[en] Escherichia coli bacterial species is subdivided into several strains that are pathogenic for man and animals, on the basis of their specific properties and factors which are responsible for their pathogenic characters. The pathogenic strains are classically subdivided into strains with intestinal tropism (enterotoxigenic, enteropathogenic, enterohaemmorrhagic, verotoxigenic and enteroinvasive) and with extraintestinal tropism (uropathogenic and invasive). Invasive strains cause septicaemia and/or bacteraemia with localisations in different internal organs (systemic infections). If specific virulence properties and factors of strains with intestinal tropism are quite well known and described, those of strains with extraintestinal tropism are much less characterised, especially in animals. The purpose of this serie of review articles is to present the current knowledge on specific properties and factors of extraintestinal strains: adhesins and colonisation factors, transmucosal transfer and survival in blood and internal organs, toxicity. The fourth manuscript will deal with the invasive strains themselves, focusing on the necrotoxigenic strains. This third manuscript presents the current knowledge on toxins produced by invasive strains of E. coli: endotoxins, cytotoxic necrotising factors, cytolethal distending toxins and haemolytic toxins.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Van Bost, S.
Mainil, Jacques ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Bactériologie et pathologie des maladies bactériennes
Language :
French
Title :
Facteurs de virulence et propriétés spécifiques des souches invasives d'Escherichia coli : III) Production de toxines
Alternative titles :
[en] Virulence factors and specific properties of invasive Escherichia coli: III) Toxin production
ARAGON V., CHAO K., DREYFUS L.A. Effect of cytolethal distending toxin on F-actin assembly and cell division in Chinese hamster ovary cells. Infect. Immun., 1997, 65, 3774-3780.
BAG P.K., RAMAMURTHY T., NAIR U.B. Evidence for the presence of a receptor for the cytolethal distending toxin (CLDT) of Campylobacter jejuni on CHO and HeLa cell membranes and development of a receptor-based enzyme-linked immunosorbent assay for detection of CLDT. FEMS Microbiol. Lett., 1993, 114, 285-291.
BAUER M.E., WELCH R.A. Characterization of an RTX toxin from enterohemorrhagic Escherichia coli O157:H7. Infect. Immun., 1996, 64, 167-175.
BEUTIN L., PRADA J., ZIMMERMANN S., STEPHAN R., ORSKOV I., ORSKOV F. Enterohemolysin, a new type of hemolysin produced by some strains of enteropathogenic Escherichia coli. Zentrabl. Bakteriol. Hyg A, 1988, 267, 576-588.
BEUTIN L., MONTENEGRO M.A., ORSKOV I., ORSKOV F., PRADA J., ZIMMERMANN S., STEPHAN R. Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli. J. Clin. Microbiol., 1989, 27, 2559-2564.
BEUTIN L. Escherichia coli as a pathogen in dogs and cats. Vet. Res., 1999, 30, 285-298.
BEUTIN L. Plasmids in VTEC: their role in virulence and their use in typing. In: Duffy G., Garvey P., Coia J., Wasteson Y., Mc Dowell D.A. (Eds), Verocytotoxigenic Escherichia coli in Europe. 3: Pathogenicity and Virulence (Proceedings). Concerted Action CT98-3935, The National Food Centre, Dublin, 2000, 126-139.
BLANCO M., BLANCO J., BLANCO J.E., RAMOS J. Enterotoxigenic, verotoxigenic, and necrotoxigenic Escherichia coli isolated from cattle in Spain. Am. J. Vet. Res., 1993, 54, 1446-1451.
BONVENTRE P.F. The nomenclature of microbial toxins: problems and recommendations. In: Ajl S.J., Kadis S., Montie T.C. (Eds), Microbial toxins: a comprehensive treatise. Volume I: bacterial protein toxins. Academic Press: London, 1970, 29-66.
BOQUET P. The cytotoxic necrotizing factor 1 (CNF1) from Escherichia coli. Toxicon, 2001, 39, 1673-1680.
BOUZARI S., VATSALA B.R., VARGHESE A. In vitro adherence property of cytolethal distending toxin (CLDT) producing EPEC strains and effect of the toxin on rabbit intestine. Microb. Pathog., 1992, 12, 153-157.
