Ablation of Intestinal Epithelial Sialylation Predisposes to Acute and Chronic Intestinal Inflammation in Mice

Cell Mol Gastroenterol Hepatol. 2024;18(5):101378. doi: 10.1016/j.jcmgh.2024.101378. Epub 2024 Jul 9.

Abstract

Background & aims: Addition of sialic acids (sialylation) to glycoconjugates is a common capping step of glycosylation. Our study aims to determine the roles of the overall sialylation in intestinal mucosal homeostasis.

Methods: Mice with constitutive deletion of intestinal epithelial sialylation (IEC Slc35a1-/- mice) and mice with inducible deletion of sialylation in intestinal epithelium (TM-IEC Slc35a1-/- mice) were generated, which were used to determine the roles of overall sialylation in intestinal mucosal homeostasis by ex vivo and mutiomics studies.

Results: IEC Slc35a1-/- mice developed mild spontaneous microbiota-dependent colitis. Additionally, 30% of IEC Slc35a1-/- mice had spontaneous tumors in the rectum greater than the age of 12 months. TM-IEC Slc35a1-/- mice were highly susceptible to acute inflammation induced by 1% dextran sulfate sodium versus control animals. Loss of total sialylation was associated with reduced mucus thickness on fecal sections and within colon tissues. TM-IEC Slc35a1-/- mice showed altered microbiota with an increase in Clostridium disporicum, which is associated a global reduction in the abundance of at least 10 unique taxa; however, metabolomic analysis did not show any significant differences in short-chain fatty acid levels. Treatment with 5-fluorouracil led to more severe small intestine mucositis in the IEC Slc35a1-/- mice versus wild-type littermates, which was associated with reduced Lgr5+ cell representation in small intestinal crypts in IEC Slc35a1-/-;Lgr5-GFP mice.

Conclusions: Loss of overall sialylation impairs mucus stability and the stem cell niche leading to microbiota-dependent spontaneous colitis and tumorigenesis.

Keywords: Colon; Inflammation; Microbiota; Mucin; Mucin-Type O-Glycans; Sialylation; Slc35a1.

MeSH terms

  • Acute Disease
  • Animals
  • Chronic Disease
  • Colitis* / chemically induced
  • Colitis* / metabolism
  • Colitis* / microbiology
  • Colitis* / pathology
  • Dextran Sulfate / toxicity
  • Disease Models, Animal
  • Gastrointestinal Microbiome*
  • Intestinal Mucosa* / immunology
  • Intestinal Mucosa* / metabolism
  • Intestinal Mucosa* / microbiology
  • Intestinal Mucosa* / pathology
  • Male
  • Mice
  • Mice, Knockout
  • N-Acetylneuraminic Acid / metabolism
  • Sialic Acids / metabolism

Substances

  • Dextran Sulfate
  • N-Acetylneuraminic Acid
  • Sialic Acids