Anaerobic conditions promote expression of Sfp fimbriae and adherence of sorbitol-fermenting enterohemorrhagic Escherichia coli O157:NM to human intestinal epithelial cells

Applied and Environmental Microbiology

Volumn 74, Issue 4, 2008, Pages 1087-1093

  Müsken, Anne ^a   Bielaszewska, Martina ^a   Greune, Lilo ^a   Schweppe, Christian H ^a   Müthing, Johannes ^a   Schmidt, Herbert ^b   Schmidt, M Alexander ^a   Karch, Helge ^a   Zhang, Wenlan ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC DIGESTION; BIOLOGICAL ORGANS; CELL CULTURE; ESCHERICHIA COLI;

ANAEROBIC CONDITIONS; GENE CLUSTERS; INTESTINAL EPITHELIUM;

GENE EXPRESSION;

SORBITOL;

ANOXIC CONDITIONS; ANTIBODY; BACTERIUM; GENE EXPRESSION;

ARTICLE; BACTERIAL STRAIN; CELL STRAIN CACO 2; CORRELATION ANALYSIS; EPITHELIUM CELL; ESCHERICHIA COLI; FERMENTATION; FIMBRIA; GENETIC TRANSCRIPTION; HEMAGGLUTINATION; HUMAN; HUMAN CELL; INTESTINE CELL; LIQUID CULTURE; NONHUMAN; PROTEIN EXPRESSION; SIMULATION; UPREGULATION;

ANAEROBIOSIS; CACO-2 CELLS; DNA PRIMERS; ESCHERICHIA COLI O157; FERMENTATION; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HEMAGGLUTINATION TESTS; HUMANS; INTESTINAL MUCOSA; MICROSCOPY, ELECTRON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SORBITOL; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ESCHERICHIA COLI;

EID: 39649087593     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02496-07     Document Type: Article

References (54)