CAPRIOLI A., FALBO V., RODA L.G., RUGGERI F.M., ZONA C. Partial purification and characterization of an Escherichia coli toxic factor that induces morphological cell alterations. Infect. Immun., 1983, 39, 1300-1306.
CAPRIOLI A., FALBO V., RUGGERI F.M., BALDASSARRI L., BISICCHIA R., IPPOLITO G., ROMALI E., DONELLI G. Cytotoxic necrotizing factor production by hemolytic strains of Escherichia coli causing extrain-testinal infections. J. Clin. Microbiol., 1987, 25, 146-149.
CHIEN C.C., TAYLOR N.S., GE Z., SCHAUER D.B., YOUNG Y.B., FOX J.G. Identification of cdtB homologues and cytolethal distending toxin activity in enterohepatic Helicobacter spp. J. Med. Microbiol., 2000, 49, 525-534.
CLARK C.G., JOHNSON S.T., EASY R.H., CAMPBELL J.L., RODGERS F.G. PCR for detection of cdt-III and the relative frequencies of cytolethal distending toxin variant-producing Escherichia coli isolates from humans and animals. J. Clin. Microbiol., 2002, 40, 2671-2674.
CLEMENT S. Etude de pathogenèse d'une souche d'Escherichia coli produisant CNF1 par l'infection expérimentale de porcelets (Mémoire présenté pour l'obtention du grade de Maître ès Sciences (MSc) en Sciences vétérinaires, Option Microbiologie). Université de Montréal: St Hyacinthe, 1997, 75 pages.
COMAYRAS C., TASCA C., PERES S.Y., DUCOMMUN B., OSWALD E., DE RYCKE J. Escherichia coli cytolethal distending toxin blocks the HeLa cell cycle at G2/M transition by preventing cdc2 protein kinase dephosphorylation and activation. Infect. Immun., 1997, 65, 5088-5095.
COOPER J.F., LEVIN J., WAGNER H.N. Quantitative comparison of in vitro and in vivo methods for detection of endotoxin. J. Lab. Clin. Med., 1971, 78, 138-148.
COPE L.D., LUMBLEY S., LATIMER J.L., KLESNEY-TAIT J., STEVENS M.K., JOHNSON L.S., PURVEN M., MUNSON R.S.Jr. A diffusible cytotoxin of Haemophilus ducreyi. Proc. Natl. Acad. Sci. USA, 1997, 94, 4056-4061.
CORTES-BRATTI X., CHAVES-OLARTE E., LAGERGAD T., THELESTAM M. The cytolethal distending toxin from the chancroid bacterium Haemophilus ducreyi induces cell-cycle arrest in the G2 phase. J. Clin. Invest., 1999, 103, 107-115.
CORTES-BRATTI X., CHAVES-OLARTE E., LAGERGAD T., THELESTAM M. Cellular internalization of cytolethal distending toxin from Haemophilus ducreyi. J. Clin. Invest., 2000, 68, 6903-6911.
DA SILVA A., DA SILVA LEITE D. Investigation of putative cdt gene in Escherichia coli isolates from pigs with diarrhea. Vet. Microbiol., 2002, 89, 195-200.
DENG K., LATIMER J.L., LEWIS D.A., HANSEN E.J. Investigation of the interaction among the components of the cytolethal distending toxin of Haemophilus ducreyi. Biochim. Bioph. Res. Commun., 2001, 285, 609-615.
DE RYCKE J., GUILLOT J.F., BOIVIN R. Cytotoxins in non-enterotoxigenic strains of Escherichia coli isolated from feces of diarrheic calves. Vet. Microbiol., 1987, 15, 137-150.
DE RYCKE J., OSWALD E., BOIVIN R. An in vivo assay for the detection of cytotoxic strains of Escherichia coli. Ann. Rech. Vét., 1989, 20, 39-46.
DE RYCKE J., GONZALEZ E.A., BLANCO J., OSWALD E., BLANCO M., BOIVIN R. Evidence for two types of cytotoxic necrotizing factor in human and animal clinical isolates of Escherichia coli. J. Clin. Microbiol., 1990, 28, 694-699.
