Escherichia coli O157:H7 is a human pathogen that was first identified from a foodborne outbreak in 1982, and in the 25 years that followed, many new strains were identified and emerged in numerous outbreaks of human disease. Extensive research has been conducted to identify virulence factor genes involved in the pathogenesis of E. coli O157:H7 and many genome sequences of E. coli O157:H7 strains have become available to the scientific community. Here, we provide a comprehensive overview of the research that has been conducted over the first 25 years to identify 394 known or putative virulence factor genes present in the genomes of E. coli O157:H7 strains. Finally, an examination of the conservation of these 394 virulence factor genes across additional genomes of E. coli O157:H7 is provided which summarizes the first 25 years and 13 genomes of this human pathogen.
Riley, L.W., Remis, R.S., Helgerson, S.D., McGee, H.B., Wells, J.G., Davis, B.R., Hebert, R.J., Olcott, E.S., Johnson, L.M., Hargrett, N.T., Blake, P.A. and Cohen, M.L. (1983) Hemorrhagic Colitis Associated with a Rare Escherichia coli Serotype. The New England Journal of Medicine, 308, 681-685. http://dx.doi.org/10.1056/NEJM198303243081203
Michino, H., Araki, K., Minami, S., Takaya, S., Sakai, N., Miyazaki, M., Ono, A. and Yanagawa, H. (1999) Massive Outbreak of Escherichia coli O157:H7 Infection in Schoolchildren in Sakai City, Japan, Associated with Consumption of White Radish Sprouts. American Journal of Epidemiology, 150, 787-796. http://dx.doi.org/10.1093/oxfordjournals.aje.a010082
Fukushima, H., Hashizume, T., Morita, Y., Tanaka, J., Azuma, K., Mizumoto, Y., Kaneno, M., Matsu-Ura, M.O., Konma, K. and Kitani, T. (1999) Clinical Experiences in Sakai City Hospital during the Massive Outbreak of Enterohemorrhagic Escherichia coli O157 Infections in Sakai City, 1996. Pediatrics International, 41, 213-217. http://dx.doi.org/10.1093/oxfordjournals.aje.a010082
Higami, S., Nishimoto, K., Kawamura, T., Tsuruhara, T., Isshiki, G. and Ookita, A. (1998) Retrospective Analysis of the Relationship between HUS Incidence and Antibiotics among Patients with Escherichia coli O157 Enterocolitis in the Sakai Outbreak. Kansenshogaku Zasshi, 72, 266-272.
Hayashi, T., Makino, K., Ohnishi, M., Kurokawa, K., Ishii, K., Yokoyama, K., Han, C.G., Ohtsubo, E., Nakayama, K., Murata, T., Tanaka, M., Tobe, T., Iida, T., Takami, H., Honda, T., Sasakawa, C., Ogasawara, N., Yasunaga, T., Kuhara, S., Shiba, T., Hattori, M. and Shinagawa, H. (2001) Complete Genome Sequence of Enterohemorrhagic Escherichia coli O157:H7 and Genomic Comparison with a Laboratory Strain K-12. DNA Research, 8, 11-22. http://dx.doi.org/10.1093/dnares/8.1.11
Spears, K.J., Roe, A.J. and Gally, D.L. (2006) A Comparison of Enteropathogenic and Enterohaemorrhagic Escherichia coli Pathogenesis. FEMS Microbiology Letters, 255, 187-202. http://dx.doi.org/10.1111/j.1574-6968.2006.00119.x
Low, A.S., Holden, N., Rosser, T., Roe, A.J., Constantinidou, C., Hobman, J.L., Smith, D.G.E., Low, J.C. and Gally, D.L. (2006) Analysis of Fimbrial Gene Clusters and Their Expression in Enterohaemorrhagic Escherichia coli O157: H7. Environmental Microbiology, 8, 1033-1047. http://dx.doi.org/10.1111/j.1462-2920.2006.00995.x
Giron, J.A., Torres, A.G., Freer, E. and Kaper, J.B. (2002) The Flagella of Enteropathogenic Escherichia coli Mediate Adherence to Epithelial Cells. Molecular Microbiology, 44, 361-379. http://dx.doi.org/10.1046/j.1365-2958.2002.02899.x
Torres, A.G., Kanack, K.J., Tutt, C.B., Popov, V. and Kaper, J.B. (2004) Characterization of the Second Long Polar (LP) Fimbriae of Escherichia coli O157: H7 and Distribution of LP Fimbriae in Other Pathogenic E. coli Strains. FEMS Microbiology Letters, 238, 333-344.
Torres, A.G., Milflores-Flores, L., Garcia-Gallegos, J.G., Patel, S.D., Best, A., La Ragione, R.M., Martinez-Laguna, Y. and Woodward, M.J. (2007) Environmental Regulation and Colonization Attributes of the Long Polar Fimbriae (LPF) of Escherichia coli O157: H7. International Journal of Medical Microbiology, 297, 177-185. http://dx.doi.org/10.1016/j.ijmm.2007.01.005
Dorsey, C.W., Laarakker, M.C., Humphries, A.D., Weening, E.H. and Baumler, A.J. (2005) Salmonella enterica Serotype Typhimurium MisL Is an Intestinal Colonization Factor That Binds Fibronectin. Molecular Microbiology, 57, 196-211. http://dx.doi.org/10.1111/j.1365-2958.2005.04666.x
De Buck, J., Van Immerseel, F., Haesebrouck, F. and Ducatelle, R. (2004) Effect of Type 1 Fimbriae of Salmonella enterica Serotype Enteritidis on Bacteraemia and Reproductive Tract Infection in Laying Hens. Avian Pathology, 33, 314-320. http://dx.doi.org/10.1080/0307945042000220561
Xicohtencatl-Cortes, J., Monteiro-Neto, V., Ledesma, M.A., Jordan, D.M., Francetic, O., Kaper, J.B., Puente, J.L. and Giron, J.A. (2007) Intestinal Adherence Associated with Type IV Pili of Enterohemorrhagic Escherichia coli O157:H7. The Journal of Clinical Investigation, 117, 3519-3529.
