Activation of the Cpx envelope stress response down-regulates expression of several locus of enterocyte effacement-encoded genes in enteropathogenic Escherichia coli

Infection and Immunity

Volumn 76, Issue 4, 2008, Pages 1465-1475

  MacRitchie, Dawn M ^a   Ward, Jordan D ^b   Nevesinjac, Anna Z ^a   Raivio, Tracy L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTIMIN; MEMBRANE PROTEIN; OLIGONUCLEOTIDE; PROTEIN CPX; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CPXA PROTEIN, E COLI; CPXR PROTEIN, BACTERIA; ESCHERICHIA COLI PROTEIN; LEE PROTEIN, E COLI; LER PROTEIN, E COLI; LUMINESCENT AGENT; PHOSPHOPROTEIN; PROTEIN KINASE; TRANSACTIVATOR PROTEIN;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; CELL SECRETION; CONTROLLED STUDY; DOWN REGULATION; ENTEROPATHOGENIC ESCHERICHIA COLI; GENE ACTIVATION; GENE EXPRESSION; GENE LOCUS; GENETIC CODE; GENETIC TRANSCRIPTION; INTESTINE CELL; NONHUMAN; OPERON; PATHOGENICITY; PLASMID; PRIORITY JOURNAL; PROTEIN FUNCTION; STRESS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MULTIGENE FAMILY;

BACTERIAL PROTEINS; DOWN-REGULATION; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LUMINESCENT AGENTS; MULTIGENE FAMILY; PHOSPHOPROTEINS; PROTEIN KINASES; TRANS-ACTIVATORS;

EID: 42149173339     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01265-07     Document Type: Article

References (59)