DE RYCKE J., PLASSIART G. Toxic effects for lambs of cytotoxic necrotizing factor from Escherichia coli. Res. Vet. Sci., 1990, 49, 349-354.
DE RYCKE J., MAZARS P., NOUGAYREDE J.P., TASCA C., BOURY M., HERAULT F., VALETTE A., OSWALD E. Mitotic block and delayed lethality in HeLa epithelial cells exposed to Escherichia coli BM2-1 producing cytotoxic necrotizing factor 1. Infect. Immun., 1996, 64, 1694-1705.
DE RYCKE J., MILON A., OSWALD E. Necrotoxic Escherichia coli (NTEC): two emerging categories of human and animal pathogens. Vet. Res., 1999, 30, 221-233.
DE RYCKE J., OSWALD E. Cytolethal distending toxin (CDT): a bacterial weapon to control host cell proliferation? FEMS Microbiol. Lett., 2001, 203, 141-148.
DOZOIS C.M., CURTISS R. III. Pathogenic diversity of Escherichia coli and the emergence of «exotic» islands in the gene stream. Vet. Res., 1999, 30, 157-180.
ELLIOTT S.J., SRINIVAS S., ALBERT M.J., ALAM K., ROBINS-BROWNE R.M., GUNZBURG S.T., MEE B.J., CHANG B.J. Characterization of the roles of hemolysin and other toxins in enteropathy caused by alpha-hemolytic Escherichia coli linked to human diarrhea. Infect. Immun., 1998, 66, 2040-2051.
ELWELL C.A., DREYFUS L.A. DNase I homologous residues in CdtB are critical for cytolethal distending toxin-mediated cell cycle arrest. Mol. Microbiol., 2000, 37, 952-963.
ELWELL C., CHAO K., PATEL K., DREYFUS L. Escherichia coli CdtB mediates cytolethal distending toxin all cycle arrest. Infect. Immun., 2001, 69, 3418-3422.
FABBRI A., GAUTHIER M., BOQUET P. The 5′ region of cnf1 harbours a translational regulatory mechanism for CNF1 synthesis and encodes the cell-binding domain of the toxin. Mol. Microbiol., 1999, 33, 108-118.
FALBO V., FAMIGLIETTI M., CAPRIOLI A. Gene block encoding production of cytotoxic necrotizing factor 1 and hemolysin in Escherichia coli isolates from extrain-testinal infections. Infect. Immun., 1992, 60, 2182-2187.
FALBO V., PACE T., PICCI L., PIZZI E., CAPRIOLI A. Isolation and nucleotide sequence of the gene encoding cytotoxic necrotizing factor 1 of Escherichia coli. Infect. Immun., 1993, 61, 4909-4914.
FALKOW S. Molecular Koch's postulates applied to microbial pathogenicity. Rev. Infect. Dis., 1988, 10, S274-S276.
FALZANO L., QUARANTA M.G., TRAVAGLIONE S., FILIPPINI P., FABBRI A., VIORA M., DONELLI G., FIORENTINI C. Cytotoxic necrotizing factor 1 enhances reactive oxygen species-dependent transcription and secretion of proinflammatory cytokines in human uroepithelial cells. Infect. Immun., 2003, 71, 4178-4181.
FLATAU G., LEMICHEZ E., GAUTHIER M., CHARDIN P., PARIS S., FIORENTINI C., BOQUET P. Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature, 1997, 387, 729-733.
FOURNOUT S., DOZOIS C.M., ODIN M., DESAUTELS C., PERES S., HERAULT F., DAIGLE F., SEGAFREDO C., LAFFITE J., OSWALD E., FAIRBROTHER J.M., OSWALD I.P. Lack of a role of cytotoxic necrotizing factor 1 toxin from Escherichia coli in bacterial pathogenicity and host cytokine response in infected germfree piglets. Infect. Immun., 2000, 68, 839-847.
FREER J.M. Toxins as virulence factors of Gram-positive pathogenic bacteria of veterinary importance. In: Roth J.A. (Ed.), Virulence mechanisms of bacterial pathogens. ASM Press : Washington, 1988, 264-288.
FRISAN T., CORTES-BRATTI X., THELESTAM M. Cytolethal distending toxins and activation of DNA damage-dependent checkpoint responses. Int. J. Med. Microbiol., 2002, 291, 495-499.
