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E. coli Nissle 1917 Affects Salmonella adhesion to porcine intestinal epithelial cells.

Schierack P, Kleta S, Tedin K, Babila JT, Oswald S, Oelschlaeger TA, Hiemann R, Paetzold S, Wieler LH - PLoS ONE (2011)

Bottom Line: Another E. coli strain expressing F1C fimbriae was also adherent to IPEC-J2 cells, and was similarly inhibitory against Salmonella invasion like EcN.We propose that EcN affects Salmonella adhesion through secretory components.This mechanism appears to be common to many E. coli strains, with strong adherence being a prerequisite for an effective reduction of SiiE-mediated Salmonella adhesion.

View Article: PubMed Central - PubMed

Affiliation: Institut für Mikrobiologie und Tierseuchen, Freie Universität Berlin, Berlin, Germany. Peter.Schierack@HS-Lausitz.de

ABSTRACT

Background: The probiotic Escherichia coli strain Nissle 1917 (EcN) has been shown to interfere in a human in vitro model with the invasion of several bacterial pathogens into epithelial cells, but the underlying molecular mechanisms are not known.

Methodology/principal findings: In this study, we investigated the inhibitory effects of EcN on Salmonella Typhimurium invasion of porcine intestinal epithelial cells, focusing on EcN effects on the various stages of Salmonella infection including intracellular and extracellular Salmonella growth rates, virulence gene regulation, and adhesion. We show that EcN affects the initial Salmonella invasion steps by modulating Salmonella virulence gene regulation and Salmonella SiiE-mediated adhesion, but not extra- and intracellular Salmonella growth. However, the inhibitory activity of EcN against Salmonella invasion always correlated with EcN adhesion capacities. EcN mutants defective in the expression of F1C fimbriae and flagellae were less adherent and less inhibitory toward Salmonella invasion. Another E. coli strain expressing F1C fimbriae was also adherent to IPEC-J2 cells, and was similarly inhibitory against Salmonella invasion like EcN.

Conclusions: We propose that EcN affects Salmonella adhesion through secretory components. This mechanism appears to be common to many E. coli strains, with strong adherence being a prerequisite for an effective reduction of SiiE-mediated Salmonella adhesion.

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Invasion efficiency of Salmonella Typhimurium into IPEC-J2 cells after incubation with E. coli culture supernatants.Confluent monolayers of IPEC-J2 cells were pre-incubated (SN before) and/or co-incubated (SN simultaneously) with E. coli supernatants (SN). Cells were infected with Salmonella Typhimurium using an MOI of 100∶1 Salmonella to host cells. Invasion levels in percent (%) are expressed as invasion of Salmonella relative to invasion without pre- and/or co-incubation with E. coli SN. The data are the mean ± S.E.M. of at least three separate experiments in duplicate wells. * = p<0.05 compared to Salmonella infection without influence of E. coli SN. EcN: E. coli Nissle 1917.
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pone-0014712-g004: Invasion efficiency of Salmonella Typhimurium into IPEC-J2 cells after incubation with E. coli culture supernatants.Confluent monolayers of IPEC-J2 cells were pre-incubated (SN before) and/or co-incubated (SN simultaneously) with E. coli supernatants (SN). Cells were infected with Salmonella Typhimurium using an MOI of 100∶1 Salmonella to host cells. Invasion levels in percent (%) are expressed as invasion of Salmonella relative to invasion without pre- and/or co-incubation with E. coli SN. The data are the mean ± S.E.M. of at least three separate experiments in duplicate wells. * = p<0.05 compared to Salmonella infection without influence of E. coli SN. EcN: E. coli Nissle 1917.

Mentions: We also tested the effects of cell-free EcN supernatants compared to supernatants of the two control strains. To create a scenario relevant to the initial experiments with bacteria (for which EcN was present in the pre- and co-incubation period), we included pre- and pre-/co-incubation experiments using E. coli culture supernatants. As shown in Figure 4, pre-incubation with E. coli supernatants (E. coli 140815) showed little or no effects on Salmonella invasion efficiency, while pre-/co-incubation noticeably inhibited Salmonella invasion. We tested the hypothesis that co-incubation of E. coli supernatants with Salmonella was predominantly responsible for the inhibitory effect in subsequent co-incubation experiments. However, co-incubation of supernatants of all three tested E. coli strains similarly inhibited Salmonella invasion (Figure 4) as was the case with E. coli pre-incubations. Also supernatants of EcN mutants ΔfocA (F1C fimbriae), ΔfimA (type 1 fimbriae) and ΔfliA inhibited Salmonella invasion comparable to EcN wildtype (Figure 4).


