Dietary Emulsifiers Directly Impact Adherent-Invasive E. coli Gene Expression to Drive Chronic Intestinal Inflammation

Emilie Viennois; Alexis Bretin; Philip E Dubé; Alexander C Maue; Charlène J G Dauriat; Nicolas Barnich; Andrew T Gewirtz; Benoit Chassaing

doi:10.1016/j.celrep.2020.108229

Dietary Emulsifiers Directly Impact Adherent-Invasive E. coli Gene Expression to Drive Chronic Intestinal Inflammation

Cell Rep. 2020 Oct 6;33(1):108229. doi: 10.1016/j.celrep.2020.108229.

Authors

Emilie Viennois¹, Alexis Bretin², Philip E Dubé³, Alexander C Maue³, Charlène J G Dauriat⁴, Nicolas Barnich⁵, Andrew T Gewirtz², Benoit Chassaing⁶

Affiliations

¹ INSERM, U1149, Center of Research on Inflammation, Université de Paris, Paris, France; Institute for Biomedical Sciences, Center for Inflammation, Immunity and Infection, Digestive Disease Research Group, Georgia State University, Atlanta, GA, USA.
² Institute for Biomedical Sciences, Center for Inflammation, Immunity and Infection, Digestive Disease Research Group, Georgia State University, Atlanta, GA, USA.
³ Taconic Biosciences Inc, Rensselaer, NY, USA.
⁴ INSERM U1016, team "Mucosal microbiota in chronic inflammatory diseases", CNRS UMR 8104, Université de Paris, Paris, France.
⁵ Université Clermont Auvergne/Inserm U1071 USC-INRA 2018, Microbes, Intestin, Inflammation et Susceptibilité de l'Hôte (M2iSH), Clermont-Ferrand, France.
⁶ Institute for Biomedical Sciences, Center for Inflammation, Immunity and Infection, Digestive Disease Research Group, Georgia State University, Atlanta, GA, USA; INSERM U1016, team "Mucosal microbiota in chronic inflammatory diseases", CNRS UMR 8104, Université de Paris, Paris, France; Neuroscience Institute, Georgia State University, Atlanta, GA, USA. Electronic address: benoit.chassaing@inserm.fr.

Abstract

Dietary emulsifiers carboxymethylcellulose (CMC) and polysorbate-80 (P80) disturb gut microbiota, promoting chronic inflammation. Mice with minimal microbiota are protected against emulsifiers' effects, leading us to hypothesize that these compounds might provoke select pathobionts to promote inflammation. Gnotobiotic wild-type (WT) and interleukin-10 (IL-10)^-/- mice were colonized with Crohn's-disease-associated adherent-invasive E. coli (AIEC) and subsequently administered CMC or P80. AIEC colonization of GF and altered Schaedler flora (ASF) mice results in chronic intestinal inflammation and metabolism dysregulations when consuming the emulsifier. In IL-10^-/- mice, AIEC mono-colonization results in severe intestinal inflammation in response to emulsifiers. Exposure of AIEC to emulsifiers in vitro increases its motility and ability to adhere to intestinal epithelial cells. Transcriptomic analysis reveals that emulsifiers directly induce expression of clusters of genes that mediate AIEC virulence and promotion of inflammation. To conclude, emulsifiers promote virulence and encroachment of pathobionts, providing a means by which these compounds may drive inflammation in hosts carrying such bacteria.

Keywords: adherent-invasive Escherichia coli; diet; emulsifier; flagellin; intestinal inflammation; microbiota; pathobiont.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Chronic Disease
Diet
Emulsifying Agents / pharmacology
Emulsifying Agents / therapeutic use*
Escherichia coli / growth & development
Escherichia coli / pathogenicity*
Flagellin / metabolism*
Gene Expression / genetics*
Humans
Inflammation / metabolism
Intestines / microbiology*
Mice

Substances

Emulsifying Agents
Flagellin

Abstract

Publication types

MeSH terms

Substances

Grants and funding