1. Aldick, T., M. Bielaszewska, W. Zhang, J. Brockmeyer, H. Schmidt, A. W. Friedrich, K. S. Kim, M. A. Schmidt, and H. Karch. 2007. Hemolysin from Shiga toxin-negative Escherichia coli O26 strains injures microvascular endothelium. Microbes Infect. 9:282-290.
2. Allison, L., S. Harding, M. Locking, K. Pollock, J. Evans, H. Knight, G. Foster, J. Cowden, and M. Hanson. 2006. Sorbitol-fermenting E. coli O157 in Scotland - laboratory investigation of an outbreak of haemolytic uraemic syndrome, abstr. P01.1.01, p. 4. In Abstracts of the 6th International Symposium on Shiga Toxin (Verocytotoxin)-Producing Escherichia coli Infections (VTEC 2006). Cambridge Publishing, West Leederville, Australia.
3. -. J. Infect. Dis. 179:1274-1277.
4. Ando, H., H. Abe, N. Sugimoto, and T. Tobe. 2007. Maturation of functional type III secretion machinery by activation of anaerobic respiration in enterohaemorrhagic Escherichia coli. Microbiology 153:464-473.
5. Bettelheim, K. A., M. Whipp, S. P. Djordjevic, and V. Ramachandran. 2002. First isolation outside Europe of sorbitol-fermenting verocytotoxigenic Escherichia coli (VTEC) belonging to O group O157. J. Med. Microbiol. 51:713-714.
6. Beumer, R. R., J. de Vries, and F. M. Rombouts. 1992. Campylobacter jejuni non-culturable coccoid cells. Int. J. Food Microbiol. 15:153-163.
7. - strains in the Czech Republic. J. Clin. Microbiol. 36:2135-2137.
8. Bielaszewska, M., P. I. Tarr, H. Karch, W. Zhang, and W. Mathys. 2005. Phenotypic and molecular analysis of tellurite resistance among enterohemorrhagic Escherichia coli O157:H7 and sorbitol-fermenting O157:NM clinical isolates. J. Clin. Microbiol. 43:452-454.
9. Bielaszewska, M., R. Köck, A. W. Friedrich, C. von Eiff, L. B. Zimmerhackl, H. Karch, and A. Mellmann. 2007. Shiga toxin-mediated hemolytic uremic syndrome: time to change the diagnostic paradigm? PLoS ONE 2:e1024. doi:10.1371/journal.pone.0001024.
10. Blumer, C., A. Kleefeld, D. Lehnen, M. Heintz, U. Dobrindt, G. Nagy, K. Michaelis, L. Emödy, T. Polen, R. Rachel, V. F. Wendisch, and G. Unden. 2005. Regulation of type 1 fimbriae synthesis and biofilm formation by the transcriptional regulator LrhA of Escherichia coli. Microbiology 151:3287-3298.
11. Brockmeyer, J., M. Bielaszewska, A. Fruth, M.-L. Bonn, A. Mellmann, H.-U. Humpf, and H. Karch. 2007. Subtypes of the plasmid-encoded serine protease EspP in Shiga toxin-producing Escherichia coli: distribution, secretion, and proteolytic activity. Appl. Environ. Microbiol. 73:6351-6359.
12. -. Infect. Immun. 69:4447-4457.
13. - strain 3072/96. Int. J. Med. Microbiol. 296:467-474.
14. Burland, V., Y. Shao, N. T. Perna, G. Plunkett, H. J. Sofia, and F. R. Blattner. 1998. The complete DNA sequence and analysis of the large virulence plasmid of Escherichia coli O157:H7. Nucleic Acids Res. 26:4196-4204.
15. Chong, Y., R. Fitzhenry, R Heuschkel, F. Torrente, G. Frankel, and A. D. Phillips. 2007. Human intestinal tissue tropism in Escherichia coli O157: H7 - initial colonization of terminal ileum and Peyer's patches and minimal colonic adhesion ex vivo. Microbiology 153:794-802.
16. Dowd, S. E., and H. Ishizaki. 2006. Microarray based comparison of two Escherichia coli O157:H7 lineages. BMC Microbiol. 6:30. doi:10.1186/1471-2180-6-30.
17. - human isolates from Finland. Clin. Microbiol. Infect. 12:634-641.
18. -. J. Clin. Microbiol. 42:4697-4701.
19. Friedrich, A. W., R. Köck, M. Bielaszewska, W. Zhang, H. Karch, and W. Mathys. 2005. Distribution of the urease gene cluster among and urease activities of enterohemorrhagic Escherichia coli O157 isolates from humans. J. Clin. Microbiol. 43:546-550.
20. Friedrich, A. W., S. Lu, M. Bielaszewska, R. Prager, P. Bruns, J. G. Xu, H. Tchäpe, and H. Karch. 2006. Cytolethal distending toxin in Escherichia coli O157:H7: spectrum of conservation, structure, and endothelial toxicity. J. Clin. Microbiol. 44:1844-1846.
21. Garmendia, J., and G. Frankel. 2005. Operon structure and gene expression of the espJ-tccP locus of enterohaemorrhagic Escherichia coli O157:H7. FEMS Microbiol. Lett. 247:137-145.
22. Gerber, A., H. Karch, F. Allerberger, H. M. Verweyen, and L. B. Zimmerhaekl. 2002. Clinical course and the role of Shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997-2000, in Germany and Austria: a prospective study. J. Infect. Dis. 186:493-500.
23. Guiney, D. G. 1997. Regulation of virulence gene expression by the host environment. J. Clin. Investig. 99:565-569.
24. Gunsalus, R. P., and S. J. Park. 1994. Aerobic-anaerobic gene regulation in Escherichia coli - control by the arcAB and fnr regulons. Res. Microbiol. 145:437-450.
25. -. Int. J. Med. Microbiol. 292:207-214.
26. - and O157:H7: characterization and evolutionary considerations. Infect. Immun. 71:3634-3638.
27. - from E. coli O157:H7. Appl. Environ. Microbiol. 71:4875-4878.
28. Kang, Y., K. D. Weber, Y. Qiu, P. J. Kiley, and F. R. Blattner. 2005. Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J. Bacteriol. 187:1135-1160.
29. -. J. Clin. Microbiol. 31:1200-1205.
