Butyrate reduces epithelial barrier dysfunction induced by the foodborne mycotoxin deoxynivalenol in cell monolayers derived from pig jejunum organoids

Gut Microbes. 2024 Jan-Dec;16(1):2430424. doi: 10.1080/19490976.2024.2430424. Epub 2024 Nov 21.

Abstract

The foodborne mycotoxin deoxynivalenol (DON) produced by Fusarium species threats animal and human health through disruption of the intestinal barrier. Targeting the gut microbiota and its products appears as a promising strategy to mitigate DON intestinal toxicity. In this study, we investigated whether the bacterial metabolite butyrate could alleviate epithelial barrier disruption induced by DON. We used a model of cell monolayers derived from porcine jejunum organoids allowing to reproduce the cellular complexity of the intestinal epithelium. Our results show that DON dose-dependently disrupted the epithelial barrier integrity, reduced epithelial differentiation, and altered innate immune defenses. Butyrate attenuated the DON-induced increase in paracellular permeability. Butyrate also prevented epithelial barrier dysfunction triggered by anisomycin, a ribosome inhibitor like DON. Moreover, butyrate partially counteracted the effects of DON on tight junctions (TJP1, OCLN), innate epithelial defenses (PTGS2, CD14, TLR4, TLR5), and absorptive cell functions (CA2, VIL1, NHE3, CFTR). In contrast, butyrate did not prevent the toxic effects of DON on mitochondrial metabolism, proliferation and goblet cell functions. Taken together, our results demonstrate that the bacterial metabolite butyrate is able to reduce DON-induced epithelial barrier disruption.

Keywords: Gut microbiota; enteroids; epithelium; metabolites; permeability; toxin.

MeSH terms

  • Animals
  • Butyrates* / metabolism
  • Butyrates* / pharmacology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Fusarium / drug effects
  • Gastrointestinal Microbiome / drug effects
  • Goblet Cells / drug effects
  • Goblet Cells / metabolism
  • Immunity, Innate / drug effects
  • Intestinal Mucosa* / drug effects
  • Intestinal Mucosa* / metabolism
  • Intestinal Mucosa* / microbiology
  • Jejunum* / drug effects
  • Jejunum* / metabolism
  • Jejunum* / microbiology
  • Jejunum* / pathology
  • Mycotoxins / metabolism
  • Mycotoxins / toxicity
  • Organoids* / drug effects
  • Organoids* / metabolism
  • Swine
  • Tight Junctions / drug effects
  • Tight Junctions / metabolism
  • Trichothecenes* / toxicity

Substances

  • Trichothecenes
  • deoxynivalenol
  • Butyrates
  • Mycotoxins

Grants and funding

This work was supported by the Institut Carnot France Futur Elevage [“OrganoPig” grant] and by the Occitanie Region and Lallemand [“Tool4GutHealth” CLE2014 grant].