RegR virulence regulon of rabbit-specific enteropathogenic Escherichia coli strain E22

Infection and Immunity

Volumn 81, Issue 4, 2013, Pages 1078-1089

  Srikhanta, Yogitha N ^a   Hocking, Dianna M ^a   Praszkier, Judyta ^a,d   Wakefield, Matthew J ^a,b   Robins Browne, Roy M ^a,c   Yang, Ji ^a   Tauschek, Marija ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

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

^c ROYAL CHILDREN'S HOSPITAL   (Australia)

^d HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ARAC PROTEIN; REGR PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CITROBACTER RODENTIUM; ENTEROPATHOGENIC ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENE SILENCING; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEOMICS; RABBIT; REGULON; TRANSCRIPTION INITIATION; UPREGULATION;

ANIMALS; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MICROARRAY ANALYSIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEOME; RABBITS; REGULON; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

EID: 84875543266     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01325-12     Document Type: Article

References (69)

1. Fagundes-Neto U, Scaletsky IC. 2000. The gut at war: the consequences of enteropathogenic Escherichia coli infection as a factor of diarrhea and malnutrition. Sao Paulo Med. J. 118:21-29.
2. Robins-Browne RM. 1987. Traditional enteropathogenic Escherichia coli of infantile diarrhea. Rev. Infect. Dis. 9:28-53.
3. Kaper JB. 1996. Defining EPEC. Rev. Microbiol. Sao Paulo. 27:130-133.
4. Trabulsi LR, Keller R, Tardelli Gomes TA. 2002. Typical and atypical enteropathogenic Escherichia coli. Emerg. Infect. Dis. 8:508-513.
5. Finlay BB, Rosenshine I, Donnenberg MS, Kaper JB. 1992. Cytoskeletal composition of attaching and effacing lesions associated with enteropathogenic Escherichia coli adherence to HeLa cells. Infect. Immun. 60: 2541-2543.
6. Frankel G, Phillips AD, Rosenshine I, Dougan G, Kaper JB, Knutton S. 1998. Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol. Microbiol. 30:911-921.
7. Elliott SJ, Sperandio V, Giron JA, Shin S, Mellies JL, Wainwright L, Hutcheson SW, McDaniel TK, Kaper JB. 2000. The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEEand non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 68:6115-6126.
8. McDaniel TK, Kaper JB. 1997. A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol. Microbiol. 23:399-407.
9. Tauschek M, Strugnell RA, Robins-Browne RM. 2002. Characterization and evidence of mobilization of the LEE pathogenicity island of rabbitspecific strains of enteropathogenic Escherichia coli. Mol. Microbiol. 44: 1533-1550.
10. Wong AR, Pearson JS, Bright MD, Munera D, Robinson KS, Lee SF, Frankel G, Hartland EL. 2011. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol. Microbiol. 80:1420-1438.
11. Bieber D, Ramer SW, Wu CY, Murray WJ, Tobe T, Fernandez R, Schoolnik GK. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:2114-2118.
12. Moura RA, Sircili MP, Leomil L, Matte MH, Trabulsi LR, Elias WP, Irino K, Pestana de Castro AF. 2009. Clonal relationship among atypical enteropathogenic Escherichia coli strains isolated from different animal species and humans. Appl. Environ. Microbiol. 75:7399-7408.
13. Johnson TJ, Nolan LK. 2009. Pathogenomics of the virulence plasmids of Escherichia coli. Microbiol. Mol. Biol. Rev. 73:750-774.
14. Marches O, Nougayrede JP, Boullier S, Mainil J, Charlier G, Raymond I, Pohl P, Boury M, De Rycke J, Milon A, Oswald E. 2000. Role of Tir and intimin in the virulence of rabbit enteropathogenic Escherichia coli serotype O103:H2. Infect. Immun. 68:2171-2182.
