Escherichia coli virulence factors

[en] Escherichia coli was described in 1885 by a German pediatrician, Theodor Escherich, in the faeces of a child suffering diarrhoea. In 1893, a Danish veterinarian postulated that the E. coli species comprises different strains, some being pathogens, others not. Today the E. coli species is subdivided into several pathogenic strains causing different intestinal, urinary tract or internal infections and pathologies, in animal species and in humans. Since this congress topic is the interaction between E. coli and the mucosal immune system, the purpose of this manuscript is to present different classes of adhesins (fimbrial adhesins, afimbrial adhesins and outer membrane proteins), the type 3 secretion system, and some toxins (oligopeptide, AB, and RTX pore-forming toxins) produced by E. coli, that can directly interact with the epithelial cells of the intestinal, respiratory and urinary tracts.

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Mainil, Jacques ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Bactériologie et pathologie des maladies bactériennes

Language :

English

Title :

Escherichia coli virulence factors

Publication date :

2013

Journal title :

Veterinary Immunology and Immunopathology

ISSN :

0165-2427

eISSN :

1873-2534

Publisher :

Elsevier Science, Amsterdam, Netherlands

Volume :

152

Pages :

2-12

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 03 December 2012

Statistics

Number of views

1385 (11 by ULiège)

Number of downloads

4799 (7 by ULiège)