Rendon, M.A., Saldana, Z., Erdem, A.L., Monteiro-Neto, V., Vazquez, A., Kaper, J.B., Puente, J.L. and Giron, J.A. (2007) Commensal and Pathogenic Escherichia coli Use a Common Pilus Adherence Factor for Epithelial Cell Colonization. Proceedings of the National Academy of Sciences of the United States of America, 104, 10637-10642. http://dx.doi.org/10.1073/pnas.0704104104
Gonnet, P., Rudd, K.E. and Lisacek, F. (2004) Fine-Tuning the Prediction of Sequences Cleaved by Signal Peptidase II: A Curated Set of Proven and Predicted Lipoproteins of Escherichia coli K-12. Proteomics, 4, 1597-1613. http://dx.doi.org/10.1002/pmic.200300749
Rogers, T.J., Paton, J.C., Wang, H., Talbot, U.M. and Paton, A.W. (2006) Reduced Virulence of an fliC Mutant of Shiga-Toxigenic Escherichia coli O113:H21. Infection and Immunity, 74, 1962-1966. http://dx.doi.org/10.1128/IAI.74.3.1962-1966.2006
Tarr, P.I., Bilge, S.S., Vary, J.C., Jelacic, S., Habeeb, R.L., Ward, T.R., Baylor, M.R. and Besser, T.E. (2000) Iha: A Novel Escherichia coli O157:H7 Adherence-Conferring Molecule Encoded on a Recently Acquired Chromosomal Island of Conserved Structure. Infection and Immunity, 68, 1400-1407. http://dx.doi.org/10.1128/IAI.68.3.1400-1407.2000
Janka, A., Bielaszewska, M., Dobrindt, U. and Karch, H. (2002) Identification and Distribution of the Enterohemorrhagic Escherichia coli Factor for Adherence (Efa1) Gene in Sorbitol-Fermenting Escherichia coli O157: H-. International Journal of Medical Microbiology, 292, 207-214. http://dx.doi.org/10.1078/1438-4221-00206
Stevens, M.P., Roe, A.J., Vlisidou, I., van Diemen, P.M., La Ragione, R.M., Best, A., Woodward, M.J., Gally, D.L., and Wallis, T.S. (2004) Mutation of ToxB and a Truncated Version of the Efa-1 Gene in Escherichia coli O157: H7 Influences the Expression and Secretion of Locus of Enterocyte Effacement-Encoded Proteins but Not Intestinal Colonization in Calves or Sheep. Infection and Immunity, 72, 5402-5411. http://dx.doi.org/10.1128/IAI.72.9.5402-5411.2004
Torres, A.G. and Kaper, J.B. (2003) Multiple Elements Controlling Adherence of Enterohemorrhagic Escherichia coli O157:H7 to HeLa Cells. Infection and Immunity, 71, 4985-4995. http://dx.doi.org/10.1128/IAI.71.9.4985-4995.2003
Lee, Y., Kim, Y., Yeom, S., Kim, S., Park, S., Jeon, C.O. and Park, W. (2008) The Role of Disulfide Bond Isomerase A (DsbA) of Escherichia coli O157:H7 in Biofilm Formation and Virulence. FEMS Microbiology Letters, 278, 213-222. http://dx.doi.org/10.1111/j.1574-6968.2007.00993.x
Mao, Y., Doyle, M.P. and Chen, J. (2001) Insertion Mutagenesis of Wca Reduces Acid and Heat Tolerance of Enterohemorrhagic Escherichia coli O157:H7. Journal of Bacteriology, 183, 3811-3815. http://dx.doi.org/10.1128/JB.183.12.3811-3815.2001
Roux, A., Beloin, C. and Ghigo, J.M. (2005) Combined Inactivation and Expression Strategy to Study Gene Function under Physiological Conditions: Application to Identification of New Escherichia coli Adhesins. Journal of Bacteriology, 187, 1001-1013. http://dx.doi.org/10.1128/JB.187.3.1001-1013.2005
Tatsuno, I., Nagano, K., Taquchi, K., Rong, L., Mori, H., and Sasakawa, C. (2003) Increased Adherence to Caco-2 Cells Caused by Disruption of the yhiE and yhiF Genes in Enterohemorrhagic Escherichia coli O157:H7. Infection and Immunity, 71, 2598-2606. http://dx.doi.org/10.1128/IAI.71.5.2598-2606.2003
Tatsuno, I., Horie, M., Abe, H., Miki, T., Makino, K., Shinagawa, H., Taguchi, H., Kamiya, S., Hayashi, T. and Sasakawa, C. (2001) ToxB Gene on pO157 of Enterohemorrhagic Escherichia coli O157:H7 Is Required for Full Epithelial Cell Adherence Phenotype. Infection and Immunity, 69, 6660-6669. http://dx.doi.org/10.1128/IAI.69.11.6660-6669.2001
Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vazquez, A., Barba, J., Ibarra, A., O’Donnel, P., Metalnikov, P., Ashman, K., Lee, S., Goode, D., Pawson, T. and Finlay, B.B. (2004) Dissecting Virulence: Systematic and Functional Analyses of a Pathogenicity Island. Proceedings of the National Academy of Sciences of the United States of America, 101, 3597-3602. http://dx.doi.org/10.1073/pnas.0400326101