1. Beeston, A. L., and M. G. Surette. 2002. pfs-dependent regulation of autoinducer 2 production in Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:3450-3456.
2. Buelow, B. R., and T. L. Raivio. 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.
3. Bustamente, V. H., F. J. Santana, E. Calva, and J. L. Puente. 2001. Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol. Microbiol. 39:664-678.
4. Carlsson, K. E., J. Lui, P. J. Edqvist, and M. S. Francis. 2007. Extracytoplasmic stress-responsive pathways modulate type III secretion in Yersinia pseudotuberculosis. Infect. Immun. 8:3913-3924.
5. Carlsson, K. E., J. Lui, P. J. Edqvist, and M. S. Francis. 2007. Influence of the Cpx extracytoplasmic-stress-responsive pathway on Yersinia sp.-eukaryotic cell contact. Infect. Immun. 75:4386-4399.
6. Casadaban, M. J. 1976. Transposition and fusion of lac genes to selected promoters in Escherichia coli using bacteriophages lambda and Mu. J. Mol. Biol. 104:541-555.
7. Chen, H. D., and G. Frankel. 2005. Enteropathogenic Escherichia coli: unraveling pathogenesis. FEMS Microbiol. Lett. 29:83-98.
8. E and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev. 11:1183-1193.
9. Daniell, S. J., N. Takahashi, R. Wilson, D. Friedberg, I. Rosenshine, F. P. Booy, R. K. Shaw, S. Knutton, G. Frankel, and S. Aizawa. 2001. The filamentous type III secretion translocon of enteropathogenic Escherichia coli. Cell. Microbiol. 3:865-871.
10. Dean, P., M. Maresca, and B. Kenny. 2005. EPECs weapons of mass subversion. Curr. Opin. Microbiol. 8:28-34.
11. Deng, W., Y. Li, P. R. Hardwidge, E. A. Frey, R. A. Pfuetzner, A. Lee, S. Gruenheid, N. C. J. Strynadka, J. L. Puente, and B. B. Finlay. 2005. Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect. Immun. 73:2135-2146.
12. Devinney, R., I. Nisan, S. Ruschkowski, I. Rosenshine, and B. B. Finlay. 2001. Tir tyrosine phosphorylation and pedestal formation are delayed in enteropathogenic Escherichia coli sepZ::TnphoA mutant 30-5-1(3). Infect. Immun. 69:559-563.
13. 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 of CpxR∼P in Escherichia coli. J. Biol. Chem. 277:26652-26661.
14. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
15. Donnenberg, M. S., H.-Z. Zhang, and K. D. Stone. 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.
16. Donnenberg, M. S., S. B. Calderwood, A. Donohue-Rolfe, G. T. Keusch, and J. P. Kaper. 1990. Construction and analysis of TnphoA mutants of enteropathogenic Escherichia coli unable to invade HEp-2 cells. Infect. Immun. 58:1565-1571.
17. Dorel, C., O. Vidal, C. Prigent-Combaret, I. Vallet, and P. Lejeuene. 1999. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol. Lett. 178:169-175.
18. Edwards, R. A., L. H. Keller, and D. M. Schifferli. 1998. Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207:149-157.
19. Elliott, S. J., L. A. Wainwright, T. K. McDaniel, K. G. Jarvis, Y. K. Deng, L. C. Lai, B. P. McNamara, M. S. Donnenberg, and J. B. Kaper. 1998. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol. Microbiol. 28:1-4.
20. Fleischer, R., R. K. Heermann, K. Jung, and H. Sabine. 2007. Purification, reconstitution, and characterization of the CpxAR envelope stress system of Escherichia coli. J. Biol. Chem. 282:8583-8593.
21. Francis, M. S., H. Wolf-Watz, and A. Forsberg. 2002. Regulation of type III secretion systems. Curr. Opin. Microbiol. 5:166-172.
22. Francis, M. S., S. A. Lloyd, and H. Wolf-Watz. 2001. The type III secretion chaperone LcrH co-operates with YopD to establish a negative, regulatory loop for control of Yop synthesis in Yersinia pseudotuberculosis. Mol. Microbiol. 42:1075-1093.
23. Gal-Mor, O., and G. Segal. 2003. Identification of CpxR as a positive regulator of icm and dot virulence genes of Legionella pneumophila. J. Bacteriol. 185:4908-4919.
24. Gomez-Duarte, O. G., and J. B. Kaper. 1995. A plasmid-encoded regulatory region activates chromosomal eaeA expression in enteropathogenic Escherichia coli. Infect. Immun. 63:1767-1776.
25. Ha, U. H., Y. Wang, and S. Jin. 2003. DsbA of Pseudomonas aeruginosa is essential for multiple virulence factors. Infect. Immun. 71:1590-1595.
26. Heraday, A. D., B. A. Braaten, G. Broitman-Maduro, P. Engelberts, and D. A. Low. 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.
27. Heusipp, G., K. M. Nelson, M. A. Schmidt, and V. L. Miller. 2004. Regulation of htrA expression in Yersinia enterocolitica. FEMS Microbiol. Lett. 16:227-235.
28. 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. 72:4654-4661.
29. 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. 20:1508-1518.
