OmpC and the σE regulatory pathway are involved in adhesion and invasion of the Crohn's disease-associated Escherichia coli strain LF82

Molecular Microbiology

Volumn 63, Issue 6, 2007, Pages 1684-1700

  Rolhion, Nathalie ^a   Carvalho, Frédéric Antonio ^a   Darfeuille Michaud, Arlette ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN C; OUTER MEMBRANE PROTEIN F; PROTEIN; RPOE PROTEIN; SIGMA FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CELL ADHESION; CELL INVASION; CONTROLLED STUDY; CORRELATION ANALYSIS; CROHN DISEASE; ESCHERICHIA COLI; GENE DELETION; HUMAN; HUMAN CELL; INTESTINE CELL; NONHUMAN; OSMOLARITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; CROHN DISEASE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS;

ESCHERICHIA COLI;

EID: 33947281521     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05638.x     Document Type: Article

References (66)

1. Ades, S.E., Connolly, L.E., Alba, B.M., and Gross, C.A. (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.
2. Alba, B.M., Leeds, J.A., Onufryk, C., Lu, C.Z., and Gross, C.A. (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.
3. Arnott, I.D., Landers, C.J., Nimmo, E.J., Drummond, H.E., Smith, B.K., Targan, S.R., and Satsangi, J. (2004) Seroreactivity to microbial components in Crohn's disease is associated with disease severity and progression, but not NOD2/CARD15 genotype. Am J Gastroenterol 99: 2376-2384.
4. Bang, I.S., Frye, J.G., McClelland, M., Velayudhan, J., and Fang, F.C. (2005) Alternative sigma factor interactions in Salmonella: sigma and sigma promote antioxidant defences by enhancing sigma levels. Mol Microbiol 56: 811-823.
5. Barnich, N., Boudeau, J., Claret, L., and Darfeuille-Michaud, A. (2003) Regulatory and functional co-operation of flagella and type 1 pili in adhesive and invasive abilities of AIEC strain LF82 isolated from a patient with Crohn's disease. Mol Microbiol 48: 781-794.
6. Barnich, N., Bringer, M.A., Claret, L., and Darfeuille-Michaud, A. (2004) Involvement of lipoprotein NlpI in the virulence of adherent invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun 72: 2484-2493.
7. Beaven, S.W., and Abreu, M.T. (2004) Biomarkers in inflammatory bowel disease. Curr Opin Gastroenterol 20: 318-327.
8. Bernardini, M.L., Sanna, M.G., Fontaine, A., and Sansonetti, P.J. (1993) OmpC is involved in invasion of epithelial cells by Shigella flexneri. Infect Immun 61: 3625-3635.
9. Boudeau, J., Glasser, A.L., Masseret, E., Joly, B., and Darfeuille-Michaud, A. (1999) Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect Immun 67: 4499-4509.
10. Boudeau, J., Barnich, N., and Darfeuille-Michaud, A. (2001) Type 1 pili-mediated adherence of Escherichia coli strain LF82 isolated from Crohn's disease is involved in bacterial invasion of intestinal epithelial cells. Mol Microbiol 39: 1272-1284.
11. Bringer, M.A., Barnich, N., Glasser, A.L., Bardot, O., and Darfeuille-Michaud, A. (2005) HtrA stress protein is involved in intramacrophagic replication of adherent and invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun 73: 712-721.
12. Burke, D.A., and Axon, A.T. (1988) Adhesive Escherichia coli in inflammatory bowel disease and infective diarrhoea. BMJ 297: 102-104.
13. Cano, D.A., Martinez-Moya, M., Pucciarelli, M.G., Groisman, E.A., Casadesus, J., and Garcia-Del Portillo, F. (2001) Salmonella enterica serovar Typhimurium response involved in attenuation of pathogen intracellular proliferation. Infect Immun 69: 6463-6474.
14. Chaveroche, M.K., Ghigo, J.M., and d'Enfert, C. (2000) A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 28: E97.
15. Chowdhury, R., Sahu, G.K., and Das, J. (1996) Stress response in pathogenic bacteria. J Biosci 21: 149-160.
16. 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.
17. Darfeuille-Michaud, A., Neut, C., Barnich, N., Lederman, E., Di Martino, P., Desreumaux, P., et al. (1998) Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 115: 1405-1413.