FRISK A., LEBENS M., JOHANSSON C., AHMED H., SVENSSON L., AHLMAN K., LAGERGAD T. The role of different protein components from the Haemophilus ducreyi cytolethal distending toxin in the generation of cell toxicity. Microb. Pathog., 2001, 30, 313-324.
GERHARD R., SCHMIDT G., HOFMANN F., AKTORIES K. Activation of Rho GTPases by Escherichia coli cytotoxic necrotizing factor 1 increases intestinal permeability in Caco-2 cells. Infect. Immun., 1998, 66, 5125-5131.
GHILARDI A.C., GOMES T.A., TRABULSI L.R. Production of cytolethal distending toxin and other virulence characteristics of Escherichia coli strains of sero-group O86. Mem. Inst. Oswaldo Cruz, 2001, 96, 703-708.
GRIFFITHS E., CHART H., STEVENSON P. High-affinity iron uptake systems and bacterial virulence. In: Roth J.A. (Ed.), Virulence mechanisms of bacterial pathogens. ASM Press : Washington, 1988, 121-137.
GYLES C.L. Escherichia coli verotoxins and other cytotoxins. In: Gyles C.L. (Ed.), Escherichia coli in domestic animals and humans. CAB International: Wallingford, 1994, 365-398.
HACKER J., KAPER J.B. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol., 2000, 54, 641-679.
HAREL J., MARTIN C. Virulence gene regulation in pathogenic Escherichia coli. Vet. Res., 1999, 30, 131-156.
HORIGUCHI Y. Escherichia coli cytotoxic necrotizing factors and Bordetella dermonecrotic toxin: the dermonecrosis-inducing toxins activating Rho small GTPases. Toxicon, 2001, 39, 1619-1627.
HULL S. Escherichia coli lipopolysaccharide in pathogenesis and virulence. In: Sussman M. (Ed.), Escherichia coli: mechanisms of virulence. Cambridge University Press: Cambridge, 1997, 145-167.
JANKA A., BIELASZEWSKA M., DOBRINDT U., GREUNE L., SCHMIDT M.A., KARCH H. Cytolethal distending toxin gene cluster in enterohemorrhagic Escherichia coli O157:H- and O157:H7: characterization and evolutionary considerations. Infect. Immun., 2003, 71, 3634-3638.
JOHNSON J.R., O'BRYAN T.T., LOW D.A., LING G., DELAVARI P., FASCHING C., RUSSO T.A., CARLINO U., STELL A.L. Evidence of commonality between canine and human extraintestinal pathogenic Escherichia coli strains that express papG allele III. Infect. Immun., 2000, 68, 3327-3336.
JOHNSON W.M., LIOR H. Response of chinese ovary hamster cells to a cytolethal distending toxin (CDT) of Escherichia coli and possible misinterpretation as heat-labile (LT) enterotoxin. FEMS Microbiol. Lett., 1987a, 43, 19-23.
JOHNSON W.M., LIOR H. Production of Shiga toxin and a cytolethal distending toxin (CLDT) produced by sero-groups of Shigella spp. FEMS Microbiol. Lett., 1987b, 48, 235-238.
JOHNSON W.M., LIOR H. A new heat-labile cytolethal distending toxin (CLDT) produced by Escherichia coli isolates from clinical material. Microb. Pathog., 1988a, 4, 103-113.
JOHNSON W.M., LIOR H. A new heat-labile cytolethal distending toxin (CLDT) produced by Campylobacter spp. Microb. Pathog., 1988b, 4, 115-126.
JORGENSEN S.E., SHORT E.C., HURTZ H.J., MUSSEN H.K., WU G.K. Studies on the origin of the alpha-haemolysin produced by Escherichia coli. J. Med. Microbiol., 1976, 9, 173-189.
KAYSER H. Ueber Bakterienshämolyse, im Besonderen das Colilysin. Zeitschr. Hyg. Infektionkrankh., 1903, 42, 118-138.
KORONAKIS V., HUGHES C. Hemolysin. In: Donnenberg M.S. (Ed), Escherichia coli: virulence mechanisms of a versatile pathogen. Academic Press: London, 2002, 361-378.
