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

Rosemarie De Weirdt UGent, Aurélie Crabbé, Stefan Roos, Sabine Vollenweider, Christophe Lacroix, Jan Peter van Pijkeren, Robert A Britton, Sshameema Sarker, Tom Van de Wiele UGent and Cheryl A Nickerson (2012) PLOS ONE. 7(5).
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.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
HOST-PATHOGEN INTERACTIONS, ENTERICA SEROVAR TYPHIMURIUM, FOOD-BORNE PATHOGENS, 2 PROBIOTIC AGENTS, LACTOBACILLUS-REUTERI, SALMONELLA-TYPHIMURIUM, ESCHERICHIA-COLI, GENE-EXPRESSION, MUCUS LAYERS, ISLAND 1
journal title
PLOS ONE
PLoS One
volume
7
issue
5
article_number
e37116
pages
11 pages
Web of Science type
Article
Web of Science id
000305338500031
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
3.73 (2012)
JCR rank
7/56 (2012)
JCR quartile
1 (2012)
ISSN
1932-6203
DOI
10.1371/journal.pone.0037116
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
3047501
handle
http://hdl.handle.net/1854/LU-3047501
date created
2012-11-05 15:54:53
date last changed
2012-11-05 16:54:47
@article{3047501,
  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.},
  articleno    = {e37116},
  author       = {De Weirdt, Rosemarie and Crabb{\'e}, Aur{\'e}lie and Roos, Stefan and Vollenweider, Sabine and Lacroix, Christophe and van Pijkeren, Jan Peter and Britton, Robert A and Sarker, Sshameema and Van de Wiele, Tom and Nickerson, Cheryl A},
  issn         = {1932-6203},
  journal      = {PLOS ONE},
  keyword      = {HOST-PATHOGEN INTERACTIONS,ENTERICA SEROVAR TYPHIMURIUM,FOOD-BORNE PATHOGENS,2 PROBIOTIC AGENTS,LACTOBACILLUS-REUTERI,SALMONELLA-TYPHIMURIUM,ESCHERICHIA-COLI,GENE-EXPRESSION,MUCUS LAYERS,ISLAND 1},
  language     = {eng},
  number       = {5},
  pages        = {11},
  title        = {Glycerol supplementation enhances L. reuteri's protective effect against S. Typhimurium colonization in a 3-D model of colonic epithelium},
  url          = {http://dx.doi.org/10.1371/journal.pone.0037116},
  volume       = {7},
  year         = {2012},
}

Chicago
De Weirdt, Rosemarie, Aurélie Crabbé, Stefan Roos, Sabine Vollenweider, Christophe Lacroix, Jan Peter van Pijkeren, Robert A Britton, Sshameema Sarker, Tom Van de Wiele, and Cheryl A Nickerson. 2012. “Glycerol Supplementation Enhances L. Reuteri’s Protective Effect Against S. Typhimurium Colonization in a 3-D Model of Colonic Epithelium.” Plos One 7 (5).
APA
De Weirdt, R., Crabbé, A., Roos, S., Vollenweider, S., Lacroix, C., van Pijkeren, J. P., Britton, R. A., et al. (2012). Glycerol supplementation enhances L. reuteri’s protective effect against S. Typhimurium colonization in a 3-D model of colonic epithelium. PLOS ONE, 7(5).
Vancouver
1.
De Weirdt R, Crabbé A, Roos S, Vollenweider S, Lacroix C, van Pijkeren JP, et al. Glycerol supplementation enhances L. reuteri’s protective effect against S. Typhimurium colonization in a 3-D model of colonic epithelium. PLOS ONE. 2012;7(5).
MLA
De Weirdt, Rosemarie, Aurélie Crabbé, Stefan Roos, et al. “Glycerol Supplementation Enhances L. Reuteri’s Protective Effect Against S. Typhimurium Colonization in a 3-D Model of Colonic Epithelium.” PLOS ONE 7.5 (2012): n. pag. Print.