Nadler, C., Shifrin, Y., Nov, S., Kobi, S. and Rosenshine, I. (2006) Characterization of Enteropathogenic Escherichia coli Mutants That Fail to Disrupt Host Cell Spreading and Attachment to Substratum. Infection and Immunity, 74, 839-849. http://dx.doi.org/10.1128/IAI.74.2.839-849.2006
Batisson, I., Guimond, M.P., Girard, F., An, H., Zhu, C., Oswald, E., Fairbrother, J.M., Jacques, M. and Harel, J. (2003) Characterization of the Novel Factor Paa Involved in the Early Steps of the Adhesion Mechanism of Attaching and Effacing Escherichia coli. Infection and Immunity, 71, 4516-4525. http://dx.doi.org/10.1128/IAI.71.8.4516-4525.2003
Crane, J.K., McNamara, B.P. and Donnenberg, M.S. (2001) Role of EspF in Host Cell Death Induced by Enteropathogenic Escherichia coli. Cellular Microbiology, 3, 197-211. http://dx.doi.org/10.1046/j.1462-5822.2001.00103.x
Elliott, S.J., Sperandio, V., Giron, J.A., Shin, S., Mellies, J.L., Wainwright, L., Hutchseon, S.W., McDaniel, T.K. and Kaper, J.B. (2000) The Locus of Enterocyte Effacement (LEE)-Encoded Regulator Controls Expression of Both LEE- and Non-LEE-Encoded Virulence Factors in Enteropathogenic and Enterohemorrhagic Escherichia coli. Infection and Immunity, 68, 6115-6126. http://dx.doi.org/10.1128/IAI.68.11.6115-6126.2000
Creasey, E.A., Delahay, R.M., Daniell, S.J. and Frankel, G. (2003) Yeast Two-Hybrid System Survey of Interactions between LEE-Encoded Proteins of Enteropathogenic Escherichia coli. Microbiology, 149, 2093-2106. http://dx.doi.org/10.1099/mic.0.26355-0
Tobe, T., Beatson, S.A., Taniguchi, H., Abe, H., Bailey, C.M., Fivian, A., Younis, R., Matthews, S., Marches, O., Frankel, G., Hayashi, T. and Pallen, M.J. (2006) An Extensive Repertoire of Type III Secretion Effectors in Escherichia coli O157 and the Role of Lambdoid Phages in Their Dissemination. Proceedings of the National Academy of Sciences of the United States of America, 103, 4941-4946. http://dx.doi.org/10.1073/pnas.0604891103
DeVinney, R., Stein, M., Reinscheid, D., Abe, A., Ruschkowski, S. and Finlay, B.B. (1999) Enterohemorrhagic Escherichia coli O157:H7 Produces Tir, Which Is Translocated to the Host Cell Membrane but Is Not Tyrosine Phosphorylated. Infection and Immunity, 67, 2389-2398.
Jepson, M.A., Pellegrin, S., Peto, L., Banbury, D.N., Leard, A.D., Mellor, H. and Kenny, B. (2003) Synergistic Roles for the Map and Tir Effector Molecules in Mediating Uptake of Enteropathogenic Escherichia coli (EPEC) into Non-Phagocytic Cells. Cellular Microbiology, 5, 773-783. http://dx.doi.org/10.1046/j.1462-5822.2003.00315.x
Kenny, B., Ellis, S., Leard, A.D., Warawa, J., Mellor, H. and Jepson, M.A. (2002) Co-Ordinate Regulation of Distinct Host Cell Signalling Pathways by Multifunctional Enteropathogenic Escherichia coli Effector Molecules. Molecular Microbiology, 44, 1095-1107. http://dx.doi.org/10.1046/j.1365-2958.2002.02952.x
Dziva, F., van Diemen, P.M., Stevens, M.P., Smith, A.J. and Wallis, T.S. (2004) Identification of Escherichia coli O157:H7 Genes Influencing Colonization of the Bovine Gastrointestinal Tract Using Signature-Tagged Mutagenesis. Microbiology, 150, 3631-3645. http://dx.doi.org/10.1099/mic.0.27448-0
Kanack, K.J., Crawford, J.A., Tatsuno, I., Karmali, M.A. and Kaper, J.B. (2005) SepZ/EspZ Is Secreted and Translocated into HeLa Cells by the Enteropathogenic Escherichia coli Type III Secretion System. Infection and Immunity, 73, 4327-4337. http://dx.doi.org/10.1128/IAI.73.7.4327-4337.2005
Elliott, S.J., Krejany, E.O., Mellies, J.L., Robins-Browne, R.M., Sasakawa, C. and Kaper, J.B. (2001) EspG, a Novel Type III System-Secreted Protein from Enteropathogenic Escherichia coli with Similarities to VirA of Shigella flexneri. Infection and Immunity, 69, 4027-4033. http://dx.doi.org/10.1128/IAI.69.6.4027-4033.2001
Hardwidge, P.R., Deng, W., Vallance, B.A., Rodriguez-Escudero, I., Cid, V.J., Molina, M. and Finlay, B.B. (2005) Modulation of Host Cytoskeleton Function by the Enteropathogenic Escherichia coli and Citrobacter Rodentium Effector Protein EspG. Infection and Immunity, 73, 2586-2594. http://dx.doi.org/10.1128/IAI.73.5.2586-2594.2005
