstable in a cpxA* background. J Bacteriol 184: 5781-5788.
25. 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.
26. Herbert Tran EE & Goodrich-Blair H (2009) CpxRA contributes to Xenorhabdus nematophila virulence through regulation of lrhA and modulation of insect immunity. Appl Environ Microbiol 75: 3998-4006.
27. Herbert Tran EE, Andersen AW & Goodrich-Blair H (2009) CpxRA influences Xenorhabdus nematophila colonization initiation and outgrowth in Steinernema carpocapsae nematodes through regulation of the nil locus. Appl Environ Microbiol 75: 4007-4014.
28. Herbert EE, Cowles KN & Goodrich-Blair H (2007) CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila. Appl Environ Microbiol 73: 7826-7836.
29. 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.
30. 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.
31. 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.
32. Humphries RM, Griener TP, Vogt SL, Mulvey GL, Raivio T, Donnenberg MS, Kitov PI, Surette M & Armstrong GD (2010) N-acetyllactosamine-induced retraction of bundle-forming pili regulates virulence-associated gene expression in enteropathogenic Escherichia coli. Mol Microbiol 76: 1111-1126.
33. 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.
34. Isaac DD, Pinkner JS, Hultgren SJ & Silhavy TJ (2005) The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. P Natl Acad Sci USA 102: 17775-17779.
35. Ize B, Stanley NR, Buchanan G & Palmer T (2003) Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol Microbiol 48: 1183-1193.
36. Jacob-Dubuisson F, Pinkner J, Xu Z, Striker R, Padmanhaban A & Hultgren SJ (1994) PapD chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of DsbA. P Natl Acad Sci USA 91: 11552-11556.
37. Jonas K, Edwards AN, Simm R, Romeo T, Römling U & Melefors O (2008) The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol Microbiol 70: 236-257.
38. 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.
39. 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.
40. Keller RF & Hunke S (2009) Misfolded maltose binding protein MalE219 induces the CpxRA envelope stress response by stimulating phosphoryl transfer from CpxA to CpxR. Res Microbiol 160: 396-400.
41. Kwon E, Kim DY, Gross CA, Gross JD & Kim KK (2010) The crystal structure Escherichia coli Spy. Protein Sci 19: 2252-2259.
42. Labandeira-Rey M, Mock JR & Hansen EJ (2009) Regulation of expression of the Haemophilus ducreyi LspB and LspA2 proteins by CpxR. Infect Immun 77: 3402-3411.
43. Labandeira-Rey M, Brautigam CA & Hansen EJ (2010) Characterization of the CpxRA regulon in Haemophilus ducreyi. Infect Immun 78: 4779-4791.
44. Lau-Wong IC, Locke T, Ellison MJ, Raivio TL & Frost LS (2008) Activation of the Cpx regulon destabilizes the F plasmid transfer activator, TraJ, via the HslVU protease in Escherichia coli. Mol Microbiol 67: 516-527.
45. 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.
46. Lima BP, Antelmann H, Gronau K, Chi BK, Becher D & Wolfe AJ (2011) Involvement of protein acetylation in glucose-induced transcription of a stress-responsive promoter. Mol Microbiol 81: 1190-1204.
47. MacRitchie DM, Buelow DR, Price NL & Raivio TL (2008a) Two-component signaling and gram negative envelope stress response systems. Adv Exp Med Biol 631: 80-110.
48. MacRitchie DM, Ward JD, Nevesinjac AZ & Raivio TL (2008b) 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.
49. Magnet S, Bellais S, Dubost L, Fourgeaud M, Mainardi JL, Petit-Frère S, Marie A, Mengin-Lecreulx D, Arthur M & Gutmann L (2007) Identification of the L, D-transpeptidases responsible for attachment of the Braun lipoprotein to Escherichia coli peptidoglycan. J Bacteriol 189: 3927-3931.
50. McEwen J & Silverman P (1980) Chromosomal mutations of Escherichia coli that alter expression of conjugative plasmid functions. P Natl Acad Sci USA 77: 513-517.
51. 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.
52. Mitobe J, Arakawa E & 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. 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.
54. Nakayama S & 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.
55. Nakayama S & Watanabe H (1998) Identification of cpxR as a positive regulator essential for expression of the Shigella sonnei virF gene. J Bacteriol 180: 3522-3528.
56. 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.
