RegA, an AraC-like protein, is a global transcriptional regulator that controls virulence gene expression in Citrobacter rodentium

Infection and Immunity

Volumn 76, Issue 11, 2008, Pages 5247-5256

  Hart, Emily ^a,b   Yang, Ji ^a,b   Tauschek, Marija ^a,b   Kelly, Michelle ^a   Wakefield, Matthew J ^c   Frankel, Gad ^d   Hartland, Elizabeth L ^a,b   Robins Browne, Roy M ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ROYAL CHILDREN'S HOSPITAL   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BICARBONATE; PROTEIN REGA; UNCLASSIFIED DRUG;

ADCA GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL VIRULENCE; CELL ADHESION; CITROBACTER RODENTIUM; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GENE FUSION; GENE INSERTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTESTINE INFECTION; KFCC GENE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; REGULON; SEQUENCE HOMOLOGY; TRANSPOSON;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CITROBACTER RODENTIUM; ENTEROBACTERIACEAE INFECTIONS; GENE EXPRESSION REGULATION, BACTERIAL; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 55849083511     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00770-08     Document Type: Article

References (54)

1. Autret, N., and A. Charbit. 2005. Lessons from signature-tagged mutagenesis on the infectious mechanisms of pathogenic bacteria. FEMS Microbiol. Rev. 29:703-717.
2. Barthold, S. W. 1980. The microbiology of transmissible murine colonic hyperplasia. Lab. Anim. Sci. 30:167-173.
3. Benz, I., and M. A. Schmidt. 1989. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect. Immun. 57:1506-1511.
4. Benz, I., and M. A. Schmidt. 1990. Diffuse adherence of enteropathogenic Escherichia coli strains. Res. Microbiol. 141:785-786.
5. Bhakdi, S., N. Mackman, G. Menestrina, L. Gray, F. Hugo, W. Seeger, and I. B. Holland. 1988. The hemolysin of Escherichia coli. Eur. J. Epidemiol. 4:135-143.
6. Bieber, D., S. W. Ramer, C. Y. Wu, W. J. Murray, T. Tobe, R. Fernandez, and G. K. Schoolnik. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:2114-2118.
7. Caron, J., L. M. Coffield, and J. R. Scott. 1989. A plasmid-encoded regulatory gene, rns, required for expression of the CS1 and CS2 adhesins of enterotoxigenic Escherichia coli. Proc. Natl. Acad. Sci. USA 86:963-967.
8. Caron, J., and J. R. Scott. 1990. A rns-like regulatory gene for colonization factor antigen I (CFA/I) that controls expression of CFA/I pilin. Infect. Immun. 58:874-878.
9. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
10. Deng, W., Y. Li, B. A. Vallance, and B. B. Finlay. 2001. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect. Immun. 69:6323-6335.
11. 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.
12. Finlay, B. B., and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169.
13. Frankel, G., A. D. Phillips, I. Rosenshine, G. Dougan, J. B. Kaper, and S. Knutton. 1998. Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol. Microbiol. 30:911-921.
14. Freter, R., P. C. O'Brien, and M. S. Macsai. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun. 34:234-240.
15. Gallegos, M. T., R. Schleif, A. Bairoch, K. Hofmann, and J. L. Ramos. 1997. Arac/XylS family of transcriptional regulators. Microbiol. Mol. Biol. Rev. 61:393-410.
16. Giron, J. A., A. S. Ho, and G. K. Schoolnik. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254:710-713.
17. 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.
18. Henderson, I. R., F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, and D. Ala'Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
19. Isaacson, R. E., B. Nagy, and H. W. Moon. 1977. Colonization of porcine small intestine by Escherichia coli: colonization and adhesion factors of pig enteropathogens that lack K88. J. Infect. Dis. 135:531-539.
20. Jones, G. W., and R. E. Isaacson. 1983. Proteinaceous bacterial adhesins and their receptors. Crit. Rev. Microbiol. 10:229-260.
21. Kelly, M., E. Hart, R. Mundy, O. Marches, S. Wiles, L. Badea, S. Luck, M. Tauschek, G. Frankel, R. M. Robins-Browne, and E. L. Hartland. 2006. Essential role of the type III secretion system effector NleB in colonization of mice by Citrobacter rodentium. Infect. Immun. 74:2328-2337.
22. Klemm, P., R. M. Vejborg, and O. Sherlock. 2006. Self-associating autotransporters, SAATs: functional and structural similarities. Int. J. Med. Microbiol. 296:187-195.
23. Laarmann, S., and M. A. Schmidt. 2003. The Escherichia coli AIDA autotransporter adhesin recognizes an integral membrane glycoprotein as receptor. Microbiology 149:1871-1882.
24. Lee, J. H., and R. E. Isaacson. 1995. Expression of the gene cluster associated with the Escherichia coli pilus adhesin K99. Infect. Immun. 63:4143-4149.