KOSTIA S., VEIJALAINEN P., HIRVI U., HANNINEN M.L. Cytolethal distending toxin B gene (cdtB) homologues in taxa 2, 3 and 8 and in six canine isolates of Helicobacter sp. Flexispira. J. Med. Microbiol., 2003, 52, 103-108.
LANDRAUD L., GIBERT M., POPOFF M.R., BOQUET P., GAUTHIER M. Expression of cnf1 by Escherichia coli J96 involves a large upstream DANN region including the hlyCABD operon, and is regulated by the RfaH protein. Mol. Microbiol., 2003, 47, 1653-1667.
LARA-TEJERO M., GALAN J.E. A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science, 2000, 290, 354-357.
LARA-TEJERO M., GALAN J.E. CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect. Immun., 2001, 69, 4358-4365.
LERM M., SELZER J., HOFFMEYER A., RAPP U.R., AKTORIES K., SCHMIDT G. Deamidation of Cdc42 and Rac by Escherichia coli cytotoxic necrotizing factor 1: activation of c-Jun N-terminal kinase in HeLa cells. Infect. Immun., 1999, 67, 496-503.
LEVIN J., TOMASULO P.A., OSER R.S. Detection of endotoxin in human blood and demonstration of an inhibitor. J. Lab. Clin. Med., 1970, 75, 903-911.
LIN J.W., CHEN L.M., CHEN H.Y., WENG S.F. Identification and analysis of the regulatory region R&R* with the cnf1 gene encoding the cytotoxic necrotizing factor type 1 that closely links to the lux regulon of Vibrio fischeri. Biochim. Biophys. Res. Commun., 1998, 250, 462-465.
LOCKMAN H.A., GILLESPIE R.A., BAKER B.D., SHAKHNOVICH E. Yersinia pseudotuberculosis produces a cytotoxic necrotizing factor. Infect. Immun., 2002, 70, 2708-2714.
LUDWIG A., TENGEL C., BAUER S., BUBERT A., BENZ B., MALBENKOPF H.J., GOEBEL W. SlyA, a regulatory protein from Salmonella typhimurium, induces a haemolytic and pore-forming protein in Escherichia coli. Mol. Gen. Genet., 1995, 249, 474-486.
LUDWIG A., GOEBEL W. Haemolysins of Escherichia coli. In: Sussman M. (Ed.), Escherichia coli: mechanisms of virulence. Cambridge University Press: Cambridge, 1997, 281-329.
MAC LAREN D.M. Soft tissue infection and septicaemia. In: Sussman M. (Ed.), Escherichia coli: mechanisms of virulence. Cambridge University Press: Cambridge, 1997, 469-494.
MAINIL J., JACQUEMIN E., HERAULT 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. Shiga/Verocytotoxins and Shiga/Verotoxigenic Escherichia coli in animals. Vet. Res., 1999, 30, 235-257.
MAINIL J., WILBAUX M., JACQUEMIN E., OSWALD E., IMBERECHTS H., VAN BOST S. Les souches pathogènes d'Escherichia coli chez les chiens et les 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., JACQUEMIN E., OSWALD E. Prevalence and identity of cdt-related sequences in necrotoxigenic Escherichia coli. Vet. Microbiol., 2003, 94, 159-165.
MAO X., DI RIENZO J.M. Functional studies of the recombinant subunits of a cytolethal distending holotoxin. Cell. Microbiol., 2002, 4, 245-255.
MEYERS K., REED S., CLEM M., BAYLY W. Circulating endotoxin-like substance(s) and altered hemostasis in horses with gastrointestinal disorders: an interim report. Am. J. Vet. Res., 1982, 43, 2233-2238.
MILLS M., MEYSICK K.C., O'BRIEN A.D. Cytotoxic necrotizing factor type 1 of uropathogenic Escherichia coli kills cultured human uroepithelial 5637 cells by an apoptotic mechanism. Infect. Immun., 2000, 68, 5869-5880.
NAGY B., FEKETE P.Zs. Enterotoxigenic Escherichia coli (ETEC) in farm animals. Vet. Res., 1999, 30, 259-284.
