The mRNA-binding protein IGF2BP1 maintains intestinal barrier function by up-regulating occludin expression

J Biol Chem. 2020 Jun 19;295(25):8602-8612. doi: 10.1074/jbc.AC120.013646. Epub 2020 May 8.

Abstract

Insulin-like growth factor 2 mRNA-binding protein 1 (IGF2BP1) is an mRNA-binding protein that has an oncofetal pattern of expression. It is also expressed in intestinal tissue, suggesting that it has a possible role in intestinal homeostasis. To investigate this possibility, here we generated Villin CreERT2:Igf2bp1flox/flox mice, which enabled induction of an IGF2BP1 knockout specifically in intestinal epithelial cells (IECs) of adult mice. Using gut barrier and epithelial permeability assays and several biochemical approaches, we found that IGF2BP1 ablation in the adult intestinal epithelium causes mild active colitis and mild-to-moderate active enteritis. Moreover, the IGF2BP1 deletion aggravated dextran sodium sulfate-induced colitis. We also found that IGF2BP1 removal compromises barrier function of the intestinal epithelium, resulting from altered protein expression at tight junctions. Mechanistically, IGF2BP1 interacted with the mRNA of the tight-junction protein occludin (Ocln), stabilizing Ocln mRNA and inducing expression of occludin in IECs. Furthermore, ectopic occludin expression in IGF2BP1-knockdown cells restored barrier function. We conclude that IGF2BP1-dependent regulation of occludin expression is an important mechanism in intestinal barrier function maintenance and in the prevention of colitis.

Keywords: RNA-binding protein; RNA-binding proteins; colitis; epithelial barrier; inflammatory bowel disease (IBD); insulin-like growth factor 2 mRNA-binding protein 1 (IGF2BP1); intestinal epithelium; intestinal mucosa; mRNA decay; occludin; permeability.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Line
  • Colitis / chemically induced
  • Colitis / mortality
  • Colitis / pathology
  • Colon / pathology
  • Humans
  • Intestinal Mucosa / cytology
  • Intestinal Mucosa / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Occludin / genetics
  • Occludin / metabolism*
  • Permeability*
  • Protein Binding
  • RNA Interference
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / metabolism
  • RNA-Binding Proteins / antagonists & inhibitors
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Severity of Illness Index
  • Survival Rate
  • Tight Junction Proteins / metabolism
  • Up-Regulation

Substances

  • CRD-BP protein, mouse
  • Occludin
  • RNA, Messenger
  • RNA, Small Interfering
  • RNA-Binding Proteins
  • Tight Junction Proteins