More statistics

Scopus citations^®

115

Scopus citations^®
without self-citations

114

OpenCitations

OpenAlex citations

142

Bibliography

Amezcua R., Friendship R.M., Dewey C.E., Gyles C., Fairbrother J.M. Presentation of postweaning Escherichia coli diarrhea in southern Ontario, prevalence of hemolytic E. coli serogroups involved, and their antimicrobial resistance patterns. Can. J. Vet. Res. 2002, 66:73-78.
An H., Fairbrother J.M., Desautels C., Harel J. Distribution of a novel locus called Paa (porcine attaching and effacing associated) amongenteric Escherichia coli. Adv. Exp. Med. Biol. 1999, 473:179-184.
Bann J.G., Dodson K.W., Frieden C., Hultgren S.J. Adhesive pili of the chaperone-usher family. Escherichia coli: Virulence Mechanisms of a Versatile Pathogen 2002, 289-306. Academic Press, San Diego, CA, U.S.A. M.S. Donnenberg (Ed.).
Bardiau M., Szalo M., Mainil J.G. Initial adherence of EPEC, EHEC and VTEC to host cells. Vet. Res. 2010, 41:57-72.
Barnhart M.M., Chapman M.R. Curli biogenesis and function. Ann. Rev. Microbiol. 2006, 60:131-147.
Bertschinger H.U., Gyles C.L. Oedema in pigs. Escherichia coli in Domestic Animals and Humans 1994, 193-219. Cab International, Wallingford, Oxon, U.K. C.L. Gyles (Ed.).
Beutin L., Prada S., Zimmermann S., Stephan R., Orskov I., Orskov F. Enterohemolysin, a new type of hemolysin produced by some strains of enteropathogenic E. coli (EPEC). Zentrl. Bakteriol. Mikrobiol. Hyg. A 1988, 267:576-588.
Bielaszewska M., Prager R., Kock R., Mellmann A., Zhang W., Tschape H., Tarr P.I., Karch H. Shiga toxin gene loss and transfer in vitro and in vivo during enterohemorrhagic Escherichia coli O26 infection in humans. Appl. Environ. Microbiol. 2007, 73:3144-3150.
Bielaszewska M., Mellmann A., Zhang W., Kock R., Fruth A., Bauwens A., Peters G., Karch H. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany 2011 a microbiological study. Lancet Infect. Dis. 2011, 70165-70167. 10.1016/S1473-3099(11).
Björk S., Briemer M.E., Hansson G.C., Karlsson K.A., Leffler H. Structure of blood group glycosphingolipids of human small intestine. J. Biol. Chem. 1987, 262:6758-6765.
Bolton D.J. Verocytotoxigenic (Shiga toxin-producing) Escherichia coli: virulence factors and pathogenicity in the farm to fork paradigm. Foodborne Pathog. Dis. 2011, 8:357-365.
Burgess M.N., Bywater R.J., Cowley C.M., Mullan N.A., Newsome P.M. Biological evaluation of a methanol-soluble, heat-stable Escherichia coli enterotoxin in infant mice, pigs, rabbits and calves. Infect. Immun. 1978, 21:526-531.
China B., Goffaux F. Secretion of virulence factors by Escherichia coli. Vet. Res. 1999, 30:181-202.
China B., Goffaux F., Pirson V., Mainil J. Comparison of eae, tir, espA, and espB genes of bovine and human attaching and effacing Escherichia coli by multiplex polymerase chain reaction. FEMS Microbiol. Lett. 1999, 178:177-182.
Clarke S.C., Haigh R.D., Freestone P.P.E., Williams P.H. Virulence of enteropathogenic Escherichia coli, a global pathogen. Clin. Microbiol. Rev. 2003, 16:365-378.
Clavijo A.P., Bai J., Gomez-Duarte O.G. The longus type IV pilus of enterotoxigenic Escherichia coli (ETEC) mediates bacterial self-aggregation and protection from antimicrobial agents. Microb. Pathog. 2010, 48:230-238.
Clements J.D., Finkelstein R.A. Demonstration of shared and unique immunological determinants in enterotoxins from Vibrio cholerae and Escherichia coli. Infect. Immun. 1978, 22:709-711.
Cookson A.L., Bennett J., Thomson-Carter F., Attwood G.T. Molecular subtyping and genetic analysis of the enterohemolysin gene (ehxA) from Shiga toxin-producing Escherichia coli and atypical enteropathogenic E. coli. Appl. Environ. Microbiol. 2007, 73:6360-6369.
De Rycke J., Milon A., Oswald E. Necrotoxic Escherichia coli (NTEC): two emerging categories of human and animal pathogens. Vet. Res. 1999, 30:221-234.
