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O104:H4 Pathogenesis: an Enteroaggregative /Shiga Toxin-Producing Explosive Cocktail of High Virulence

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  • Author: Fernando Navarro-Garcia1
  • Editors: Vanessa Sperandio2, Carolyn J. Hovde3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Cell Biology, Centro de Investigación y de Estudios Avanzados del IPN, México DF, Mexico; 2: University of Texas Southwestern Medical Center, Dallas, TX; 3: University of Idaho, Moscow, ID
    • Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.EHEC-0008-2013
  • Received 08 May 2013 Accepted 29 July 2013 Published 14 November 2014
  • Fernando Navarro-Garcia, fnavarro@cell.cinvestav.mx
image of <span class="jp-italic">Escherichia coli</span> O104:H4 Pathogenesis: an Enteroaggregative <span class="jp-italic">E. coli</span>/Shiga Toxin-Producing <span class="jp-italic">E. coli</span> Explosive Cocktail of High Virulence

  • Abstract:

    A major outbreak caused by of serotype O104:H4 spread throughout Europe in 2011. This large outbreak was caused by an unusual strain that is most similar to enteroaggregative (EAEC) of serotype O104:H4. A significant difference, however, is the presence of a prophage encoding the Shiga toxin, which is characteristic of enterohemorrhagic (EHEC) strains. This combination of genomic features, associating characteristics from both EAEC and EHEC, represents a new pathotype. The 2011 O104:H4 outbreak of hemorrhagic diarrhea in Germany is an example of the explosive cocktail of high virulence and resistance that can emerge in this species. A total of 46 deaths, 782 cases of hemolytic-uremic syndrome, and 3,128 cases of acute gastroenteritis were attributed to this new clone of EAEC/EHEC. In addition, recent identification in France of similar O104:H4 clones exhibiting the same virulence factors suggests that the EHEC O104:H4 pathogen has become endemically established in Europe after the end of the outbreak. EAEC strains of serotype O104:H4 contain a large set of virulence-associated genes regulated by the AggR transcription factor. They include, among other factors, the pAA plasmid genes encoding the aggregative adherence fimbriae, which anchor the bacterium to the intestinal mucosa (stacked-brick adherence pattern on epithelial cells). Furthermore, sequencing studies showed that horizontal genetic exchange allowed for the emergence of the highly virulent Shiga toxin-producing EAEC O104:H4 strain that caused the German outbreak. This article discusses the role these virulence factors could have in EAEC/EHEC O104:H4 pathogenesis.

  • Citation: Navarro-Garcia F. 2014. O104:H4 Pathogenesis: an Enteroaggregative /Shiga Toxin-Producing Explosive Cocktail of High Virulence. Microbiol Spectrum 2(6):EHEC-0008-2013. doi:10.1128/microbiolspec.EHEC-0008-2013.

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/content/journal/microbiolspec/10.1128/microbiolspec.EHEC-0008-2013
2014-11-14
2018-07-16

Abstract:

A major outbreak caused by of serotype O104:H4 spread throughout Europe in 2011. This large outbreak was caused by an unusual strain that is most similar to enteroaggregative (EAEC) of serotype O104:H4. A significant difference, however, is the presence of a prophage encoding the Shiga toxin, which is characteristic of enterohemorrhagic (EHEC) strains. This combination of genomic features, associating characteristics from both EAEC and EHEC, represents a new pathotype. The 2011 O104:H4 outbreak of hemorrhagic diarrhea in Germany is an example of the explosive cocktail of high virulence and resistance that can emerge in this species. A total of 46 deaths, 782 cases of hemolytic-uremic syndrome, and 3,128 cases of acute gastroenteritis were attributed to this new clone of EAEC/EHEC. In addition, recent identification in France of similar O104:H4 clones exhibiting the same virulence factors suggests that the EHEC O104:H4 pathogen has become endemically established in Europe after the end of the outbreak. EAEC strains of serotype O104:H4 contain a large set of virulence-associated genes regulated by the AggR transcription factor. They include, among other factors, the pAA plasmid genes encoding the aggregative adherence fimbriae, which anchor the bacterium to the intestinal mucosa (stacked-brick adherence pattern on epithelial cells). Furthermore, sequencing studies showed that horizontal genetic exchange allowed for the emergence of the highly virulent Shiga toxin-producing EAEC O104:H4 strain that caused the German outbreak. This article discusses the role these virulence factors could have in EAEC/EHEC O104:H4 pathogenesis.

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O104:H4 Pathogenesis: an Enteroaggregative /Shiga Toxin-Producing Explosive Cocktail of High Virulence
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Citation: Navarro-Garcia F. 2014. o104:h4 pathogenesis: an enteroaggregative /shiga toxin-producing explosive cocktail of high virulence. microbiolspec 2(6): doi:10.1128/microbiolspec.EHEC-0008-2013
/content/microbiolspec/10.1128/microbiolspec.EHEC-0008-2013.fig1
FIGURE 1

