Local Stabilization of Hypoxia-Inducible Factor-1α Controls Intestinal Inflammation via Enhanced Gut Barrier Function and Immune Regulation

Front Immunol. 2021 Jan 14:11:609689. doi: 10.3389/fimmu.2020.609689. eCollection 2020.

Abstract

Intestinal epithelial cells are adapted in mucosal hypoxia and hypoxia-inducible factors in these cells can fortify barrier integrity to support mucosal tissue healing. Here we investigated whether hypoxia-related pathways could be proposed as potential therapeutic targets for inflammatory bowel disease. We developed a novel hypoxia-inducible factor (HIF) prolyl hydroxylase inhibitor, CG-598 which stabilized HIF-1α in the gut tissue. Treatment of CG-598 did not affect extra-intestinal organs or cause any significant adverse effects such as erythropoiesis. In the experimental murine colitis model, CG-598 ameliorated intestinal inflammation with reduction of inflammatory lesions and pro-inflammatory cytokines. CG-598 treatment fortified barrier function by increasing the expression of intestinal trefoil factor, CD73, E-cadherin and mucin. Also, IL-10 and IL-22 were induced from lamina propria CD4+ T-cells. The effectiveness of CG-598 was comparable to other immunosuppressive therapeutics such as TNF-blockers or JAK inhibitors. These results suggest that CG-598 could be a promising therapeutic candidate to treat inflammatory bowel disease.

Keywords: gut barrier; hypoxia-inducible factor; immune regulation; inflammatory bowel disease; prolyl hydroxylase inhibitor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caco-2 Cells
  • Cell Line, Tumor
  • Colitis / drug therapy
  • Colitis / immunology
  • Colitis / metabolism
  • Cytokines / immunology
  • Cytokines / metabolism
  • Disease Models, Animal
  • Female
  • HCT116 Cells
  • HeLa Cells
  • Humans
  • Hypoxia / drug therapy
  • Hypoxia / immunology
  • Hypoxia / metabolism
  • Hypoxia-Inducible Factor 1, alpha Subunit / immunology*
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Inflammation / immunology*
  • Inflammation / metabolism*
  • Inflammatory Bowel Diseases / drug therapy
  • Inflammatory Bowel Diseases / immunology
  • Inflammatory Bowel Diseases / metabolism
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred ICR
  • Prolyl-Hydroxylase Inhibitors / pharmacology
  • Trefoil Factor-3 / immunology
  • Trefoil Factor-3 / metabolism

Substances

  • Cytokines
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Prolyl-Hydroxylase Inhibitors
  • Trefoil Factor-3