OKEKE I.N., LAMIKANRA A., STEINRÜCK H., KAPER J.B. Characterization of Escherichia coli strains from cases of childhood in provincial southwestern Nigeria. J. Clin. Microbiol., 2000, 38, 7-12.
OKUDA J., KURAZANO H., TAKEDA Y. Distribution of the cytolethal distending toxin A gene (cdtA) among species of Shigella and Vibrio, and cloning and sequencing of the cdt gene from Shigella dysenteriae. Microb. Pathog., 1995, 18, 167-172.
OKUDA J., KUKUMOTO H., TAKEDA Y., NISHIHICHI M. Examination of diarrheagenicity of cytolethal distending toxin: suckling mouse response to the products of the cdtABC genes of Shigella dysenteriae. Infect. Immun., 1997, 65, 428-433.
OSWALD E., DE RYCKE J., GUILLOT J.F., BOIVIN R. Cytotoxic effect of multinucleation in HeLa cultures associated with the presence of Vir plasmid in Escherichia coli strains. FEMS Microbiol. Lett., 1989, 58, 95-100.
OSWALD E., DE RYCKE J. A single protein of 110 kDa is associated with the multinucleating and necrotizing activity coded by the Vir plasmid of Escherichia coli. FEMS Microbiol. Lett., 1990, 68, 279-284.
OSWALD E., POHL P., JACQUEMIN E., LINTERMANS P., VAN MUYLEM K., O'BRIEN A.D., MAINIL J. Specific DNA probes to detect Escherichia coli strainns producing cytotoxic necrotising factor type 1 or type 2. J. Med. Microbiol., 1994a, 40, 428-434.
OSWALD E., SUGAI M., LABIGNE A., WU H.C., FIORENTINI C., BOQUET P., O'BRIEN A.D. Cytotoxic necrotizing factor type 2 produced by virulent Escherichia coli modifies the small GTP-binding proteins Rho involved in assembly of actin stress fibers. Proc. Natl. Acad. Sci. USA, 1994b, 91, 3814-3818.
OSWALD E., TABOURET M., BOIVIN R., DE RYCKE J. Detection of Escherichia coli strains producing the cytotoxic necrotizing factor type two (CNF2) by enzyme-linked immunosorbent assay. Vet. Microbiol., 1994c, 40, 209-218.
PATON J.C., PATON A.W. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev., 1998, 11, 450-479.
PERES S.Y., MARCHES O., DAIGLE F., NOUGAYREDE J.P., HERAULT F., TASCA C., DE RYCKE J., OSWALD E. A new cytolethal distending toxin (CDT) from Escherichia coli producing CNF2 blocks HeLa cell division in G2/M phase. Mol. Microbiol., 1997, 24, 1095-1107.
PICKETT C.L., COTTLE D.L., PESCI E.C., BIKAH G. Cloning, sequencing, and expression of the Escherichia coli cytolethal distending toxin genes. Infect. Immun., 1994, 62, 1046-1051.
PICKETT C.L., PESCI S.C., CATTLE D.L., RUSSEL G., NALCA ERDEM A., ZEYTIN H. Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB genes. Infect. Immun., 1996, 64, 2070-2078.
POHL P., OSWALD E., VAN ROBAEYS G., STOCKMANS F., LINTERMANS P., MAINIL J. Tests simples pour le diagnostic présumé des Escherichia coli isolées principalement chez les bovins et productrices des cytotoxines nécrosantes (CNF). Ann. Méd. Vét., 1993, 137, 503-505.
PURDY D., BUSWELL C.M., HODGSON A.E., McALPINE K., HENDERSON I., LEACH A.A. characterisation of cytolethal distending toxin (CDT) mutants of Campylobacter jejuni. J. Med. Microbiol., 2000, 49, 473-479.
RENNIE R.P., ARBUTHNOTT J.P. Partial characterization of Escherichia coli haemolysin. J. Med. Microbiol., 1974, 7, 179-188.
RIPPERE-LAMPE K.E., O'BRIEN A.D., CORION R., LOCKMAN H.A. Mutation of the gene encoding cytotoxic necrotizing factor type 1 (cnf1) attenuates the virulence of uropathogenic Escherichia coli. Infect. Immun., 2001, 69, 3954-3964.