15. Milon A, Oswald E, De Rycke J. 1999. Rabbit EPEC: a model for the study of enteropathogenic Escherichia coli. Vet. Res. 30:203-219.
16. Abe A, Heczko U, Hegele RG, Brett Finlay B. 1998. Two enteropathogenic Escherichia coli type III secreted proteins, EspA and EspB, are virulence factors. J. Exp. Med. 188:1907-1916.
17. Ochoa TJ, Contreras CA. 2011. Enteropathogenic Escherichia coli infection in children. Curr. Opin. Infect. Dis. 24:478-483.
18. Nguyen RN, Taylor LS, Tauschek M, Robins-Browne RM. 2006. Atypical enteropathogenic Escherichia coli infection and prolonged diarrhea in children. Emerg. Infect. Dis. 12:597-603.
19. Levine MM, Nataro JP, Karch H, Baldini MM, Kaper JB, Black RE, Clements ML, O'Brien AD. 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.
20. Yang J, Tauschek M, Robins-Browne RM. 2011. Control of bacterial virulence by AraC-like regulators that respond to chemical signals. Trends Microbiol. 19:128-135.
21. Mahan MJ, Slauch JM, Mekalanos JJ. 1996. Environmental regulation of virulence gene expression in Escherichia, Salmonella, and Shigella spp., p 2803-2815. In Neidhardt FC et al (ed), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, DC.
22. Stoebel DM, Free A, Dorman CJ. 2008. Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology 154:2533-2545.
23. Gomez-Duarte OG, Kaper JB. 1995. A plasmid-encoded regulatory region activates chromosomal eaeA expression in enteropathogenic Escherichia coli. Infect. Immun. 63:1767-1776.
24. Murphree D, Froehlich B, Scott JR. 1997. Transcriptional control of genes encoding CS1 pili: negative regulation by a silencer and positive regulation by Rns. J. Bacteriol. 179:5736-5743.
25. Nataro JP, Yikang D, Yingkang D, Walker K. 1994. AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J. Bacteriol. 176:4691-4699.
26. DiRita VJ, Parsot C, Jander G, Mekalanos JJ. 1991. Regulatory cascade controls virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 88: 5403-5407.
27. Gallegos MT, Schleif R, Bairoch A, Hofmann K, Ramos JL. 1997. Arac/XylS family of transcriptional regulators. Microbiol. Mol. Biol. Rev. 61:393-410.
28. Hart E, Yang J, Tauschek M, Kelly M, Wakefield MJ, Frankel G, Hartland EL, Robins-Browne RM. 2008. RegA, an AraC-like protein, is a global transcriptional regulator that controls virulence gene expression in Citrobacter rodentium. Infect. Immun. 76:5247-5256.
29. Deng W, Li Y, Vallance BA, Finlay BB. 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.
30. Schauer DB, Falkow S. 1993. Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect. Immun. 61:2486-2492.
31. Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, Vazquez A, Barba J, Ibarra JA, O'Donnell P, Metalnikov P, Ashman K, Lee S, Goode D, Pawson T, Finlay BB. 2004. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc. Natl. Acad. Sci. U. S. A. 101:3597-3602.
32. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. 2005. Citrobacter rodentium of mice and man. Cell. Microbiol. 7:1697-1706.
33. Frankel G, Phillips AD, Novakova M, Field H, Candy DC, Schauer DB, Douce G, Dougan G. 1996. Intimin from enteropathogenic Escherichia coli restores murine virulence to a Citrobacter rodentium eaeA mutant: induction of an immunoglobulin A response to intimin and EspB. Infect. Immun. 64:5315-5325.
34. Tauschek M, Yang J, Hocking D, Azzopardi K, Tan A, Hart E, Praszkier J, Robins-Browne RM. 2010. Transcriptional analysis of the grlRA virulence operon from Citrobacter rodentium. J. Bacteriol. 192:3722-3734.