18. Darfeuille-Michaud, A., Boudeau, J., Bulois, P., Neut, C., Glasser, A.L., Barnich, N., et al. (2004) High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127: 412-421.
19. Dartigalongue, C., Missiakas, D., and Raina, S. (2001) Characterization of the Escherichia coli sigma E regulon. J Biol Chem 276: 20866-20875.
20. De Las Penas, A., Connolly, L., and Gross, C.A. (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.
21. Duchmann, R., Lochs, H., and Kruis, W. (1999) [Crohn disease, ulcerative colitis. When bacteria attack the intestinal wall...]. MMW Fortschr Med 141: 48-51.
22. Elson, C.O. (2000) Commensal bacteria as targets in Crohn's disease. Gastroenterology 119: 254-257.
23. Fordtran, J.S., and Ingelfinger, F.J. (1968) Absorption of water, electrolytes, and sugars from the human gut. In Handbook of Physiology. Heidel, W., and Code, C.F. (eds). Baltimore, MD: Waverly Press, pp. 1457-1490.
24. Forst, S., and Inouye, M. (1988) Environmentally regulated gene expression for membrane proteins in Escherichia coli. Annu Rev Cell Biol 4: 21-42.
25. Foster, J.W., and Spector, M.P. (1995) How Salmonella survive against the odds. Annu Rev Microbiol 49: 145-174.
26. Grigorova, I.L., Chaba, R., Zhong, H.J., Alba, B.M., Rhodius, V., Herman, C., and Gross, C.A. (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.
27. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
28. Hall, M.N., and Silhavy, T.J. (1981a) Genetic analysis of the ompB locus in Escherichia coli K-12. J Mol Biol 151: 1-15.
29. Hall, M.N., and Silhavy, T.J. (1981b) The ompB locus and the regulation of the major outer membrane porin proteins of Escherichia coli K12. J Mol Biol 146: 23-43.
30. Hara-Kaonga, B., and Pistole, T.G. (2004) OmpD but not OmpC is involved in adherence of Salmonella enterica serovar typhimurium to human cells. Can J Microbiol 50: 719-727.
31. Humphreys, S., Stevenson, A., Bacon, A., Weinhardt, A.B., and Roberts, M. (1999) The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect Immun 67: 1560-1568.
32. Kanehara, K., Ito, K., and 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.
33. Kovacikova, G., and Skorupski, K. (2002) The alternative sigma factor sigma (E) plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect Immun 70: 5355-5362.
34. Kutsukake, K. (1997) Autogenous and global control of the flagellar master operon, flhD. Salmonella typhimurium. Mol Gen Genet 254: 440-448.
35. Lamps, L.W., Madhusudhan, K.T., Havens, J.M., Greenson, J.K., Bronner, M.P., Chiles, M.C., et al. (2003) Pathogenic Yersinia DNA is detected in bowel and mesenteric lymph nodes from patients with Crohn's disease. Am J Surg Pathol 27: 220-227.
36. Landers, C.J., Cohavy, O., Misra, R., Yang, H., Lin, Y.C., Braun, J., and Targan, S.R. (2002) Selected loss of tolerance evidenced by Crohn's disease-associated immune responses to auto- and microbial antigens. Gastroenterology 123: 689-699.
37. Levine, M.M., Ristaino, P., Marley, G., Smyth, C., Knutton, S., Boedeker, E., et al. (1984) Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans. Infect Immun 44: 409-420.
38. Liu, Y., van Kruiningen, H.J., West, A.B., Cartun, R.W., Cortot, A., and Colombel, J.F. (1995) Immunocytochemical evidence of Listeria, Escherichia coli, and Streptococcus antigens in Crohn's disease. Gastroenterology 108: 1396-1404.
39. McBroom, A.J., Johnson, A.P., Vemulapalli, S., and Kuehn, M.J. (2006) Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 188: 5385-5392.
40. Manganelli, R., Voskuil, M.I., Schoolnik, G.K., and Smith, I. (2001) The Mycobacterium tuberculosis ECF sigma factor sigmaE: role in global gene expression and survival in macrophages. Mol Microbiol 41: 423-437.
41. Martin, H.M., Campbell, B.J., Hart, C.A., Mpofu, C., Nayar, M., Singh, R., et al. (2004) Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 127: 80-93.
42. Mecsas, J., Rouviere, P.E., Erickson, J.W., Donohue, T.J., and Gross, C.A. (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.