Gruenheid, S., Sekirov, I., Thomas, N.A., Deng, W., O’Donnell, P., Goode, D., Li, Y., Frey, E.A., Brown, N.F., Metalnikov, P., Pawson, T., Ashman, K. and Finlay, B.B. (2004) Identification and Characterization of NleA, a Non-LEE-Encoded Type III Translocated Virulence Factor of Enterohaemorrhagic Escherichia coli O157:H7. Molecular Microbiology, 51, 1233-1249. http://dx.doi.org/10.1046/j.1365-2958.2003.03911.x
Kelly, M., Hart, E., Mundy, R., Marchès, O., Wiles, S., Badea, L., Luck, S., Tauschek, M., Frankel, G., Robins-Browne, R.M. and Hartland, E.L. (2006) Essential Role of the Type III Secretion System Effector NleB in Colonization of Mice by Citrobacter rodentium. Infection and Immunity, 74, 2328-2337. http://dx.doi.org/10.1128/IAI.74.4.2328-2337.2006
Marches, O., Wiles, S., Dziva, F., La Ragione, R.M., Schuller, S., Best, A., Phillips, A.D., Hartland, E.L., Woodward, M.L., Stevens, M.P. and Frankel, G. (2005) Characterization of Two Non-Locus of Enterocyte Effacement-Encoded Type III-Translocated Effectors, NleC and NleD, in Attaching and Effacing Pathogens. Infection and Immunity, 73, 8411-8417. http://dx.doi.org/10.1128/IAI.73.12.8411-8417.2005
Wickham, M. E., Lupp, C., Vazquez, A., Mascarenhas, M., Coburn, B., Coombes, B.K., Karmali, M.A., Puente, J.L., Deng, W. and Finlay, B.B. (2007) Citrobacter rodentium Virulence in Mice Associates with Bacterial Load and the Type III Effector NleE. Microbes and Infection, 9, 400-407. http://dx.doi.org/10.1016/j.micinf.2006.12.016
Garmendia, J., Ren, Z., Tennant, S., Viera, M.A.M., Chong, Y., Whale, A., Azzopardi, K., Dahan, S., Sircili, M.P., Franzolin, M.R., Trabulsi, L.R., Phillips, A., Gomes, T.A.T., Xu, J., Robins-Browne, R. and Frankel, G. (2005) Distribution of tccP in Clinical Enterohemorrhagic and Enteropathogenic Escherichia coli Isolates. Journal of Clinical Microbiology, 43, 5715-5720. http://dx.doi.org/10.1128/JCM.43.11.5715-5720.2005
Garmendia, J., Phillips, A.D., Carlier, M.F., Chong, Y., Schuller, S., Marches, O., and Shaw, R.K., Knutton, S. and Frankel, G. (2004) TccP Is an Enterohaemorrhagic Escherichia coli O157:H7 Type III Effector Protein That Couples Tir to the Actin-Cytoskeleton. Cellular Microbiology, 6, 1167-1183. http://dx.doi.org/10.1111/j.1462-5822.2004.00459.x
Garmendia, J., Carlier, M.F., Egile, C., Didry, D. and Frankel, G. (2006) Characterization of TccP-Mediated N-WASP Activation during Enterohaemorrhagic Escherichia coli Infection. Cellular Microbiology, 8, 1444-1455. http://dx.doi.org/10.1111/j.1462-5822.2006.00723.x
Vlisidou, I., Dziva, F., La Ragione, R.M., Best, A., Garmendia, J., Hawes, P., Monaghan, P., Cawthraw, S.A., Frankel, G., Woodward, M.J. and Stevens, M.P. (2006) Role of Intimin-Tir Interactions and the Tir-Cytoskeleton Coupling Protein in the Colonization of Calves and Lambs by Escherichia coli O157:H7. Infection and Immunity, 74, 758-764. http://dx.doi.org/10.1128/IAI.74.1.758-764.2006
Ogura, Y., Ooka, T., Whale, A., Garmendia, J., Beutin, L., Tennant, S., Krause, G., Morabito, S., Chinen, I., Tobe, T., Abe, H., Tozzoli, R., Caprioli, A., Rivas, M., Robins-Browne, R., Hayasha, T. and Frankel, G. (2007) TccP2 of O157: H7 and Non-O157 Enterohemorrhagic Escherichia coli (EHEC): Challenging the Dogma of EHEC-Induced Actin Polymerization. Infection and Immunity, 75, 604-612. http://dx.doi.org/10.1128/IAI.01491-06
Garmendia, J. and Frankel, G. (2005) Operon Structure and Gene Expression of the EspJ-TccP Locus of Enterohaemorrhagic Escherichia coli O157:H7. FEMS Microbiology Letters, 247, 137-145. http://dx.doi.org/10.1016/j.femsle.2005.04.035
Ideses, D., Gophna, U., Paitan, Y., Chaudhuri, R.R., Pallen, M.J. and Ron, E.Z. (2005) A Degenerate Type III Secretion System from Septicemic Escherichia coli Contributes to Pathogenesis. Journal of Bacteriology, 187, 8164-8171. http://dx.doi.org/10.1128/JB.187.23.8164-8171.2005
Han, Y., Zhou Z.J. and Zhang, Y.J. (2005) Genes of E. coli O157 Associated with Adherence to Hep-2 Cells. Chinese Journal of Veterinary Science, 3, 266-269.