57. Nixon BT, Ronson CW & Ausubel FM (1986) Two-component regulatory systems responsive to environmental stimuli share strongly conserved domains with the nitrogen assimilation regulatory genes ntrB and ntrC. P Natl Acad Sci USA 83: 7850-7854.
58. Ogasawara H, Yamada K, Kori A, Yamamoto K & Ishihama A (2010) Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. Microbiology 156: 2470-2483.
59. Otto K & Silhavy TJ (2002) Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. P Natl Acad Sci USA 99: 2287-2292.
60. Peek JA & Taylor RK (1992) Characterization of a periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. P Natl Acad Sci USA 89: 6210-6214.
61. 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.
62. Price NL & Raivio TL (2009) Characterization of the Cpx regulon in Escherichia coli strain MC4100. J Bacteriol 191: 1798-1815.
63. Prigent-Combaret C, Brombacher E, Vidal O, Ambert A, Lejeune P, Landini P & Dorel C (2001) Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183: 7213-7223.
64. Quan S, Koldewey P, Tapley T et al. (2011) Genetic selection designed to stabilize proteins uncovers a chaperone called Spy. Nat Struct Mol Biol 18: 262-269.
65. Raivio TL & Silhavy TJ (1997) Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J Bacteriol 179: 7724-7733.
66. Raivio TL, Popkin DL & Silhavy TJ (1999) The Cpx envelope stress response is controlled by amplification and feedback inhibition. J Bacteriol 181: 5263-5272.
67. 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.
68. Shimohata N, Chiba S, Saikawa N, Ito K & Akiyama Y (2002) The Cpx stress response system of Escherichia coli senses plasma membrane proteins and controls HtpX, a membrane protease with a cytosolic active site. Genes Cells 7: 653-662.
69. Silverman PM, Tran L, Harris R & Gaudin HM (1993) Accumulation of the F plasmid TraJ protein in cpx mutants of Escherichia coli. J Bacteriol 175: 921-925.
70. Siryaporn A & Goulian M (2008) Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli. Mol Microbiol 70: 494-506.
71. 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.
72. Spinola SM, Fortney KR, Baker B, Janowicz DM, Zwickl B, Katz BP, Blick RJ & Munson RS (2010) Activation of the CpxRA system by deletion of cpxA impairs the ability of Haemophilus ducreyi to infect humans. Infect Immun 78: 3898-3904.
73. van Stelten J, Silva F, Belin D & Silhavy TJ (2009) Effects of antibiotics and a proto-oncogene homolog on destruction of protein translocator SecY. Science 325: 753-756.
74. Thede GL, Arthur DC, Edwards RA, Buelow DR, Wong JL, Raivio TL & Glover JN (2011) Structure of the periplasmic stress response protein CpxP. J Bacteriol 193: 2149-2157.
75. Vincent CD, Buscher BA, Friedman JR, Williams LA, Bardill P & Vogel JP (2006) Identification of non-dot/icm suppressors of the Legionella pneumophila ΔdotL lethality phenotype. J Bacteriol 188: 8231-8243.
76. Vogt SL, Nevesinjac AZ, Humphries R, Donnenberg MS, Armstrong GD & Raivio TL (2010) The Cpx envelope stress response both facilitates and inhibits elaboration of the enteropathogenic Escherichia coli bundle-forming pilus. Mol Microbiol 76: 1095-1110.
77. Weatherspoon-Griffin N, Zhao G, Kong W, Kong Y, Morigen M, Andrews-Polymenis H, McClelland M & Shi Y (2011) The CpxR/CpxA two-component system upregulates two Tat-dependent peptidoglycan amidases to confer bacterial resistance to antimicrobial peptide. J Biol Chem 286: 5529-5539.
78. Wolanin PM, Thomason PA & Stock JB (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 3: REVIEWS3013.
79. Wolfe AJ, Parikh N, Lima BP & Zemaitaitis B (2008) Signal integration by the two-component signal transduction response regulator CpxR. J Bacteriol 190: 2314-2322.
80. Yamamoto K & Ishihama A (2006) Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci Biotechnol Biochem 70: 1688-1695.
81. Zhang HZ & Donnenberg MS (1996) DsbA is required for stability of the type IV pilin of enteropathogenic Escherichia coli. Mol Microbiol 21: 787-797.
82. Zhou X, Keller R, Volkmer R, Krauss N, Scheerer P & Hunke S (2011) Structural basis for two-component system inhibition and pilus sensing by the auxiliary CpxP protein. J Biol Chem 286: 9805-9814.