E. coli Nissle 1917 Affects Salmonella adhesion to porcine intestinal epithelial cells.

Schierack P, Kleta S, Tedin K, Babila JT, Oswald S, Oelschlaeger TA, Hiemann R, Paetzold S, Wieler LH - PLoS ONE (2011)

Invasion efficiency of Salmonella Typhimurium into IPEC-J2 cells after incubation with E. coli culture supernatants.Confluent monolayers of IPEC-J2 cells were pre-incubated (SN before) and/or co-incubated (SN simultaneously) with E. coli supernatants (SN). Cells were infected with Salmonella Typhimurium using an MOI of 100∶1 Salmonella to host cells. Invasion levels in percent (%) are expressed as invasion of Salmonella relative to invasion without pre- and/or co-incubation with E. coli SN. The data are the mean ± S.E.M. of at least three separate experiments in duplicate wells. * = p<0.05 compared to Salmonella infection without influence of E. coli SN. EcN: E. coli Nissle 1917.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3040738&req=5

pone-0014712-g004: Invasion efficiency of Salmonella Typhimurium into IPEC-J2 cells after incubation with E. coli culture supernatants.Confluent monolayers of IPEC-J2 cells were pre-incubated (SN before) and/or co-incubated (SN simultaneously) with E. coli supernatants (SN). Cells were infected with Salmonella Typhimurium using an MOI of 100∶1 Salmonella to host cells. Invasion levels in percent (%) are expressed as invasion of Salmonella relative to invasion without pre- and/or co-incubation with E. coli SN. The data are the mean ± S.E.M. of at least three separate experiments in duplicate wells. * = p<0.05 compared to Salmonella infection without influence of E. coli SN. EcN: E. coli Nissle 1917.
Mentions: We also tested the effects of cell-free EcN supernatants compared to supernatants of the two control strains. To create a scenario relevant to the initial experiments with bacteria (for which EcN was present in the pre- and co-incubation period), we included pre- and pre-/co-incubation experiments using E. coli culture supernatants. As shown in Figure 4, pre-incubation with E. coli supernatants (E. coli 140815) showed little or no effects on Salmonella invasion efficiency, while pre-/co-incubation noticeably inhibited Salmonella invasion. We tested the hypothesis that co-incubation of E. coli supernatants with Salmonella was predominantly responsible for the inhibitory effect in subsequent co-incubation experiments. However, co-incubation of supernatants of all three tested E. coli strains similarly inhibited Salmonella invasion (Figure 4) as was the case with E. coli pre-incubations. Also supernatants of EcN mutants ΔfocA (F1C fimbriae), ΔfimA (type 1 fimbriae) and ΔfliA inhibited Salmonella invasion comparable to EcN wildtype (Figure 4).

Bottom Line: Another E. coli strain expressing F1C fimbriae was also adherent to IPEC-J2 cells, and was similarly inhibitory against Salmonella invasion like EcN.We propose that EcN affects Salmonella adhesion through secretory components.This mechanism appears to be common to many E. coli strains, with strong adherence being a prerequisite for an effective reduction of SiiE-mediated Salmonella adhesion.

View Article: PubMed Central - PubMed

Affiliation: Institut für Mikrobiologie und Tierseuchen, Freie Universität Berlin, Berlin, Germany. Peter.Schierack@HS-Lausitz.de

ABSTRACT

Background: The probiotic Escherichia coli strain Nissle 1917 (EcN) has been shown to interfere in a human in vitro model with the invasion of several bacterial pathogens into epithelial cells, but the underlying molecular mechanisms are not known.

Methodology/principal findings: In this study, we investigated the inhibitory effects of EcN on Salmonella Typhimurium invasion of porcine intestinal epithelial cells, focusing on EcN effects on the various stages of Salmonella infection including intracellular and extracellular Salmonella growth rates, virulence gene regulation, and adhesion. We show that EcN affects the initial Salmonella invasion steps by modulating Salmonella virulence gene regulation and Salmonella SiiE-mediated adhesion, but not extra- and intracellular Salmonella growth. However, the inhibitory activity of EcN against Salmonella invasion always correlated with EcN adhesion capacities. EcN mutants defective in the expression of F1C fimbriae and flagellae were less adherent and less inhibitory toward Salmonella invasion. Another E. coli strain expressing F1C fimbriae was also adherent to IPEC-J2 cells, and was similarly inhibitory against Salmonella invasion like EcN.

Conclusions: We propose that EcN affects Salmonella adhesion through secretory components. This mechanism appears to be common to many E. coli strains, with strong adherence being a prerequisite for an effective reduction of SiiE-mediated Salmonella adhesion.

Show MeSH
Related in: MedlinePlus