35. Yang J, Hart E, Tauschek M, Price GD, Hartland EL, Strugnell RA, Robins-Browne RM. 2008. Bicarbonate-mediated transcriptional activation of divergent operons by the virulence regulatory protein, RegA, from Citrobacter rodentium. Mol. Microbiol. 68:314-327.
36. Datsenko KA, Wanner BL. 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.
37. Chalker AF, Minehart HW, Hughes NJ, Koretke KK, Lonetto MA, Brinkman KK, Warren PV, Lupas A, Stanhope MJ, Brown JR, Hoffman PS. 2001. Systematic identification of selective essential genes in Helicobacter pylori by genome prioritization and allelic replacement mutagenesis. J. Bacteriol. 183:1259-1268.
38. Smyth G. 2005. limma: linear models for microarray data, p 397-420. In Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S (ed), Bioinformatics and computational biology solutions using R and Bioconductor. Springer, New York, NY.
39. Smyth GK. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:Article 3.
40. Smyth GK, Speed T. 2003. Normalization of cDNA microarray data. Methods 31:265-273.
41. Yang J, Tauschek M, Strugnell R, Robins-Browne RM. 2005. The H-NS protein represses transcription of the eltAB operon, which encodes heatlabile enterotoxin in enterotoxigenic Escherichia coli, by binding to regions downstream of the promoter. Microbiology 151:1199-1208.
42. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 43. Miller JH. 1974. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Plainview, NY.
43. Miller JH. 1974. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Plainview, NY.
44. Adams LM, Simmons CP, Rezmann L, Strugnell RA, Robins-Browne RM. 1997. Identification and characterization of a K88- and CS31A-like operon of a rabbit enteropathogenic Escherichia coli strain which encodes fimbriae involved in the colonization of rabbit intestine. Infect. Immun. 65:5222-5230.
45. Scaletsky IC, Michalski J, Torres AG, Dulguer MV, Kaper JB. 2005. Identification and characterization of the locus for diffuse adherence, which encodes a novel afimbrial adhesin found in atypical enteropathogenic Escherichia coli. Infect. Immun. 73:4753-4765.
46. Edwards RA, Matlock BC, Heffernan BJ, Maloy SR. 2001. Genomic analysis and growth-phase-dependent regulation of the SEF14 fimbriae of Salmonella enterica serovar Enteritidis. Microbiology 147:2705-2715.
47. Tan A, Yang J, Tauschek M, Praszkier J, Robins-Browne RM. 2011. Autogenous transcriptional regulation of the regA gene, encoding an AraC-like, essential virulence regulator in Citrobacter rodentium. J. Bacteriol. 193:1777-1782.
48. Zhu C, Feng S, Thate TE, Kaper JB, Boedeker EC. 2006. Towards a vaccine for attaching/effacing Escherichia coli: a LEE encoded regulator (ler) mutant of rabbit enteropathogenic Escherichia coli is attenuated, immunogenic, and protects rabbits from lethal challenge with the wild-type virulent strain. Vaccine 24:3845-3855.
49. Henderson IR, Navarro-Garcia F, Nataro JP. 1998. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:370-378.
50. Yen YT, Kostakioti M, Henderson IR, Stathopoulos C. 2008. Common themes and variations in serine protease autotransporters. Trends Microbiol. 16:370-379.
51. Kobayashi RK, Gaziri LC, Vidotto MC. 2010. Functional activities of the Tsh protein from avian pathogenic Escherichia coli (APEC) strains. J. Vet. Sci. 11:315-319.