ROBERTSON D.C. Pathogenesis and enterotoxins of diarrheagenic Escherichia coli. In: Roth J. A. (Ed.), Virulence mechanisms of bacterial pathogens. ASM Press: Washington, 1988, 241-263.
ROUX E., YERSIN A. Contribution à l'étude de la diphtérie. Ann. Inst. Pasteur, 1888, 2, 629-661.
RUTTER J.M. Bacterial toxins as virulence determinants of veterinary pathogens: an overview. In: Roth J.A. (Ed.), Virulence mechanisms of bacterial pathogens. ASM Press: Washington, 1988, 213-227.
SCHMIDT G., SEHR P., WILM J., SELZER J., MANN M., AKTORIES K. Gln63 Rho is deaminated by Escherichia coli cytotoxic necrotizing factor-1. Nature, 1997, 387, 725-729.
SCHMIDT H., KARCH H., BEUTIN L. The large sized plasmids of enterohemorrhagic Escherichia coli O157 strains encode hemolysins which are presumably members of the E. coli α-hemolysin family. FEMS Microbiol. Lett., 1994, 117, 189-196.
SCOTT D.A., KAPER J.B. Cloning and sequencing of the genes encoding Escherichia coli cytolethal distending toxin. Infect. Immun., 1994, 62, 244-251.
SHEWEN P.E. Cytocidal toxins of Gram-negative rods. In: Roth J.A. (Ed.), Virulence mechanisms of bacterial pathogens. ASM Press: Washington, 1988, 228-240.
SMITH H.W. The haemolysins of Escherichia coli. J. Pathol. Bacteriol., 1963, 85, 197-211.
SMITH H.W. A search for transmissible pathogenic characters in invasive strains of Escherichia coli: the discovery of a plasmid-controlled toxin and a plasmid-controlled lethal character closely associated, or identical, with Colicin V. J. Gen. Microbiol., 1974, 83, 95-111.
SMITH H.W. Observations on Escherichia coli infection in calves. In: Rutter J.M. (Ed.), Proceedings of the First Seminar on «Pathology», in the CEC Programme of Coordination of Research in Beef Production. Perinatal Ill-Health in Calves, 1975, Bruxelles. European Commission: Bruxelles, 1975, 47-59.
SMITH H.W. Transmissible pathogenic characteristics of invasive strains of Escherichia coli. J. Am. Vet. Med. Assoc., 1978, 173, 601-607.
STARCIC M. JOHNSON J.R., STELL A.L., VEN DER GOOT J., HENDRICKS H.G., VAN VORSTENBOSCH C., VAN DIJK L., GAASTRA W. Haemolytic Escherichia coli isolated from dogs with diarrhea have characteristics of both uropathogenic and necrotoxigenic strains. Vet. Microbiol., 2002, 85, 361-375.
STOPIK K., HERTVRIG S., APPEL B., BEUTIN L. Cloning of genes encoding Escherichia coli beta-hemolysin, a new type of hemolysin associated with VTEC from pigs. In: Duffy G., Garvey P., Coia J., Wasteson Y., Mc Dowell D.A. (Eds), Verocytotoxigenic Escherichia coli in Europe. 3: Pathogenicity and Virulence (Proceedings). Concerted Action CT98-3935, The National Food Centre, Dublin, 2000, 200.
SUGAI M., KAWAMOTO T., PERES S.Y., UENO Y., KOMATSUWAZA H., FUJIWARA T., KURIHAWA H., SUGINAKA H., OSWALD E. The cell cycle-specific growth-inhibitory factor produced by Actinobacillus actinomycetemcomitans is a cytolethal distending toxin. Infect. Immun., 1998, 66, 5008-5019.
SUGAI M., HATAKAZI K., MOGAMI A., OHTA H., PERES S.Y., HERAULT F., HORIGUCHI Y., MASUDA M., UENO Y., KOMATSUWAZA H., SUGINAKA H., OSWALD E. Cytotoxic necrotizing factor type 2 produced by pathogenic Escherichia coli deamidates a Gln residue in the conserved G-3 domain of the Rho family and preferentially inhibits the GTPase activity of RhoA and Rac1. Infect. Immun., 1999, 67, 6550-6557.