30. Karch, H., P. I. Tarr, and M. Bielaszewska. 2005. Enterohaemorrhagic Escherichia coli in human medicine. Int. J. Med. Microbiol. 295:405-418.
31. Kim, S. O., K. Merchant, R. Nudelman., W. F. Bayer., T. Keng., J. DeAngelo, A. Hausladen, and J. S. Stamler. 2002. OxyR: a molecular code for redox-mediated signalling. Cell 109:383-396.
32. Klapproth, J. M., I. C. Scaletsky, B. P. McNamara, L. C. Lai, C. Malstrom, S. P. James, and M. S. Donnenberg. 2000. A large toxin from pathogenic Escherichia coli strains that inhibits lymphocyte activation. Infect. Immun. 68:2148-2155.
33. Krishnan, H. H., A. Ghosh, K. Paul, and R. Chowdhury. 2004. Effect of anaerobiosis on expression of virulence factors in Vibrio cholerae. Infect. Immun. 72:3961-3967.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Lee, J. H., and S. J. Choi. 2006. Isolation and characteristics of sorbitol-fermenting Escherichia coli O157 strains from cattle. Microbes Infect. 8:2021-2026.
36. Low, A. S., N. Holden, T. Rosser, A. J. Roe, C. Constantinidou, J. L. Hobman, D. G. Smith, J. C. Low, and D. L. Gally. 2006. Analysis of fimbrial gene clusters and their expression in enterohaemorrhagic Escherichia coli O157: H7. Environ. Microbiol. 8:1033-1047.
37. Mekalanos, J. J. 1992. Environmental signals controlling expression of virulence determinants in bacteria. J. Bacteriol. 174:1-7.
38. Müthing, J., I. Meisen, P. Bulau, M. Langer, K. Witthohn, H. Lentzen, U. Neumann, and J. Peter-Katalinić. 2004. Mistletoe lectin I is a sialic acid-specific lectin with strict preference to gangliosides and glycoproteins with terminal Neu5Acα2-6Galβ1-4GlcNAc residues. Biochemistry 43:2996-3007.
39. Nicholls, L., T. H. Grant, and R. M. Robins-Browne. 2000. Identification of a novel genetic locus that is required for in vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelial cells. Mol. Microbiol. 35:275-288.
40. Orth, D., K. Grif, M. P. Dierich, and R. Würzner. 2006. Sorbitol-fermenting Shiga toxin-producing Escherichia coli O157: indications for an animal reservoir. Epidemiol. Infect. 134:719-723.
41. Orth, D., K. Grit, M. P. Dierich, and R. Würzner. 2006. Prevalence, structure and expression of urease genes in Shiga toxin-producing Escherichia coli from humans and the environment. Int. J. Hyg. Environ. Health 209:513-520.
42. Orth, D., K. Grif, M. P. Dierich, and R. Würzner. 2007. Variability in tellurite resistance and the ter gene cluster among Shiga toxin-producing Escherichia coli isolated from humans, animals and food. Res. Microbiol. 158:105-111.
43. Overton, T. W., L. Griffiths, M. D. Patel, J. L. Hobman, C. W. Penn, J. A. Cole, and C. Constantinidou. 2006. Microarray analysis of gene regulation by oxygen, nitrate, nitrite, FNR, NarL and NarP during anaerobic growth of Escherichia coli: new insights into microbial physiology. Biochem. Soc. Trans. 34:104-107.
44. -: Untersuchungsergebnisse und Lehren für die Surveillance. Epidemiol. Bull. 22:171-175.
45. Rollenhagen, C., and D. Bumann. 2006. Salmonella enterica highly expressed genes are disease specific. Infect. Immun. 74:1649-1660.
46. Ruiz-Perez, F., J. Sheikh, S. Davis, E. C. Boedeker, and J. P. Nataro. 2004. Use of a continuous-flow anaerobic culture to characterize enteric virulence gene expression. Infect. Immun. 72:3793-3802.
47. Salmon, K., S. P. Hung, K. Mekjian, P. Baldi, G. W. Hatfield, and R. P. Gunsalus. 2003. Global gene expression profiling in Escherichia coli K12: the effects of oxygen availability and FNR. J. Biol Chem. 278:29837-29855.
48. Shaikh, N., N. J. Holt, J. R. Johnson, and P. I. Tarr. 2007. Fim operon variation in the emergence of enterohemorrhagic Escherichia coli: an evolutionary and functional analysis. FEMS Microbiol. Lett. 273:58-63.
49. Sperandio, V., J. L. Mellies, W. Nguyen, S. Shin, and J. B. Kaper. 1999. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 96:15196-15201.
50. Sperandio, V., A. G. Torres, B. Jarvis, J. P. Nataro, and J. B. Kaper. 2003. Bacteria-host communication: the language of hormones. Proc. Natl. Acad. Sci. USA 100:8951-8956.
51. Tarr, P. I., C. A. Gordon, and W. L. Chandler. 2005. Shiga toxin-producing Escherichia coli and the haemolytic uraemic syndrome. Lancet 365:1073-1086.
52. Tatsuno, I., M. Horie, H. Abe, T. Miki, K. Makino, H. Shinagawa, H. Taniguchi, S. Kamiya, T. Hayashi, and C. Sasakawa. 2001. toxB gene on pO157 of enterohemorrhagic Escherichia coli O157:H7 is required for full epithelial cell adherence phenotype. Infect. Immun. 69:6660-6669.
53. Torres, A. G., L. Milflores-Flores, J. G. Garcia-Gallegos, S. D. Patel, A. Best, R. M. La Ragione, Y. Martinez-Laguna, and M. J. Woodward. 2007. Environmental regulation and colonization attributes of the long polar fimbriae of Escherichia coli O157:H7. Int. J. Med. Microbiol. 297:177-185.
54. Vallet-Gely, I., J. S. Sharp, and S. L. Dove. 2007. Local and global regulators linking anaerobiosis to cupA fimbrial gene expression in Pseudomonas aeruginosa. J. Bacteriol. doi:10.1128/JB.01344-07.