Dho-Moulin M., Fairbrother J.M. Avian pathogenic Escherichia coli (APEC). Vet. Res. 1999, 30:299-316.
Donnenberg M.S., Welch R.A. Virulence determinants of uropathogenic Escherichia coli. Urinary Tract Infections: Molecular Pathogenesis and Clinical Management 1996, 135-174. ASM Press, Washington, D.C., U.S.A. H.L.T. Mobley, J.W. Warren (Eds.).
Dozois C.M., Curtiss R. Pathogenic diversity of Escherichia coli and the emergence of exotic islands in the gene stream. Vet. Res. 1999, 30:157-180.
Dubreuil J.D. Escherichia coli STb toxin and colibacillosis: knowing is half the battle. FEMS Microbiol. Lett. 2008, 278:137-145.
Duguid J.P., Smith I.W., Dempster G., Edmunds P.N. Non flagellar filamentous appendages " Fimbriae" and haemagglutinating activity in Bacterium coli. J. Pathol. Bacteriol. 1955, 90:335-348.
Escherich T. Die Darmbacterien des Neugeborenen und Saglings. Fortschr. Med. 1885, 3:515-522.
Falkow S. Molecular Koch's postulates applied to microbial pathogenicity. Rev. Infect. Dis. 1988, 10:S274-S276.
Farfan M.J., Inman K.G., Nataro J.P. The major pilin subunit of the AAF/II fimbriae from enteroaggregative Escherichia coli mediates binding to extracellular matrix proteins. Infect. Immun. 2008, 76:4378-4384.
Flores J., Okhuysen P.C. Enteroaggregative Escherichia coli infection. Curr. Opin. Gastroenterol. 2009, 25:8-11.
Fukuta S., Magnani J.L., Twiddy E.M., Holmes R.K., Ginsburg V. Comparison of carbohydrate specificities of cholera toxin, and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect. Immun. 1988, 56:1748-1753.
Garmendia J., Frankel G., Crepin V.F. Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect. Immun. 2005, 73:2573-2585.
Gérardin J., Lalioui L., Jacquemin E., Le Bouguénec C., Mainil J.G. The afa-related gene cluster in necrotoxigenic and other Escherichia coli from animals belongs to the afa-8 variant. Vet. Microbiol. 2000, 76:175-184.
Giron J.A., Gomez-Duarte O.G., Jarvois K.G., Kaper J.B. Longus pilus of enterotoxigenic Escherichia coli and its relatedness to other type-4 pili - a minireview. Gene 1997, 192:39-43.
Gonçalves C., Vachon V., Schwartz J.L., Dubreuil J.D. The Escherichia coli enterotoxin STb permeabilizes piglet jejunal brush border membrane vesicles. Infect. Immun. 2007, 75:2208-2213.
Goulter R.M., Gentle I.R., Dykes G.A. Issues in determining factors influencing bacterial attachment: a review using the attachment of Escherichia coli to abiotic surfaces as an example. Lett. Appl. Microbiol. 2009, 49:1-7.
Guth B.E., Pickett C.L., Twiddy E.M., Holmes R.K., Gomes T.A., Lima A.A., Guerrant R.L., Francs B.D., Trabulsi L.R. Production of type II heat-labile enterotoxin by Escherichia coli isolated from food and human feces. Infect. Immun. 1986, 54:529-536.
Gyles C.L. Escherichia coli verotoxins and other cytotoxins. Escherichia coli in Domestic Animals and Humans 1994, 365-398. Cab International, Wallingford, Oxon, U.K. C.L. Gyles (Ed.).
Gyles C.L., Barnum D.A. A heat-labile enterotoxin from strains of Escherichia coli enteropathogenic for pigs. J. Infect. Dis. 1969, 120:419-426.
Gyles C.L., Fairbrother J.M. Escherichia coli. Pathogenesis of Bacterial Infections in Animals 2010, 267-308. Wiley-Blackwell, Ames, IA, U.S.A. C.L. Gyles, J.F. Prescott, J.G. Songer, C.O. Thoen (Eds.).
Gyles C.L., So M., Falkow S. The enterotoxin plasmids of Escherichia coli. J. Infect. Dis. 1974, 130:40-49.
Hampson D.J. Postweaning Escherichia coli diarrhoea in pigs. Escherichia coli in Domestic Animals and Humans 1994, 171-191. Cab International, Wallingford, Oxon, U.K. C.L. Gyles (Ed.).
Harrington S.M., Dudley E.G., Nataro J.P. Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol. Lett. 2006, 254:12-18.
Hartland E.L., Batchelor M., Delahay R.M., Hale C., Matthews S., Dougan G., Knutton S., Connerton I., Frankel G. Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol. Microbiol. 1999, 32:151-158.