Pallen, M.J., Beatson, S.A. and Bailey, C.M. (2005) Bioinformatics Analysis of the Locus for Enterocyte Effacement Provides Novel Insights into Type-III Secretion. BMC Microbiology, 5, 9. http://dx.doi.org/10.1186/1471-2180-5-9
Yip, C.K., Finlay, B.B. and Strynadka, N.C. (2005) Structural Characterization of a Type III Secretion System Filament Protein in Complex with Its Chaperone. Nature Structural & Molecular Biology, 12, 75-81. http://dx.doi.org/10.1038/nsmb879
Elliott, S.J., Hutcheson, S.W., Dubois, M.S., Mellies, J.L., Wainwright, L.A., Batchelor, M., Frankel, G., Knutton, S. and Kaper, J.B. (1999) Identification of CesT, a Chaperone for the Type III Secretion of Tir in Enteropathogenic Escherichia coli. Molecular Microbiology, 33, 1176-1189. http://dx.doi.org/10.1046/j.1365-2958.1999.01559.x
Ogino, T., Ohno, R., Sekiya, K., Kuwae, A., Matsuzawa, T., Nonaka, T., Fukuda, H., Imajoh-Ohmi, S. and Abe, A. (2006) Assembly of the Type III Secretion Apparatus of Enteropathogenic Escherichia coli. Journal of Bacteriology, 188, 2801-2811. http://dx.doi.org/10.1128/JB.188.8.2801-2811.2006
Boerlin, P., McEwen, S.A., Boerlin-Petzold, F., Wilson, J.B., Johnson, R.P. and Gyles, C.L. (1999) Associations between Virulence Factors of Shiga Toxin-Producing Escherichia coli and Disease in Humans. Journal of Clinical Microbiology, 37, 497-503.
Siegler, R.L., Obrig, T.G., Pysher, T.J., Tesh, V.L., Denkers, N.D. and Taylor, F.B. (2003) Response to Shiga Toxin 1 and 2 in a Baboon Model of Hemolytic Uremic Syndrome. Pediatric Nephrology, 18, 92-96.
Louise, C.B. and Obrig, T.G. (1995) Specific Interaction of Escherichia coli O157:H7-Derived Shiga-Like Toxin II with Human Renal Endothelial Cells. The Journal of Infectious Diseases, 172, 1397-401. http://dx.doi.org/10.1093/infdis/172.5.1397
Ashkenazi, S. and Cleary, T.G. (1989) Rapid Method to Detect Shiga Toxin and Shiga-Like Toxin I Based on Binding to Globotriosyl Ceramide (Gb3), Their Natural Receptor. Journal of Clinical Microbiology, 27, 1145-1150.
Grys, T.E., Siegel, M.B., Lathem, W.W. and Welch, R.A. (2005) The StcE Protease Contributes to Intimate Adherence of Enterohemorrhagic Escherichia coli O157:H7 to Host Cells. Infection and Immunity, 73, 1295-1303. http://dx.doi.org/10.1128/IAI.73.3.1295-1303.2005
Brunder, W., Schmidt, H. and Karch, H. (1997) EspP, a Novel Extracellular Serine Protease of Enterohaemorrhagic Escherichia coli O157:H7 Cleaves Human Coagulation Factor V. Molecular Microbiology, 24, 767-778. http://dx.doi.org/10.1128/IAI.73.3.1295-1303.2005
Wandersman, C. and Delepelaire, P. (1990) TolC, an Escherichia coli Outer Membrane Protein Required for Hemolysin Secretion. Proceedings of the National Academy of Sciences of the United States of America, 87, 4776-4780. http://dx.doi.org/10.1073/pnas.87.12.4776
Fong, K.P., Chung, W.O., Lamont, R.J. and Demuth, D.R. (2001) Intra- and Interspecies Regulation of Gene Expression by Actinobacillus actinomycetemcomitans LuxS. Infection and Immunity, 69, 7625-7634. http://dx.doi.org/10.1128/IAI.69.12.7625-7634.2001
Bauer, M.E. and Welch, R.A. (1996) Characterization of an RTX Toxin from Enterohemorrhagic Escherichia coli O157:H7. Infection and Immunity, 64, 167-175.