25. 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.
26. Martinez-Laguna, Y., E. Calva, and J. L. Puente. 1999. Autoactivation and environmental regulation of bfpT expression, the gene coding for the transcriptional activator of bfpA in enteropathogenic Escherichia coli. Mol. Microbiol. 33:153-166.
27. 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.
28. Mildiner-Earley, S., and V. L. Miller. 2006. Characterization of a novel porin involved in systemic Yersinia enterocolitica infection. Infect. Immun. 74: 4361-4365.
29. Miller, J. H. 1974. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
30. Mundy, R., D. Pickard, R. K. Wilson, C. P. Simmons, G. Dougan, and G. Frankel. 2003. Identification of a novel type IV pilus gene cluster required for gastrointestinal colonization of Citrobacter rodentium Mol. Microbiol. 48:795-809.
31. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
32. Nataro, J. P., D. Yikang, D. Yingkang, and K. Walker. 1994. AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J. Bacteriol. 176:4691-4699.
33. 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.
34. Nishi, J., J. Sheikh, K. Mizuguchi, B. Luisi, V. Burland, A. Boutin, D. J. Rose, F. R. Blattner, and J. P. Nataro. 2003. The export of coat protein from enteroaggregative Escherichia coli by a specific ATP-binding cassette transporter system. J. Biol. Chem. 278:45680-45689.
35. Pilonieta, M. C., M. D. Bodero, and G. P. Munson. 2007. CfaD-dependent expression of a novel extracytoplasmic protein from enterotoxigenic Escherichia coli. J. Bacteriol. 189:5060-5067.
36. 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. 54:1117-1133.
37. Praszkier, J., I. W. Wilson, and A. J. Pittard. 1992. Mutations affecting translational coupling between the rep genes of an IncB miniplasmid. J. Bacteriol. 174:2376-2383.
38. Russell, R. M., F. C. Sharp, D. A. Rasko, and V. Sperandio. 2007. QseA and GrlR/GrlA regulation of the locus of enterocyte effacement genes in enterohemorrhagic Escherichia coli. J. Bacteriol. 189:5387-5392.
39. 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.
40. Schauer, D. B., and S. Falkow. 1993. Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect. Immun. 61:2486-2492.
41. Schembri, M. A., D. Dalsgaard, and P. Klemm. 2004. Capsule shields the function of short bacterial adhesins. J. Bacteriol. 186:1249-1257.
42. Shea, J. E., J. D. Santangelo, and R. G. Feldman. 2000. Signature-tagged mutagenesis in the identification of virulence genes in pathogens. Curr. Opin. Microbiol. 3:451-458.
43. Sheikh, J., J. R. Czeczulin, S. Harrington, S. Hicks, I. R. Henderson, C. Le Bouguenec, P. Gounon, A. Phillips, and J. P. Nataro. 2002. A novel dispersin protein in enteroaggregative Escherichia coli. J. Clin. Investig. 110:1329-1337.
44. Sherlock, O., M. A. Schembri, A. Reisner, and P. Klemm. 2004. Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J. Bacteriol. 186:8058-8065.
45. Smyth, G. K. 2005. Limma: linear models for microarray data, p. 397-420. In R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, and W. Huber (ed.), Bioinformatics and computational biology solutions using R and Bioconductor. Springer, New York, NY.
46. Smyth, G. K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:article 3.
47. Smyth, G. K., and T. Speed. 2003. Normalization of cDNA microarray data. Methods 31:265-273.
48. Tobe, T., and C. Sasakawa. 2001. Role of bundle-forming pilus of enteropathogenic Escherichia coli in host cell adherence and in microcolony development. Cell. Microbiol. 3:579-585.
49. Twigg, A. J., and D. Sherratt. 1980. Trans-complementable copy-number mutants of plasmid ColE1. Nature 283:216-218.
50. Ulett, G. C., R. I. Webb, and M. A. Schembri. 2006. Antigen-43-mediated autoaggregation impairs motility in Escherichia coli. Microbiology 152: 2101-2110.
51. Vial, P. A., J. J. Mathewson, H. L. DuPont, L. Guers, and M. M. Levine. 1990. Comparison of two assay methods for patterns of adherence to HEp-2 cells of Escherichia coli from patients with diarrhea. J. Clin. Microbiol. 28:882-885.
52. Wiles, S., S. Clare, J. Harker, A. Huett, D. Young, G. Dougan, and G. Frankel. 2005. Corrigendum: organ specificity, colonization and clearance dynamics in vivo following oral challenge with the murine pathogen Citrobacter rodentium. Cell. Microbiol. 7:459.
53. Yang, J., E. Hart, M. Tauschek, G. D. Price, E. L. Hartland, R. A. Strugnell, and R. Robins-Browne. 2008. Bicarbonate-mediated transcriptional activation of divergent operons by the virulence regulatory protein, RegA, from Citrobacter rodentium Mol. Microbiol. 68:314-327.
54. Zhu, J., and J. J. Mekalanos. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5:647-656.