52. Skyberg JA, Johnson TJ, Johnson JR, Clabots C, Logue CM, Nolan LK. 2006. Acquisition of avian pathogenic Escherichia coli plasmids by a commensal E. coli isolate enhances its abilities to kill chicken embryos, grow in human urine, and colonize the murine kidney. Infect. Immun. 74:6287-6292.
53. Dozois CM, Dho-Moulin M, Bree A, Fairbrother JM, Desautels C, Curtiss R, 3rd. 2000. Relationship between the Tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the Tsh genetic region. Infect. Immun. 68:4145-4154.
54. Navarro-Garcia F, Canizalez-Roman A, Sui BQ, Nataro JP, Azamar Y. 2004. The serine protease motif of EspC from enteropathogenic Escherichia coli produces epithelial damage by a mechanism different from that of Pet toxin from enteroaggregative E. coli. Infect. Immun. 72:3609-3621.
55. Xicohtencatl-Cortes J, Saldana Z, Deng W, Castaneda E, Freer E, Tarr PI, Finlay BB, Puente JL, Giron JA. 2010. Bacterial macroscopic ropelike fibers with cytopathic and adhesive properties. J. Biol. Chem. 285: 32336-32342.
56. Vidal JE, Navarro-Garcia F. 2008. EspC translocation into epithelial cells by enteropathogenic Escherichia coli requires a concerted participation of type V and III secretion systems. Cell Microbiol. 10:1975-1986.
57. Ogunniyi AD, Kotlarski I, Morona R, Manning PA. 1997. Role of SefA subunit protein of SEF14 fimbriae in the pathogenesis of Salmonella enterica serovar Enteritidis. Infect. Immun. 65:708-717.
58. Edwards RA, Schifferli DM, Maloy SR. 2000. A role for Salmonella fimbriae in intraperitoneal infections. Proc. Natl. Acad. Sci. U. S. A. 97: 1258-1262.
59. Abuaita BH, Withey JH. 2009. Bicarbonate Induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect. Immun. 77: 4111-4120.
60. Morin N, Tirling C, Ivison SM, Kaur AP, Nataro JP, Steiner TS. 2010. Autoactivation of the AggR regulator of enteroaggregative Escherichia coli in vitro and in vivo. FEMS Immunol. Med. Microbiol. 58:344-355.
61. Munson GP, Holcomb LG, Scott JR. 2001. Novel group of virulence activators within the AraC family that are not restricted to upstream binding sites. Infect. Immun. 69:186-193.
62. Nunez MF, Pellicer MT, Badia J, Aguilar J, Baldoma L. 2001. The gene yghK linked to the glc operon of Escherichia coli encodes a permease for glycolate that is structurally and functionally similar to L-lactate permease. Microbiology 147:1069-1077.
63. Krejany EO, Grant TH, Bennett-Wood V, Adams LM, Robins-Browne RM. 2000. Contribution of plasmid-encoded fimbriae and intimin to capacity of rabbit-specific enteropathogenic Escherichia coli to attach to and colonize rabbit intestine. Infect. Immun. 68:6472-6477.
64. Tennant SM, Tauschek M, Azzopardi K, Bigham A, Bennett-Wood V, Hartland EL, Qi W, Whittam TS, Robins-Browne RM. 2009. Characterisation of atypical enteropathogenic E. coli strains of clinical origin. BMC Microbiol. 9:117.
65. Tobes R, Ramos JL. 2002. AraC-XylS database: a family of positive transcriptional regulators in bacteria. Nucleic Acids Res. 30:318-321.
66. Casadaban MJ. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104:541-555.
67. Chang AC, Cohen SN. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
68. Posfai G, Koob MD, Kirkpatrick HA, Blattner FR. 1997. Versatile insertion plasmids for targeted genome manipulations in bacteria: isolation, deletion, and rescue of the pathogenicity island LEE of the Escherichia coli O157:H7 genome. J. Bacteriol. 179:4426-4428.
69. Yang J, Baldi DL, Tauschek M, Strugnell RA, Robins-Browne RM. 2007. Transcriptional regulation of the yghJ-pppA-yghG-gspCDEFGHIJKLM cluster, encoding the type II secretion pathway in enterotoxigenic Escherichia coli. J. Bacteriol. 189:142-150.