30. Ide, T., S. Laarmann, L. Greune, H. Schilers, H. Oberleithner, and M. A. Schmidt. 2001. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell. Microbiol. 3:669-679.
31. Isaac, D. D., J. S. Pinkner, S. J. Hultgren, and T. J. Silhavy. 2005. The extracytoplasmic adaptor protein CpxP is degraded with substrate by DegP. Proc. Natl. Acad. Sci. USA 102:17775-17779.
32. Jackson, M. W., and G. V. Plano. 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.
33. Johnson, K., I. Charles, G. Dougan, D. Pickard, P. O'Goara, G. Costa, T. Ali, I. Miller, and C. E. Hormaeche. 1991. The role of a stress-response protein in Salmonella typhimurium virulence. Mol. Microbiol. 5:401-407.
34. 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. 16:6394-6406.
35. Kaper, J. B., J. P. Nataro, and H. L. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140.
36. Kenny, B., A. Abe, M. Stein, and B. B. Finlay. 1997. Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect. Immun. 65:2606-2612.
37. Kitagawa, M., A. Takeshi, M. Afrifuzzaman, T. Ioka-Nakamichi, E. Inamoto, H. Toyonaga, and H. Mori. 2005. Complete set of orf clones of Escherichia coli ASKA library (a complete set of E. coli H-12 orf archive): unique resources for biological research. DNA Res. 12:291-299.
38. Knutton, S., I. Rosenshine, M. J. Pallen, I. Nissan, B. C. Nevesw, C. Bain, C. Wolff, G. Dougan, and G. Frankel. 1998. A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 17:2166-2176.
39. Leverton, L. Q., and J. B. Kaper. 2005. Temporal expression of enteropathogenic Escherichia coli virulence genes in an in vitro model of infection. Infect. Immun. 73:1034-1043.
40. Levine, M. M., J. P. Nataro, H. Karch, M. M. Baldini, J. B. Kaper, R. E. Black, M. L. Clements, and A. D. O'Brien. 1985. The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J. Infect. Dis. 152:550-559.
41. Li, S. R., N. Dorrell, P. H. Everest, G. Dougan, and B. W. Wren. 1996. Construction and characterization of a Yersinia entemcolitica O:8 high-temperature requirement (htrA) isogenic mutant. Infect. Immun. 64:2088-2094.
42. Mellies, J. L., and A. M. S. Barron. June 2006, posting date. Chapter 8.9.1. Virulence gene regulation in Escherichia coli. In R. Curtiss III et al. (ed.), EcoSal - Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC. http://www.ecosal.org.
43. Mellies, J. L., S. J. Elliott, V. Sperandio, M. S. Donnenberg, and J. B. Kaper. 1999. The Per regulon of enteropathogenic Escherichia coli: identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol. Microbiol. 33:296-306.
44. Miki, T., N. Okada, and H. Danbara. 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.
45. 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. 187:107-113.
46. Nakayama, S., A. Kushiro, T. Asahara, R. Tanaka, L. Hu, D. J. Kopecko, and H. Watanabe. 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.
47. Nakayama, S., and H. Watanabe. 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.
48. Nakayama, S., and H. Watanabe. 1998. Identification of cpxR as a positive regulator essential for expression of the Shigella sonnei virF gene. J. Bacteriol. 180:3522-3528.
49. 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. 187:672-686.
50. Otto, K., and T. J. Silhavy. 2002. Surface sensing and adhesion of Escherichia coli by the Cpx-signaling pathway. Proc. Natl. Acad. Sci. USA 99:2287-2292.
51. Pogliano, J. A., S. Lynch, D. Belin, E. C. C. Lin, and J. Beckwith. 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.
52. Porter, M. E., P. Mitchell, A. J. Roe, A. Free, D. G. Smith, and D. L. Gally. 2004. Direct and indirect transcriptional activation of virulence genes by an AraC-like protein, PerA from enteropathogenic Escherichia coli. Mol. Microbiol. 4:1117-1133.
53. Raivio, T. L. 2005. Envelope stress responses and gram-negative bacterial pathogenesis. Mol. Microbiol. 56:1119-1128.
54. Raivio, T. L., and T. J. Silhavy. 1997. Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J. Bacteriol. 179:7724-7733.
55. 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. 181:5263-5272.
56. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. 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. 177:4216-4223.
58. Stenson, T. H., and A. A. Weiss. 2002. DsbA and DsbC are required for secretion of Bordetella pertussis. Infect. Immun. 70:2297-2303.
59. Watarai, M., T. Tobe, M. Yoshikawa, and C. Sasakawa. 1995. Disulfide oxidoreductase activity of Shigella flexneri is required for release of Ipa proteins and invasion of epithelial cells. Proc. Natl. Acad. Sci. USA 92:4927-4931.