43. Missiakas, D., Mayer, M.P., Lemaire, M., Georgopoulos, C., and 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.
44. Mizuno, T., and Mizushima, S. (1990) Signal transduction and gene regulation through the phosphorylation of two regulatory components: the molecular basis for the osmotic regulation of the porin genes. Mol Microbiol 4: 1077-1082.
45. Mow, W.S., Vasiliauskas, E.A., Lin, Y.C., Fleshner, P.R., Papadakis, K.A., Taylor, K.D., et al. (2004) Association of antibody responses to microbial antigens and complications of small bowel Crohn's disease. Gastroenterology 126: 414-424.
46. Nikaido, H., and Rosenberg, E.Y. (1983) Porin channels in Escherichia coli: studies with liposomes reconstitued from purified proteins. J Bacteriol 153: 241-252.
47. Onufryk, C., Crouch, M.L., Fang, F.C., and Gross, C.A. (2005) Characterization of six lipoproteins in the sigmaE regulon. J Bacteriol 187: 4552-4561.
48. Oshima, T., Aiba, H., Masuda, Y., Kanaya, S., Sugiura, M., Wanner, B.L., et al. (2002) Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 46: 281-291.
49. Podolsky, D.K. (2002) Inflammatory bowel disease. N Engl J Med 347: 417-429.
50. Pratt, L.A., Hsing, W., Gibson, K.E., and Silhavy, T.J. (1996) From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli. Mol Microbiol 20: 911-917.
51. Pruss, B.M. (1998) Acetyl phosphate and the phosphorylation of OmpR are involved in the regulation of the cell division rate in Escherichia coli. Arch Microbiol 170: 141-146.
52. Pugsley, A.P., and Schnaitman, C.A. (1979) Factors affecting the electrophoretic mobility of the major outer membrane proteins of Escherichia coli in polyacrylamide gels. Biochim Biophys Acta 581: 163-178.
53. Raina, S., Missiakas, D., and Georgopoulos, C. (1995) The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli. EMBO J 14: 1043-1055.
54. Raivio, T.L., and Silhavy, T.J. (1999) The sigmaE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr Opin Microbiol 2: 159-165.
55. Rezuchova, B., Miticka, H., Homerova, D., Roberts, M., and Kormanec, J. (2003) New members of the Escherichia coli sigmaE regulon identified by a two-plasmid system. FEMS Microbiol Lett 225: 1-7.
56. Rhodius, V.A., Suh, W.C., Nonaka, G., West, J., and Gross, C.A. (2006) Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 4: e2.
57. Rolhion, N., Barnich, N., Claret, L., and Darfeuille-Michaud, A. (2005) Strong decrease in invasive ability and outer membrane vesicle release in Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 with the yfgL gene deleted. J Bacteriol 187: 2286-2296.
58. Sartor, R.B., Rath, H.C., Lichtman, S.N., and van Tol, E.A. (1996) Animal models of intestinal and joint inflammation. Baillieres Clin Rheumatol 10: 55-76.
59. Schultsz, C., Moussa, M., van Ketel, R., Tytgat, G.N., and Dankert, J. (1997) Frequency of pathogenic and enteroadherent Escherichia coli in patients with inflammatory bowel disease and controls. J Clin Pathol 50: 573-579.
60. Schwan, W.R., Seifert, H.S., and Duncan, J.L. (1992) Growth conditions mediate differential transcription of fim genes involved in phase variation of type 1 pili. J Bacteriol 174: 2367-2375.
61. Shanahan, F. (2002) Crohn's disease. Lancet 359: 62-69.
62. Shin, S., and Park, C. (1995) Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 177: 4696-4702.
63. Testerman, T.L., Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Libby, S.J., and Fang, F.C. (2002) The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol Microbiol 43: 771-782.
64. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
65. Turner, A.K., Terry, T.D., Sack, D.A., Londono-Arcila, P., and Darsley, M.J. (2001) Construction and characterization of genetically defined aro omp mutants of enterotoxigenic Escherichia coli and preliminary studies of safety and immunogenicity in humans. Infect Immun 69: 4969-4979.
66. 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.