Dual regulatory pathways of flagellar gene expression by ClpXP protease in enterohaemorrhagic Escherichia coli

Microbiology

Volumn 157, Issue 11, 2011, Pages 3094-3103

  Kitagawa, Ryo ^a   Takaya, Akiko ^a   Yamamoto, Tomoko ^a  

^a CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CLPXP PROTEASE; FLHC PROTEIN; FLHD PROTEIN; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CELL MUTANT; DOWN REGULATION; ENTEROHEMORRHAGIC ESCHERICHIA COLI; FLAGELLUM; GENE EXPRESSION; GENETIC TRANSCRIPTION; LOCUS OF ENTEROCYTE EFFACEMENT; NONHUMAN; OPERON; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ENDOPEPTIDASE CLP; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; MUTATION; PROMOTER REGIONS, GENETIC; REGULON; TRANS-ACTIVATORS;

ENTEROBACTERIACEAE; ESCHERICHIA COLI; SALMONELLA;

EID: 80155200877     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.051151-0     Document Type: Article

References (42)

1. Abe, H., Tatsuno, I., Tobe, T., Okutani, A. & Sasakawa, C. (2002). Bicarbonate ion stimulates the expression of locus of enterocyte effacement-encoded genes in enterohemorrhagic Escherichia coli O157:H7. Infect Immun 70, 3500-3509.
2. Akashi, S., Joh, K., Mori, T., Tsuji, A., Ito, H., Hoshi, H., Hayakawa, T., Ihara, J., Abe, T. & other authors (1994). A severe outbreak of haemorrhagic colitis and haemolytic uraemic syndrome associated with Escherichia coli O157:H7 in Japan. Eur J Pediatr 153, 650-655.
3. Berin, M. C., Darfeuille-Michaud, A., Egan, L. J., Miyamoto, Y. & Kagnoff, M. F. (2002). Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-κB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell Microbiol 4, 635-648.
4. Bustamante, V. H., Santana, F. J., Calva, E. & Puente, J. L. (2001). Transcriptional regulation of type III secretion genes in enteropathogenic Escherichia coli: Ler antagonizes H-NS-dependent repression. Mol Microbiol 39, 664-678.
5. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158, 9-14.
6. Cummings, L. A., Wilkerson, W. D., Bergsbaken, T. & Cookson, B. T. (2006). In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted. Mol Microbiol 61, 795-809.
7. Datsenko, K. A. & Wanner, B. L. (2000). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640-6645.
8. Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vázquez, A., Barba, J., Ibarra, J. A., O'Donnell, P. & other authors (2004). Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci U S A 101, 3597-3602.
9. Donnenberg, M. S. & Kaper, J. B. (1991). Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59, 4310-4317.
10. Fontaine, F., Stewart, E. J., Lindner, A. B. & Taddei, F. (2008). Mutations in two global regulators lower individual mortality in Escherichia coli. Mol Microbiol 67, 2-14.
11. Francez-Charlot, A., Laugel, B., Van Gemert, A., Dubarry, N., Wiorowski, F., Castanié-Cornet, M. P., Gutierrez, C. & Cam, K. (2003). RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol Microbiol 49, 823-832.
12. Friedberg, D., Umanski, T., Fang, Y. & Rosenshine, I. (1999). Hierarchy in the expression of the locus of enterocyte effacement genes of enteropathogenic Escherichia coli. Mol Microbiol 34, 941-952.
13. Gamer, J., Bujard, H. & Bukau, B. (1992). Physical interaction between heat shock proteins DnaK, DnaJ, and GrpE and the bacterial heat shock transcription factor σ32. Cell 69, 833-842.
14. Gottesman, S., Roche, E., Zhou, Y. & Sauer, R. T. (1998). The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 12, 1338-1347.
15. Grant, A. J., Farris, M., Alefounder, P., Williams, P. H., Woodward, M. J. & O'Connor, C. D. (2003). Co-ordination of pathogenicity island expression by the BipA GTPase in enteropathogenic Escherichia coli (EPEC). Mol Microbiol 48, 507-521.
16. Habdas, B. J., Smart, J., Kaper, J. B. & Sperandio, V. (2010). The LysR-type transcriptional regulator QseD alters type three secretion in enterohemorrhagic Escherichia coli and motility in K-12 Escherichia coli. J Bacteriol 192, 3699-3712.
17. Iyoda, S. & Watanabe, H. (2005). ClpXP protease controls expression of the type III protein secretion system through regulation of RpoS and GrlR levels in enterohemorrhagic Escherichia coli. J Bacteriol 187, 4086-4094.
18. Iyoda, S., Koizumi, N., Satou, H., Lu, Y., Saitoh, T., Ohnishi, M. & Watanabe, H. (2006). The GrlR-GrlA regulatory system coordinately controls the expression of flagellar and LEE-encoded type III protein secretion systems in enterohemorrhagic Escherichia coli. J Bacteriol 188, 5682-5692.