Hernandes R.T., Elias W.P., Vieira M.A.M., Gomes T.A.T. An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol. Lett. 2009, 297:137-149.
Hoey D.E., Currie C., Else R.W., Nutikka A., Lingwood C.A., Gally D.L., Smith D.G. Expression of receptors for verotoxin 1 from Escherichia coli O157 on bovine intestinal epithelium. J. Med. Microbiol. 2002, 51:143-149.
Hoey D.E., Sharp L., Currie C., Lingwood C.A., Gally D.L., Smith D.G. Verotoxin 1 binding to intestinal crypt epithelial cells results in localization to lysosomes and abrogation of toxicity. Cell. Microbiol. 2003, 5:85-97.
Holmes R.K., Twiddy E.M., Pickett C.L. Purification and characterization of type II heat-labile enterotoxin of Escherichia coli. Infect. Immun. 1986, 53:464-473.
Honda T., Tsuji T., Takeda Y., Miwatani T. Immunological non-identity of heat-labile enterotoxins from human and porcine enterotoxigenic Escherichia coli. Infect. Immun. 1981, 34:337-340.
Huang D.B., Mohanty A., DuPont H.L., Okhuysen P.C., Chiang T. A review of an emerging enteric pathogen: enteroaggregative Escherichia coli. J. Med. Microbiol. 2006, 55:1303-1311.
Hurley B.P., Jacewicz M., Thorpe C.M., Lincicome L.L., King A.J., Keusch G.T., Acheson D.W.K. Shiga toxins 1 and 2 translocate differently across polarized intestinal epithelial cells. Infect. Immun. 1999, 67:6670-6677.
Jenkins C., Perry N.T., Cheasty T., Shaw D.J., Frankel G., Dougan G., Gunn G.J., Smith H.R., Paton A.W., Paton J.C. Distribution of the saa gene in strains of Shiga toxin-producing Escherichia coli of human and bovine origins. J. Clin. Microbiol. 2003, 41:1775-1778.
Jensen C.O. Ueber die Kälberruhr und deren Aetiologie. Mh. Tierhelk. 1893, 4:97-124.
Johannes L., Romer W. Shiga toxins - from cell biology to biomedical applications. Nat. Rev. Microbiol. 2010, 8:105-116.
Johansen M., Andresen L.O., Jorsal S.E., Thomsen L.K., Waddell T.E., Gyles C.L. Prevention of edema disease in pigs by vaccination with verotoxin 2e toxoid. Can. J. Vet. Res. 1997, 61:280-285.
Johnson J.R. Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol. Rev. 1991, 4:80-128.
Johnson J.R. Microbial virulence determinants and the pathogenesis of urinary tract infection. Infect. Dis. Clin. North Am. 2003, 17:261-278.
Kaper J.B., Nataro J.P., Mobley H.L. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2:123-140.
Karch H., Meyer T., Russmann H., Heesemann J. Frequent loss of Shiga-like toxin genes in clinical isolates of Escherichia coli upon subcultivation. Infect. Immun. 1992, 60:3464-3467.
Karmali M.A., Gannon V., Sargeant J.M. Verocytotoxin-producing Escherichia coli (VTEC). Vet. Microbiol. 2010, 140:360-370.
Kauffmann F. The serology of the coli group. J. Immunol. 1947, 57:71-100.
Kayser H. Ueber Bakterienshämolyse, im Besonderen das Colilysin. Zeitschr. Hyg. Infektionkrankh. 1903, 42:118-138.
Koch R. Die Aetiologie der Tuberkulose. Mitt. Kaiser Gesundh. 1884, 2:1-88.
Konno T., Yatsuyanagi J., Saito S. Virulence gene profiling of enteroaggregative Escherichia coli heat-stable enterotoxin 1-harbouring E. coli (EAST1EC) derived from sporadic diarrheal patients. FEMS Immunol. Med. Microbiol. 2011, 10.1111/j.1574-695X.2011.00913.x.
Konowalchuk J., Speirs J.I., Stavric S. Vero response to a cytotoxin of Escherichia coli. Infect. Immun. 1977, 18:775-779.
Lalioui L., Jouve M., Gounon P., Le Bouguénec C. Molecular cloning and characterization of the afa-7 and afa-8 gene clusters encoding afimbrial adhesins in Escherichia coli strains associated with diarrhea or septicemia in calves. Infect. Immun. 1999, 67:5048-5059.
Law D., Chart H. Enteroaggregative Escherichia coli. J. Appl. Microbiol. 1998, 84:685-697.
Le Bouguénec C., Bertin Y. AFA and F17 adhesins produced by pathogenic Escherichia coli in animals. Vet. Res. 1999, 30:317-342.