Dowd, S.E. and Ishizaki, H. (2006) Microarray Based Comparison of Two Escherichia coli O157:H7 Lineages. BMC Microbiology, 6, 30. http://dx.doi.org/10.1186/1471-2180-6-30
Lloyd, A.L., Rasko, D.A. and Mobley, H.L. (2007) Defining Genomic Islands and Uropathogen-Specific Genes in Uropathogenic Escherichia coli. Journal of Bacteriology, 189, 3532-3546. http://dx.doi.org/10.1128/JB.01744-06
Lopez-Solanilla, E., Garcia-Olmedo, F. and Rodriguez-Palenzuela, P. (1998) Inactivation of the SapA to SapF Locus of Erwinia Chrysanthemi Reveals Common Features in Plant and Animal Bacterial Pathogenesis. The Plant Cell, 10, 917-924.
Lopez-Solanilla, E., Llama-Palacios, A., Collmer, A., Garcia-Olmedo, F. and Rodriguez-Palenzuela, P. (2001) Relative Effects on Virulence of Mutations in the Sap, Pel, and Hrp Loci of Erwinia chrysanthemi. Molecular Plant-Microbe Interactions, 14, 386-393. http://dx.doi.org/10.1094/MPMI.2001.14.3.386
De Koning-Ward, T.F. and Robins-Browne, R.M. (1995) Contribution of Urease to Acid Tolerance in Yersinia enterocolitica. Infection and Immunity, 63, 3790-3795.
Friedrich, A.W., Lukas, R., Mellmann, A., Kock, R., Zhang, W., Mathys, W., Bielaszewska, M., Karch, H. (2006) Urease Genes in Non-O157 Shiga Toxin-Producing Escherichia coli: Mostly Silent but Valuable Markers for Pathogenicity. Clinical Microbiology and Infection, 12, 483-486. http://dx.doi.org/10.1111/j.1469-0691.2006.01379.x
Sanfrigari, F.J., Seoane, A., Rodriguez, M.C., Aquero, J. and Garcia Lobo, J.M. (2007) Characterization of the Urease operon of Brucella abortus and Assessment of Its Role in Virulence of the Bacterium. Infection and Immunity, 75, 774-780. http://dx.doi.org/10.1128/IAI.01244-06
Nakano, M., Iida, T., Ohnishi, M., Kurokawa, K., Takahashi, A., Tsukamoto, T., Yasunaga, T., Hayasha, T. and Honda, T. (2001) Association of the Urease Gene with Enterohemorrhagic Escherichia coli Strains Irrespective of Their Serogroups. Journal of Clinical Microbiology, 39, 4541-4543. http://dx.doi.org/10.1128/JCM.39.12.4541-4543.2001
Nakano, M., Iida, T. and Honda, T. (2004) Urease Activity of Enterohaemorrhagic Escherichia coli Depends on a Specific One-Base Substitution in UreD. Microbiology, 150, 3483-3489. http://dx.doi.org/10.1099/mic.0.27280-0
Fleming, A. and Young, M.Y. (1940) The Inhibitory Action of Potassium Tellurite on Coliform Bacteria. The Journal of Pathology and Bacteriology, 51, 29-35. http://dx.doi.org/10.1002/path.1700510106
Taylor, D.E., Rooker, M., Keelan, M., Ng, L.K., Martin, I., Perna, N.T., Burland, N.T. and Blattner, F.R. (2002) Genomic Variability of O Islands Encoding Tellurite Resistance in Enterohemorrhagic Escherichia coli O157:H7 Isolates. Journal of Bacteriology, 184, 4690-4698. http://dx.doi.org/10.1128/JB.184.17.4690-4698.2002
Summers, A.O. and Jacoby, G.A. (1977) Plasmid-Determined Resistance to Tellurium Compounds. Journal of Bacteriology, 129, 276-281.
Valkova, D., Valkovicova, L., Vavrova, S., Kovacova, E., Mravec, J. and Turna, J. (2007) The Contribution of Tellurite Resistance Genes to the Fitness of Escherichia coli Uropathogenic Strains. Central European Journal of Biology, 2, 182-191. http://dx.doi.org/10.2478/s11535-007-0019-9
Wilson, R.K., Shaw, R.K., Daniell, S., Knutton, S. and Frankel, G. (2001) Role of EscF, a Putative Needle Complex Protein, in the Type III Protein Translocation System of Enteropathogenic Escherichia coli. Cell Microbiology, 3, 753-762. http://dx.doi.org/10.1046/j.1462-5822.2001.00159.x
Brunder, W., Schmidt, H. and Karch, H. (1996) KatP, a Novel Catalase-Peroxidase Encoded by the Large Plasmid of Enterohaemorrhagic Escherichia coli O157:H7. Microbiology, 142, 3305-3315. http://dx.doi.org/10.1099/13500872-142-11-3305
Raetz, C.R.H. and Whitfield, C. (2002) Lipopolysaccharide Endotoxins. Annual Review of Biochemistry, 71,635-700. http://dx.doi.org/10.1146/annurev.biochem.71.110601.135414
Neves, B.C., Mundy, R., Petrovska, L., Dougan, G., Knutton, S. and Frankel, G. (2003) CesD2 of Enteropathogenic Escherichia coli Is a Second Chaperone for the Type III Secretion Translocator Protein EspD. Infection and Immunity, 71, 2130-2141. http://dx.doi.org/10.1128/IAI.71.4.2130-2141.2003