TABOURET M., DE RYCKE J. Detection of cytotoxic necrotising factor (CNF) in extracts of Escherichia coli strains by enzyme-linked immunosorbent assay. J. Med. Microbiol., 1990, 32, 73-81.
TOMASULO P.A., LEVIN J., MURPHY P.A., WINKELSTEIN J.A. Biological activities of tritiated endotoxins: Correlation of the Limulus lysate assay with rabbit pyrogen and complement-activation assays for endotoxin. J. Lab. Clin. Med., 1977, 89, 308-315.
TOTH I., OSWALD E., MAINIL J., AWAD-MASALMEH M., NAGY B. Characterization of intestinal Cnf+ and CDT+ Escherichia coli from weaned piglets. Int. J. Med. Microbiol., 2000a, 290, 539-542.
TOTH I., OSWALD E., SZABO B., BARCS I., EMODY L. Virulence markers of human uropathogenic Escherichia coli strains isolated in Hungary. Adv. Experim. Med. Biol., 2000b, 485, 335-338.
TOTH I., HERAULT F., BEUTIN L., OSWALD E. Production of cytolethal distending toxins by human and animal pathogenic Escherichia coli strains: establishment of the existence of a new cdt variant (type IV). J. Clin. Microbiol., 2003, 41, 4285-4291.
TRAVAGLIONE S., FALZANO L., FABBRI A., STRINGARO A., FAIS S., FIORENTINI C. Epithelial cells and expression of the phagocytic marker CD68: scavenging of apoptotic bodies following Rho activation. Toxicol. in Vitro, 2002, 16, 405-411.
UHLIN B.E., MIZUNOE Y., OSCARSSON J., WAI S.N., WESTERMARK M. The cytolysin A from Escherichia coli. In: 4th International Workshop «Shiga toxin (verocytotoxin)-producing Escherichia coli infections», Kyoto, Japan. 2000, 47.
VAN BOST S., MAINIL J. Reproduction of lesions and clinical signs with a CNF2-producing Escherichia coli in neonatal calves. Adv. Exp. Med., 1999, 473, 125-128.
VAN BOST S., ROELS S., MAINIL J. Necrotoxigenic Escherichia coli type 2 invade and cause diarrhoea during experimental infection in colostrum- restricted newborn calves. Vet. Microbiol., 2001, 81, 315-329.
VAN BOST S., ROELS S., OSWALD E., MAINIL J. Putative roles of CNF2 and CDTIII toxins in experimental infections with necrotoxigenic Escherichia coli type 2 (NTEC2) strains in calves. Microbes Infect., 2003, 5, 1189-1193.
VAN HEYNINGEN W.E. General characteristics. In: Ajl S.J., Kadis S., Montie T.C. (Eds), Microbial toxins: a comprehensive treatise. Volume I: Bacterial protein toxins. Academic Press : London, 1970, 1-28.
WALTON J.R., SMITH D.H. New hemolysin (γ) produced by Escherichia coli. J. Bacteriol., 1969, 98, 304-305.
WELCH R.A., HULL R., FALKOW S. Molecular cloning and physical characterization of a chromosomal hemolysin from Escherichia coli. Infect. Immun., 1983, 42, 178-186.
WHITFIELD C., KENLEYSIDE W.J., CLARKE B.R. Structure, function and synthesis of surface polysaccharides in Escherichia coli. In: Gyles C.L. (Ed.), Escherichia coli in domestic animals and humans. CAB International: Wallingford, 1994, 437-494.
WRAY C., PIERCY D.W.T., CARROLL P.J., COOLEY W.A. Experimental infection of neonatal pigs with CNF toxin-producing strains of Escherichia coli. Res. Vet. Science, 1993, 54, 290-298.
YAMAMOTO S., TERAI A., YURI K., KURAZONO H., TAKEDA Y., YOSHIDA O. Detection of urovirulence factors in Escherichia coli by multiplex polymerase chain reaction. FEMS Immunol. Med. Microbiol., 1995, 12, 85-90.
YOUNG Y.B., CHIEN C.C., KNOX K.A., TAYLOR N.S., SCHAUER D.B., FOX J.G. Cytolethal distending toxin in avian and human isolates of Helicobacter pullorum. J. Infect. Dis., 2000, 182, 620-623.