Leclerc S., Boerlin P., Gyles C., Dubreuil J.D., Mourez M., Fairbrother J.M., Harel J. paa, originally identified in attaching and effacing Escherichia coli, is also associated with enterotoxigenic E. coli. Res. Microbiol. 2007, 158:97-104.
Levine M.M. Escherichia coli that cause diarrhea: enterotoxigenic, enteroinvasive, enterohemorrhagic and enteroadherent. J. Infect. Dis. 1987, 155:377-389.
Lior H. Classification of Escherichia coli. Escherichia coli in Domestic Animals and Humans 1994, 31-72. Cab International, Wallingford, Oxon, U.K. C.L. Gyles (Ed.).
Ludwig A., Goebel W. Haemolysins of Escherichia coli. Escherichia coli - Mechanisms of Virulence 1997, 281-329. Cambridge University Press, Cambridge, U.K. M. Sussman (Ed.).
Luo Y., Frey E.A., Pfuetzner R.A., Creagh A.L., Knoechel D.G., Haynes C.A., Finlay B.B., Strynadka N.C. Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature 2000, 405:1073-1077.
Mainil J. Les souches pathogènes d'Escherichia coli chez les chiens et chats: IV) Discussion générale. Ann. Méd. Vét. 2002, 146:219-224.
Mainil J. Facteurs de virulence et propriétés spécifiques des souches invasives d'Escherichia coli: I) Les adhésines et facteurs de colonisation. Ann. Méd. Vét. 2003, 147:105-126.
Mainil J. Facteurs de virulence et propriétés spécifiques des souches invasives d'Escherichia coli: III) Production de toxines. Ann. Méd. Vét. 2003, 147:327-342.
Mainil J. Molecular and cellular pathogenesis of bacterial infections 2) Colonisation of the mucosae: adherence factors and their interaction with host cells. Ann. Méd. Vét. 2005, (Suppl. 2):5-14.
Mainil J. Molecular and cellular pathogenesis of bacterial infections 3) Development of disease: bacterial toxins and their interaction with host cells. Ann. Méd. Vét. 2005, (Suppl. 2):15-23.
Mainil J.G., Daube G. Verotoxigenic Escherichia coli from animals, humans and foods: who's who?. J. Appl. Microbiol. 2005, 98:1332-1344.
Mainil J.G., Bex F., Dreze P., Kaeckenbeeck A., Couturier M. Replicon typing of virulence plasmids of enterotoxigenic Escherichia coli isolates from cattle. Infect. Immun. 1992, 60:3376-3380.
Mainil J.G., Jacquemin E., Hérault F., Oswald E. Presence of pap-, sfa- and afa-related sequences in necrotoxigenic Escherichia coli isolates from cattle: evidence for new variants of the AFA family. Can. J. Vet. Res. 1997, 61:193-199.
Mainil J.G., Bez S., Jacquemin E., Kaeckenbeeck A. Les souches pathogènes d'Escherichia coli chez le chien et le chat: I) Détection des souches entérotoxinogènes (ETEC), entéropathogènes (EPEC), vérotoxinogènes (VTEC), entérohémorragiques (EHEC) et nécrotoxinogènes (NTEC). Ann. Méd. Vét. 1998, 142:39-46.
Mainil J.G., Daube G., Jacquemin E., Pohl P., Kaeckenbeeck A. Virulence plasmids of enterotoxigenic Escherichia coli isolates from piglets. Vet. Microbiol. 1998, 62:291-301.
Mainil J.G., Jacquemin E., Pohl P., Fairbrother J.M., Ansuini A., Le Bouguénec Ch., Ball H.J., De Rycke J., Oswald E. Comparison of necrotoxigenic Escherichia coli isolates from farm animals and humans. Vet. Microbiol. 1999, 70:123-135.
Mainil J., Wilbaux M., Jacquemin E., Imberechts H., Van Bost S. Les souches pathogènes d'Escherichia coli chez les chiens et chats: III) Données bactériologiques et cliniques sur les souches nécrotoxinogènes et sur celles positives pour des adhésines. Ann. Méd. Vét. 2001, 145:343-354.
Mainil J.G., Jacquemin E., Pohl P., Kaeckenbeeck A., Benz I. DNA sequences coding for the F18 fimbriae and AIDA adhesin are localized on the same plasmid in Escherichia coli isolates from piglets. Vet. Microbiol. 2002, 86:303-311.
Moseley S.L., Hardy J.W., Hucq I., Echeverria P., Falkow S. Isolation and nucleotide sequence détermination of a gene encoding a heat-stable enterotoxin of Escherichia coli. Infect. Immun. 1983, 39:1167-1174.