Shaw, R.K., Berger, C.N., Feys, B., Knutton, S., Pallen, M.J. and Frankel, G. (2008) Enterohemorrhagic Escherichia coli Exploits EspA Filaments for Attachment to Salad Leaves. Applied and Environmental Microbiology, 74, 2908-2914. http://dx.doi.org/10.1128/AEM.02704-07
Kresse, A.U., Beltrametti, F., Muller, A., Ebel, F. and Guzman, C.A. (2000) Characterization of SepL of Enterohemorrhagic Escherichia coli. Journal of Bacteriology, 182, 6490-6498. http://dx.doi.org/10.1128/JB.182.22.6490-6498.2000
Deng, W., Li, Y., Hardwidge, P.R., Frey, E.A., Pfuetzner, R.A., Lee, S., Gruendheid, S., Styrnakda, N.C.J., Puente, J.L. and Finlay, B.B. (2005) Regulation of Type III Secretion Hierarchy of Translocators and Effectors in Attaching and Effacing Bacterial Pathogens. Infection and Immunity, 73, 2135-2146. http://dx.doi.org/10.1128/IAI.73.4.2135-2146.2005
Jerse, A.E., Yu, J., Tall, B.D. and Kaper, J.B. (1990) A Genetic Locus of Enteropathogenic Escherichia coli Necessary for the Production of Attaching and Effacing Lesions on Tissue Culture Cells. Proceedings of the National Academy of Sciences of the United States of America, 87, 7839-7843. http://dx.doi.org/10.1073/pnas.87.20.7839
Elliott, S.J., O’Connell, C.B., Koutsouris, A., Brinkley, C., Donnenberg, M.S., Hecht, G. and Kaper, J.B. (2002) A Gene from the Locus of Enterocyte Effacement That Is Required for Enteropathogenic Escherichia coli to Increase Tight-Junction Permeability Encodes a Chaperone for EspF. Infection and Immunity, 70, 2271-2277. http://dx.doi.org/10.1128/IAI.70.5.2271-2277.2002
Gauthier, A., Puente, J.L. and Finlay, B.B. (2003) Secretin of the Enteropathogenic Escherichia coli Type III Secretion System Requires Components of the Type III Apparatus for Assembly and Localization. Infection and Immunity, 71, 3310-3319. http://dx.doi.org/10.1128/IAI.71.6.3310-3319.2003
O’Connell, C.B., Creasey, E.A., Knutton, S., Elliott, S., Crowther, L.J., Luo, W., Albert, M.J., Kaper, J.B., Frankel, G. and Donnenberg, M.S. (2004) SepL, a Protein Required for Enteropathogenic Escherichia coli Type III Translocation, Interacts with Secretion Component SepD. Molecular Microbiology, 52, 1613-1625. http://dx.doi.org/10.1111/j.1365-2958.2004.04101.x
Reading, N.C., Torres, A.G., Kendall, M.M., Hughes, D.T., Yamamoto, K. and Sperandio, V. (2007) A Novel Two-Component Signaling System That Activates Transcription of an Enterohemorrhagic Escherichia coli Effector Involved in Remodeling of Host Actin. Journal of Bacteriology, 189, 2468-2476. http://dx.doi.org/10.1128/JB.01848-06
Torres, A.G., Lopez-Sanchez, G.N., Milflores-Flores, L., Patel, S.D., Rojas-Lopez, M., de la Pena, C.F.M., Arenas-Hernandez, M.M.P. and Martinez-Laguna, Y. (2007) Ler and H-NS, Regulators Controlling Expression of the Long Polar Fimbriae of Escherichia coli O157:H7. Journal of Bacteriology, 189, 5916-5928. http://dx.doi.org/10.1128/JB.00245-07
Ogierman, M.A., Paton, A.W. and Paton, J.C. (2000) Up-Regulation of Both Intimin Andeae-Independent Adherence of Shiga Toxigenic Escherichia coli O157 by ler and Phenotypic Impact of a Naturally Occurring ler Mutation. Infection and Immunity, 68, 5344-5353. http://dx.doi.org/10.1128/IAI.68.9.5344-5353.2000
Kim, J., Nietfeldt, J. and Benson, A.K. (1999) Octamer-Based Genome Scanning Distinguishes a Unique Subpopulation of Escherichia coli O157:H7 Strains in Cattle. Proceedings of the National Academy of Sciences of the United States of America, 96, 13288-13293. http://dx.doi.org/10.1073/pnas.96.23.13288
Lee, M.S., Kaspar, C.W., Brosch, R., Shere, J. and Luchansky, J.B. (1996) Genomic Analysis Using Pulsed-Field Gel Electrophoresis of Escherichia coli O157:H7 Isolated from Dairy Calves during the United States National Dairy Heifer Evaluation Project (1991-1992). Veterinary Microbiology, 48, 223-230. http://dx.doi.org/10.1016/0378-1135(95)00135-2
Dahan, S., Wiles, S., La Ragione, R.M., Best, A., Woodward, M.J., Stevens, M.P., Shaw, R.K., Chong, Y., Knutton, S., Phillips, A. and Frankel, G. (2005) EspJ Is a Prophage-Carried Type III Effector Protein of Attaching and Effacing Pathogens That Modulates Infection Dynamics. Infection and Immunity, 73, 679-686. http://dx.doi.org/10.1128/IAI.73.2.679-686.2005