19. Lehnen, D., Blumer, C., Polen, T., Wackwitz, B., Wendisch, V. F. & Unden, G. (2002). LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol Microbiol 45, 521-532.
20. Macnab, R. M. (1996). Flagella and motility. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, pp. 123-145. Edited by F. C. Neidhardt, R., III, H. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter & H. E. Umbarger.Washington, D.C.: American Society for Microbiology.
21. Macnab, R. M. (2003). How bacteria assemble flagella. Annu Rev Microbiol 57, 77-100.
22. Mahajan, A., Currie, C. G., Mackie, S., Tree, J., McAteer, S., McKendrick, I., McNeilly, T. N., Roe, A., La Ragione, R. M. & other authors (2009). An investigation of the expression and adhesion function of H7 flagella in the interaction of Escherichia coli O157:H7 with bovine intestinal epithelium. Cell Microbiol 11, 121-137.
23. Ortega, J., Singh, S. K., Ishikawa, T., Maurizi, M. R. & Steven, A. C. (2000). Visualization of substrate binding and translocation by the ATP-dependent protease, ClpXP. Mol Cell 6, 1515-1521.
24. Schneider, K. & Beck, C. F. (1986). Promoter-probe vectors for the analysis of divergently arranged promoters. Gene 42, 37-48.
25. Shi, W., Li, C., Louise, C. J. & Adler, J. (1993). Mechanism of adverse conditions causing lack of flagella in Escherichia coli. J Bacteriol 175, 2236-2240.
26. Shin, S. & Park, C. (1995). Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 177, 4696-4702.
27. Soutourina, O., Kolb, A., Krin, E., Laurent-Winter, C., Rimsky, S., Danchin, A. & Bertin, P. (1999). Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol 181, 7500-7508.
28. Soutourina, O. A., Krin, E., Laurent-Winter, C., Hommais, F., Danchin, A. & Bertin, P. N. (2002). Regulation of bacterial motility in response to low pH in Escherichia coli: the role of H-NS protein. Microbiology 148, 1543-1551.
29. Sperandio, V., Torres, A. G. & Kaper, J. B. (2002). Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43, 809-821.
30. Takaya, A., Matsui, M., Tomoyasu, T., Kaya, M. & Yamamoto, T. (2006). The DnaK chaperone machinery converts the native FlhD2C2 hetero-tetramer into a functional transcriptional regulator of flagellar regulon expression in Salmonella. Mol Microbiol 59, 1327-1340.
31. Tomoyasu, T., Ohkishi, T., Ukyo, Y., Tokumitsu, A., Takaya, A., Suzuki, M., Sekiya, K., Matsui, H., Kutsukake, K. & Yamamoto, T. (2002). The ClpXP ATP-dependent protease regulates flagellum synthesis in Salmonella enterica serovar typhimurium. J Bacteriol 184, 645-653.
32. Tomoyasu, T., Takaya, A., Isogai, E. & Yamamoto, T. (2003). Turnover of FlhD and FlhC, master regulator proteins for Salmonella flagellum biogenesis, by the ATP-dependent ClpXP protease. Mol Microbiol 48, 443-452.
33. Tomoyasu, T., Takaya, A., Handa, Y., Karata, K. & Yamamoto, T. (2005). ClpXP controls the expression of LEE genes in enterohaemorrhagic Escherichia coli. FEMS Microbiol Lett 253, 59-66.
34. Umanski, T., Rosenshine, I. & Friedberg, D. (2002). Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 148, 2735-2744.
35. Vazquez-Juarez, R. C., Kuriakose, J. A., Rasko, D. A., Ritchie, J. M., Kendall, M. M., Slater, T. M., Sinha, M., Luxon, B. A., Popov, V. L. & other authors (2008). CadA negatively regulates Escherichia coli O157:H7 adherence and intestinal colonization. Infect Immun 76, 5072-5081.
36. Wada, T., Morizane, T., Abo, T., Tominaga, A., Inoue-Tanaka, K. & Kutsukake, K. (2011). EAL domain protein YdiV acts as an anti-FlhD4C2 factor responsible for nutritional control of the flagellar regulon in Salmonella enterica serovar Typhimurium. J Bacteriol 193, 1600-1611.
37. Wei, B. L., Brun-Zinkernagel, A. M., Simecka, J. W., Prüß, B. M., Babitzke, P. & Romeo, T. (2001). Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40, 245-256.
38. Wozniak, C. E., Lee, C. & Hughes, K. T. (2009). T-POP array identifies EcnR and PefI-SrgD as novel regulators of flagellar gene expression. J Bacteriol 191, 1498-1508.
39. Yona-Nadler, C., Umanski, T., Aizawa, S., Friedberg, D. & Rosenshine, I. (2003). Integration host factor (IHF) mediates repression of flagella in enteropathogenic and enterohaemorrhagic Escherichia coli. Microbiology 149, 877-884.
40. S for degradation by ClpXP. Genes Dev 15, 627-637.
41. Zhou, X., Girón, J. A., Torres, A. G., Crawford, J. A., Negrete, E., Vogel, S. N. & Kaper, J. B. (2003). Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect Immun 71, 2120-2129.
42. Zhou, X., Meng, X. & Sun, B. (2008). An EAL domain protein and cyclic AMP contribute to the interaction between the two quorum sensing systems in Escherichia coli. Cell Res 18, 937-948.