Moxley R.A., Smith D.R. Attaching-effacing Escherichia coli infections in cattle. Vet. Clin. North Am. Food Anim. Pract. 2010, 26:29-56.
Nagy B., Fekete P.Z. Enterotoxigenic Escherichia coli (ETEC) in farm animals. Vet. Res. 1999, 30:259-284.
Nataro J.P. Enteroaggregative Escherichia coli pathogenesis. Curr. Opin. Gastroenterol. 2005, 21:4-8.
Nataro J.P., Levine M.M. Escherichia coli diseases in humans in Escherichia coli. Domestic Animals and Humans 1994, 285-333. Cab International, Wallingford, Oxon, U.K. C.L. Gyles (Ed.).
Nataro J.P., Kaper J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998, 11:142-201.
Nataro J.P., Bopp C.A., Fields P.I., Kaper J.B., Strockbine N.A. Escherichia, Shigella and Salmonella. Manual of Clinical Microbiology 2011, 603-626. ASM Press, Washington, DC. 10th ed. J. Versalovic, K.C. Caroll, G. Funke, J.H. Jorgensen, M.L. Landry, D.W. Warnock (Eds.).
Niewerth U., Frey A., Voss T., Le Bouguénec C., Baljer G., Franke S., Schmidt M.A. The AIDA autotransporter system is associated with F18 and Stx2e in Escherichia coli isolates from pigs diagnosed with edema disease and postweaning diarrhea. Clin. Diagn. Lab. Immunol. 2001, 8:143-149.
O'Brien A.D., LaVeck G.D., Thompson M.R., Formal S.B. Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli. J. Infect. Dis. 1982, 146:763-769.
Orskov F., Orskov I. Escherichia coli serotyping and disease in man and animals. Can. J. Microbiol. 1992, 38:699-704.
Orskov I., Orskov F. Serologic classification of fimbriae. Curr. Top. Microbiol. Immunol. 1990, 151:71-90.
Oswald E., Schmidt H., Morabito S., Karch H., Marches O., Caprioli A. Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect. Immun. 2000, 68:64-71.
Oxhamre C., Richter-Dahlfors A. Membrane-damaging toxins: family of RTX toxins. Bacterial Protein Toxins 2003, 203-214. ASM Press, Washington D.C., U.S.A. D.L. Burns, J.T. Barbieri, B.H. Iglewski, R. Rappuoli (Eds.).
Pennington H. Escherichia coli O157. Lancet 2010, 376:1428-1435.
Philpott D.J., Ackerley C.A., Kiliaan A.J., Karmali M.A., Perdue M.H., Sherman P.M. Translocation of Verotoxin-1 across T84 monolayers: mechanism of bacterial toxin penetration of epithelium. Am. J. Physiol. 1997, 273:G1349-G1358.
Pickett C.L., Twiddy E.M., Belisie B.W., Holmes R.K. Cloning of genes that encode a new heat-labile enterotoxin of Escherichia coli. J. Bacteriol. 1986, 165:348-352.
Pickett C.L., Twiddy E.M., Coker C., Holmes R.K. Cloning, nucleotide sequence, and hybridization studies of the type IIb heat-labile enterotoxin gene of Escherichia coli. J. Bacteriol. 1989, 171:4945-4952.
Piérard D., De Greve H., Haesebrouck F., Mainil J.G. O157:H7 and O104:H4 Vero/Shiga toxin-producing Escherichia coli: respective role of cattle and humans. Vet. Res. 2012, 10.1186/1297-9716-43-13.
Pruimboom-Brees I.M., Morgan T.W., Ackermann M.R., Nyström E.D., Samuel J.E., Cornick N.A., Moon H.W. Cattle lack vascular receptors for Escherichia coli O157:H7 Shiga toxins. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:10325-10329.
Radostits O., Gay C.C., Hinchcliff K., Constable P.D. Veterinary Medicine - A Textbook of the Diseases of Cattle, Horses, Sheep, Pigs, and Goats. Part 2: Special Medicine: Diseases Associated with Bacteria - III. Colibacillosis of Newborn Calves, Piglets, Lambs, Kids and Foals 2007, Saunders Elsevier, Philadelphia, PA, U.S.A., pp. 851-876.
Rasheed K., Guzman-Verduzio L.M., Kupersztoch Y.M. Two precursors of the heat-stable enterotoxin of Escherichia coli: evidence for extracellular processing. Mol. Microbiol. 1990, 4:265-274.
Rasko D.A., Rosovitz M.J., Myers G.S., Mongodin E.F., Fricke W.F., Gajer P., Crabtree J., Sebaihia M., Thomson N.R., Chaudhuri R., Henderson I.R., Sperandio V., Ravel J. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J. Bacteriol. 2008, 190:6881-6893.