Hybrid characteristics of O104:H4 outbreak strain (EAEC/STEC). Schematic representation of the genes harbored by O104:H4; the main genes from EAEC or STEC are highlighted: (coding for Stx 2), , , and (coding for the SPATE proteins); Pic, protein involved in intestinal colonization; SigA, a homolog of Pet, with cytotoxic activity; SepA, a colonization factor of ), (coding for ShET1, a holotoxin AB5), (coding for Iha, a STEC adhesin that is an IrgA homolog), , , , (genes from EAEC plasmids coding for transcription regulator, AAF/I, dispersin, and dispersin transporter, respectively), (coding for Lpf of STEC), (coding for a cluster for Tellurite resistance), CTX-M15 and TEM-1 (antibiotic resistance genes). SigA and SepA are SPATEs detected mainly in sp. doi:10.1128/microbiolspec.EHEC-0008-2013.f1

microbiolspec/2/6/EHEC-0008-2013-fig1_thmb.gif
microbiolspec/2/6/EHEC-0008-2013-fig1.gif
Image of FIGURE 1

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FIGURE 1

Hybrid characteristics of O104:H4 outbreak strain (EAEC/STEC). Schematic representation of the genes harbored by O104:H4; the main genes from EAEC or STEC are highlighted: (coding for Stx 2), , , and (coding for the SPATE proteins); Pic, protein involved in intestinal colonization; SigA, a homolog of Pet, with cytotoxic activity; SepA, a colonization factor of ), (coding for ShET1, a holotoxin AB5), (coding for Iha, a STEC adhesin that is an IrgA homolog), , , , (genes from EAEC plasmids coding for transcription regulator, AAF/I, dispersin, and dispersin transporter, respectively), (coding for Lpf of STEC), (coding for a cluster for Tellurite resistance), CTX-M15 and TEM-1 (antibiotic resistance genes). SigA and SepA are SPATEs detected mainly in sp. doi:10.1128/microbiolspec.EHEC-0008-2013.f1

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.EHEC-0008-2013
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FIGURE 2

Adherence patterns of EAEC, STEC, and O104:H4 outbreak strain to epithelial cells. Subconfluent epithelial cell cultures are infected with the different bacterial strains. Cells are fixed and stained with Giemsa stain. From Scalesky et al. 1999. 3410; Paton et al. 2001. 6999; and Martina Bielaszewska. http://ecdc.europa.eu/en/press/events/Documents/22-231111-Breakthroughs-in-molecular-epidemiology-Bielaszewska.pdf. doi:10.1128/microbiolspec.EHEC-0008-2013.f2

microbiolspec/2/6/EHEC-0008-2013-fig2_thmb.gif
microbiolspec/2/6/EHEC-0008-2013-fig2.gif
Image of FIGURE 2

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FIGURE 2

Adherence patterns of EAEC, STEC, and O104:H4 outbreak strain to epithelial cells. Subconfluent epithelial cell cultures are infected with the different bacterial strains. Cells are fixed and stained with Giemsa stain. From Scalesky et al. 1999. 3410; Paton et al. 2001. 6999; and Martina Bielaszewska. http://ecdc.europa.eu/en/press/events/Documents/22-231111-Breakthroughs-in-molecular-epidemiology-Bielaszewska.pdf. doi:10.1128/microbiolspec.EHEC-0008-2013.f2

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.EHEC-0008-2013
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FIGURE 3

Transmission electron microscopy (TEM) of Stx2 phage (P13374) induction from lysogenic strain K-12 strain TPE2364 (C600) infected with phage lysates of O104:H4 strain CB13374. (A, B) Ultrathin sections of two bacterial cells (TPE2364) with maturating virion particles within the cytoplasm indicated by arrows (bars, 500 nm). (C) TEM of CsCl-purified, negatively stained phage (P13374) particles released by strain TPE2364 (bar, 100 nm). Short tails (arrows) and a hexagonal head are shown. From Beutin et al. 2012. 10444. doi:10.1128/microbiolspec.EHEC-0008-2013.f3

microbiolspec/2/6/EHEC-0008-2013-fig3_thmb.gif
microbiolspec/2/6/EHEC-0008-2013-fig3.gif
Image of FIGURE 3

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FIGURE 3

Transmission electron microscopy (TEM) of Stx2 phage (P13374) induction from lysogenic strain K-12 strain TPE2364 (C600) infected with phage lysates of O104:H4 strain CB13374. (A, B) Ultrathin sections of two bacterial cells (TPE2364) with maturating virion particles within the cytoplasm indicated by arrows (bars, 500 nm). (C) TEM of CsCl-purified, negatively stained phage (P13374) particles released by strain TPE2364 (bar, 100 nm). Short tails (arrows) and a hexagonal head are shown. From Beutin et al. 2012. 10444. doi:10.1128/microbiolspec.EHEC-0008-2013.f3

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.EHEC-0008-2013
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FIGURE 4

Schematic representation of O104:H4 virulence factors and their targets on the mucosal epithelium. The targets and virulence factors are extrapolated from their known function in other pathogens, and the action mechanism for ShET1 is hypothetical. doi:10.1128/microbiolspec.EHEC-0008-2013.f4

microbiolspec/2/6/EHEC-0008-2013-fig4_thmb.gif
microbiolspec/2/6/EHEC-0008-2013-fig4.gif
Image of FIGURE 4

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FIGURE 4

Schematic representation of O104:H4 virulence factors and their targets on the mucosal epithelium. The targets and virulence factors are extrapolated from their known function in other pathogens, and the action mechanism for ShET1 is hypothetical. doi:10.1128/microbiolspec.EHEC-0008-2013.f4

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.EHEC-0008-2013
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