Glycerol supplementation enhances L. reuteri's protective effect against S. Typhimurium colonization in a 3-D model of colonic epithelium

Rosemarie de Weirdt, Aurélie Crabbé, Stefan Roos, Sabine Vollenweider, Christophe Lacroix, Jan Peter van Pijkeren, Robert A. Britton, Shameema Sarker, Tom van de Wiele, Cheryl Nickerson

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

The probiotic effects of Lactobacillus reuteri have been speculated to partly depend on its capacity to produce the antimicrobial substance reuterin during the reduction of glycerol in the gut. In this study, the potential of this process to protect human intestinal epithelial cells against infection with Salmonella enterica serovar Typhimurium was investigated. We used a three-dimensional (3-D) organotypic model of human colonic epithelium that was previously validated and applied to study interactions between S. Typhimurium and the intestinal epithelium that lead to enteric salmonellosis. Using this model system, we show that L. reuteri protects the intestinal cells against the early stages of Salmonella infection and that this effect is significantly increased when L. reuteri is stimulated to produce reuterin from glycerol. More specifically, the reuterin-containing ferment of L. reuteri caused a reduction in Salmonella adherence and invasion (1 log unit), and intracellular survival (2 log units). In contrast, the L. reuteri ferment without reuterin stimulated growth of the intracellular Salmonella population with 1 log unit. The short-term exposure to reuterin or the reuterin-containing ferment had no observed negative impact on intestinal epithelial cell health. However, long-term exposure (24 h) induced a complete loss of cell-cell contact within the epithelial aggregates and compromised cell viability. Collectively, these results shed light on a potential role for reuterin in inhibiting Salmonella-induced intestinal infections and may support the combined application of glycerol and L. reuteri. While future in vitro and in vivo studies of reuterin on intestinal health should fine-tune our understanding of the mechanistic effects, in particular in the presence of a complex gut microbiota, this the first report of a reuterin effect on the enteric infection process in any mammalian cell type.

Original languageEnglish (US)
Article numbere37116
JournalPLoS One
Volume7
Issue number5
DOIs
StatePublished - May 31 2012

Fingerprint

Lactobacillus reuteri
Glycerol
protective effect
glycerol
epithelium
Epithelium
Salmonella
salmonellosis
epithelial cells
Salmonella Infections
infection
cells
chronic exposure
cell aggregates
intestinal mucosa
in vivo studies
Infection
Epithelial Cells
Cells
intestinal microorganisms

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Glycerol supplementation enhances L. reuteri's protective effect against S. Typhimurium colonization in a 3-D model of colonic epithelium. / de Weirdt, Rosemarie; Crabbé, Aurélie; Roos, Stefan; Vollenweider, Sabine; Lacroix, Christophe; van Pijkeren, Jan Peter; Britton, Robert A.; Sarker, Shameema; van de Wiele, Tom; Nickerson, Cheryl.

In: PLoS One, Vol. 7, No. 5, e37116, 31.05.2012.

Research output: Contribution to journalArticle

de Weirdt, R, Crabbé, A, Roos, S, Vollenweider, S, Lacroix, C, van Pijkeren, JP, Britton, RA, Sarker, S, van de Wiele, T & Nickerson, C 2012, 'Glycerol supplementation enhances L. reuteri's protective effect against S. Typhimurium colonization in a 3-D model of colonic epithelium', PLoS One, vol. 7, no. 5, e37116. https://doi.org/10.1371/journal.pone.0037116
de Weirdt, Rosemarie ; Crabbé, Aurélie ; Roos, Stefan ; Vollenweider, Sabine ; Lacroix, Christophe ; van Pijkeren, Jan Peter ; Britton, Robert A. ; Sarker, Shameema ; van de Wiele, Tom ; Nickerson, Cheryl. / Glycerol supplementation enhances L. reuteri's protective effect against S. Typhimurium colonization in a 3-D model of colonic epithelium. In: PLoS One. 2012 ; Vol. 7, No. 5.
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abstract = "The probiotic effects of Lactobacillus reuteri have been speculated to partly depend on its capacity to produce the antimicrobial substance reuterin during the reduction of glycerol in the gut. In this study, the potential of this process to protect human intestinal epithelial cells against infection with Salmonella enterica serovar Typhimurium was investigated. We used a three-dimensional (3-D) organotypic model of human colonic epithelium that was previously validated and applied to study interactions between S. Typhimurium and the intestinal epithelium that lead to enteric salmonellosis. Using this model system, we show that L. reuteri protects the intestinal cells against the early stages of Salmonella infection and that this effect is significantly increased when L. reuteri is stimulated to produce reuterin from glycerol. More specifically, the reuterin-containing ferment of L. reuteri caused a reduction in Salmonella adherence and invasion (1 log unit), and intracellular survival (2 log units). In contrast, the L. reuteri ferment without reuterin stimulated growth of the intracellular Salmonella population with 1 log unit. The short-term exposure to reuterin or the reuterin-containing ferment had no observed negative impact on intestinal epithelial cell health. However, long-term exposure (24 h) induced a complete loss of cell-cell contact within the epithelial aggregates and compromised cell viability. Collectively, these results shed light on a potential role for reuterin in inhibiting Salmonella-induced intestinal infections and may support the combined application of glycerol and L. reuteri. While future in vitro and in vivo studies of reuterin on intestinal health should fine-tune our understanding of the mechanistic effects, in particular in the presence of a complex gut microbiota, this the first report of a reuterin effect on the enteric infection process in any mammalian cell type.",
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