Saldana Z., Sanchez E., Xicohtencatl-Cortes J., Puente J.L., Giron J.A. Surface structures involved in plant stomata and leaf colonization by Shiga-toxigenic Escherichia coli O157:H7. Frontiers Microbiol. 2011, 2:1-9.
Sandvig K., Bergan J., Dyve A.B., Skotland T., Torgersen M.L. Endocytosis and retrograde transport of Shiga toxin. Toxicon 2010, 56:1181-1185.
Savarino S.J., Fasano A., Watson J., Martin B.M., Levine M.M., Guandalini S., Guerry P. Enteroaggregative Escherichia coli heat-stable enterotoxin 1 represents another subfamily of E. coli heat-stable toxin. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:3093-3097.
Scaletsky I., Silva M.L.M., Trabulsi L.R. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect. Immun. 1984, 45:534-536.
Scheutz F., Moller N.E., Frimodt-Moller J., Boisen N., Morabito S., Tozzoli R., Nataro J., Caprioli A. Characteristics of the enteroaggregative Shiga toxin/verotoxin-producing Escherichia coli O104:H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany May to June 2011. Euro Surveill. 2011, 16.
Scheutz F., Teel L.D., Beutin L., Piérard D., Buvens G., Karch H., Mellmann A., Caprioli A., Tozzoli R., Morabito S., Strockbine N.A., Melton-Celsa A.R., Sanchez M., Persson S., O'Brien A.D. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J. Clin. Microbiol. 2012, 50:2951-2963.
Schmidt M.A. LEE ways: tales of EPEC ATEC and EHEC. Cell Microbiol. 2010, 12:1544-1552.
Sears C.L., Kaper J.B. Enteric bacterial toxin: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 1996, 60:167-215.
Servin A.L. Pathogenesis of Afa/Dr diffusely adhering Escherichia coli. Clin. Microbiol. Rev. 2005, 18:264-292.
Sherlock O., Schembri M.A., Reisner A., Klemm P. Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J. Bacteriol. 2004, 186:8058-8065.
Smith H.W., Halls S. Observation by the ligated intestinal segment and oral inoculation methods on Escherichia coli infections in pigs, calves, lambs, and rabbits. J. Pathol. Bacteriol. 1967, 93:499-529.
Sojka W.J. Escherichia coli in Domestic Animals and Poultry. Part I General Characteristics and Biochemical Behaviour 1965, Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, U.K., pp. 1-63.
Stordeur P., Marlier D., Blanco J., Oswald E., Biet F., Dho-Moulin M., Mainil J. Examination of Escherichia coli from poultry for selected adhesin genes important in disease caused by mammalian pathogenic E. coli. Vet. Microbiol. 2002, 84:231-241.
Sussman M. Escherichia coli and human diseases. Escherichia coli - Mechanisms of Virulence 1997, 3-48. Cambridge University Press, Cambridge, U.K. M. Sussman (Ed.).
Toth I., Schmidt H., Dow M., Malik A., Oswald E., Nagy B. Transduction of porcine enteropathogenic Escherichia coli with a derivative of a Shiga toxin 2-encoding bacteriophage in a porcine ligated ileal loop system. Appl. Environ. Microbiol. 2003, 69:7242-7247.
Trabulsi L.R., Keller R., Gomes T.A.T. Typical and atypical enteropathogenic Escherichia coli. Emerg. Infect. Dis. 2002, 8:508-513.
Waddell T.E., Lingwood C.A., Gyles C.L. Interaction of Verotoxin 2e with pig intestine. Infect. Immun. 1996, 64:1714-1719.
Wasteson Y., Olsvik O., Skancke E., Bopp C.A., Fossum K. Heat-stable-enterotoxin-producing Escherichia coli strains isolated from dogs. J. Clin. Microbiol. 1988, 26:2564-2566.
Weintraub A. Enteroaggregative Escherichia coli: epidemiology, virulence and detection. J. Med. Microbiol. 2007, 56:4-8.
World Health Organization (W.H.O.) Scientific Working Group Escherichia coli diarrhoea. Bull. WHO 1980, 58:23-36.
Wray C., Woodward M.J. Escherichia coli infections in farm animals. Escherichia coli - Mechanisms of Virulence 1997, 49-84. Cambridge University Press, Cambridge, U.K. M. Sussman (Ed.).
Wu H., Fives-Taylor P.M. Molecular strategies for fimbrial expression and assembly. Crit. Rev. Oral Biol. Med. 2001, 12:101-115.