Jay, M.T., Cooley, M., Carychao, D., Wiscomb, G.W., Sweitzer, R.A., Crawford-Miksza, L., Farrar, J.A., Lau, D.K., O’Connel, J., Millington, A., Asmundson, R.V., Atwill, E.R. and Mandrell, R.E. (2007) Escherichia coli O157: H7 in Feral Swine Near Spinach Fields and Cattle, Central California Coast. Emerging Infectious Diseases, 13, 1908. http://dx.doi.org/10.3201/eid1312.070763
Baker, D.R., Moxley, R.A., Steele, M.B., Lejeune, J.T., Christopher-Hennings, J., Chen, D.G., Hardwidge, P.R. and Francis, D.H. (2007) Differences in Virulence among Escherichia coli O157:H7 Strains Isolated from Humans during Disease Outbreaks and from Healthy Cattle. Applied and Environmental Microbiology, 73, 7338-7346. http://dx.doi.org/10.1128/AEM.00755-07
Donohue-Rolfe, A., Kondova, I., Oswald, S., Hutto, D. and Tzipori, S. (2000) Escherichia coli O157:H7 Strains That Express Shiga Toxin (Stx) 2 Alone Are More Neurotropic for Gnotobiotic Piglets than Are Isotypes Producing only Stx1 or Both Stx1 and Stx2. The Journal of Infectious Diseases, 181, 1825-1829. http://dx.doi.org/10.1086/315421
Ritchie, J.M., Brady, M.J., Riley, K.N., Ho, T.D., Campellone, K.G., Herman, I.M., Donohue-Rolfe, A., Tzipori, S., Waldor, M.K. and Leong, J.M. (2008) EspFU, a Type III-Translocated Effector of Actin Assembly, Fosters Epithelial Association and Late-Stage Intestinal Colonization by E. coli O157:H7. Cell Microbiology, 10, 836-847. http://dx.doi.org/10.1111/j.1462-5822.2007.01087.x
Moreira, C.G., Carneiro, S.M., Nataro, J.P., Trabulsi, L.R. and Elias, W.P. (2003) Role of Type I Fimbriae in the Aggregative Adhesion Pattern of Enteroaggregative Escherichia coli. FEMS Microbiology Letters, 226, 79-85. http://dx.doi.org/10.1016/S0378-1097(03)00561-5
Schmidt, H., Henkel, B. and Karch, H. (1997) A Gene Cluster Closely Related to Type II Secretion Pathway Operons of Gram-Negative Bacteria Is Located on the Large Plasmid of Enterohemorrhagic Escherichia coli O157 Strains. FEMS Microbiology Letters, 148, 265-272. http://dx.doi.org/10.1111/j.1574-6968.1997.tb10299.x
Ledeboer, N.A. and Jones, B.D. (2005) Exopolysaccharide Sugars Contribute to Biofilm Formation by Salmonella enterica Serovar Typhimurium on HEp-2 Cells and Chicken Intestinal Epithelium. Journal of Bacteriology, 187, 3214-3226. http://dx.doi.org/10.1128/JB.187.9.3214-3226.2005
Makino, S.I., Tobe, T., Asakura, H., Watarai, M., Ikeda, T., Takeshi, K. and Sasakawa, C. (2003) Distribution of the Secondary Type III Secretion System Locus Found in Enterohemorrhagic Escherichia coli O157:H7 Isolates among the Shiga Toxin-Producing E. coli Strains. Journal of Clinical Microbiology, 41, 2341-2347. http://dx.doi.org/10.1128/JCM.41.6.2341-2347.2003
Baumler, D.J., Banta, L.M., Hung, K.F., Schwarz, J.A., Cabot, E.C., Glasner, J.D. and Perna, N.T. (2012) Using Comparative Genomics for Inquiry-Based Learning to Dissect Virulence of Escherichia coli O157:H7. CBE-Life Sciences Education, 11, 81-93.
Jandu, N., Ho, N.K., Donato, K.A., Karmali, M.A., Mascarenhas, M., Duffy, S.P., Tailor, C. and Sherman, P.M. (2009) Enterohemorrhagic Escherichia coli O157:H7 Gene Expression Profiling in Response to Growth in the Presence of Host Epithelia. PLoS ONE, 4, e4889. http://dx.doi.org/10.1371/journal.pone.0004889
Bansal, T., Englert, D., Lee, J., Hegde, M., Wood, T.K. and Jayaraman, A. (2007) Differential Effects of Epinephrine, Norepinephrine, and Indole on Escherichia coli O157:H7 Chemotaxis, Colonization, and Gene Expression. Infection and Immunity, 75, 4597-4607. http://dx.doi.org/10.1128/IAI.00630-07
Mukherjee, A., Mammel, M.K., LeClerc, J.E. and Cebula, T.A. (2008) Altered Utilization of N-acetyl-D-Galactosamine by Escherichia coli O157:H7 from the 2006 Spinach Outbreak. Journal of Bacteriology, 190, 1710-1717. http://dx.doi.org/10.1128/JB.01737-07
Chin, N., Frey, J., Chang, C.F. and Chang, Y.F. (1996) Identification of a Locus Involved in the Utilization of Iron by Actinobacillus pleuropneumoniae. FEMS Microbiology Letters, 143, 1-6. http://dx.doi.org/10.1111/j.1574-6968.1996.tb08452.x
Baumler, D.J., Peplinski, R.G., Reed, J.L., Glasner, J.D. and Perna, N.T. (2011) The Evolution of Metabolic Networks of E. coli. BMC Systems Biology, 5, 182.