Downregulated KLF4, induced by m6A modification, aggravates intestinal barrier dysfunction in inflammatory bowel disease

Cell Mol Life Sci. 2024 Nov 29;81(1):470. doi: 10.1007/s00018-024-05514-7.

Abstract

Background: Krüppel-like factor 4 (KLF4), a transcription factor, is involved in various biological processes. However, the role of KLF4 in regulating the intestinal epithelial barrier (IEB) in inflammatory bowel disease (IBD) and its mechanism have not been extensively studied.

Methods: KLF4 expression in IBD patients and colitis mice was analyzed using Gene Expression Omnibus(GEO) database, immunohistochemistry (IHC) and Western blot. The roles of KLF4 in IEB and colitis symptoms were verified in dextran sulfate sodium (DSS)-induced and 2,4,6-trinitrobenzenesulfonic acid (TNBS)-induced colitis model mice using an adenovirus carrying KLF4 shRNA (shKLF4-Adv). Furthermore, the influence of KLF4 on trans-epithelium electrical resistance (TEER), paracellular permeability, apical junction complex (AJC) protein expression and apoptosis was assessed in vitro and in vivo. MeRIP and RIP assays were used to verify the effects of m6A modification on KLF4 expression.

Results: KLF4 expression was significantly decreased in IBD patients and was negatively associated with inflammatory features. KLF4 deletion aggravated colitis symptoms and IEB injuries by reducing AJC protein expression and increasing apoptosis in mice with colitis. Furthermore, KLF4 transcriptionally regulated the expression of AJC proteins and inhibited apoptosis by reducing cellular ROS levels and proinflammatory cytokine expression. Moreover, we observed that METTL3/ALKBH5/YTHDF2-mediated m6A modification led to a decrease in KLF4 expression in Caco-2 cells. In addition, APTO-253, an inducer of KLF4, exhibited a synergistic effect with mesalazine on IEB function.

Conclusions: Our study demonstrated that KLF4 is a crucial regulator of IEB, suggesting that targeting KLF4 may be a promising therapeutic alternative for IBD.

Keywords: Apical junction complex; Apoptosis; Inflammatory bowel disease; Intestinal epithelial barrier; KLF4; m6A Modification.

MeSH terms

  • Animals
  • Apoptosis
  • Caco-2 Cells
  • Colitis* / chemically induced
  • Colitis* / genetics
  • Colitis* / metabolism
  • Colitis* / pathology
  • Dextran Sulfate
  • Disease Models, Animal
  • Down-Regulation / drug effects
  • Female
  • Humans
  • Inflammatory Bowel Diseases* / chemically induced
  • Inflammatory Bowel Diseases* / genetics
  • Inflammatory Bowel Diseases* / metabolism
  • Inflammatory Bowel Diseases* / pathology
  • Intestinal Mucosa* / metabolism
  • Intestinal Mucosa* / pathology
  • Kruppel-Like Factor 4* / metabolism
  • Kruppel-Like Transcription Factors* / genetics
  • Kruppel-Like Transcription Factors* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*

Substances

  • Kruppel-Like Factor 4
  • KLF4 protein, human
  • Klf4 protein, mouse
  • Kruppel-Like Transcription Factors
  • Dextran Sulfate