Astragalus polysaccharide protects experimental colitis through an aryl hydrocarbon receptor-dependent autophagy mechanism

Br J Pharmacol. 2024 Mar;181(5):681-697. doi: 10.1111/bph.16229. Epub 2023 Oct 12.

Abstract

Background and purpose: Disruption of intestinal barriers plays a vital role in the pathogenesis of colitis. The aryl hydrocarbon receptor (AhR) is a recognition sensor that mediates intestinal immune homeostasis and minimizes intestinal inflammation. Astragalus polysaccharide (APS) exerts pharmacological actions in colitis; however, the mechanism has not been elucidated. We investigated whether APS protects through AhR-dependent autophagy.

Experimental approach: The symptoms of dextran sulfate sodium (DSS)-induced colitis in mice involving intestinal barrier function and inflammatory injury were evaluated after APS administration. Intestinal-specific Becn1 conditional knockout (Becn1 cKO) mice were constructed and compared with wild-type mice. Autophagy and the effects of APS were investigated after the deactivation of AhRs. The relationship between APS-induced AhRs and autophagic Becn1 was investigated using a dual-luciferase reporter system and chromatin immunoprecipitation (ChIP)-quantitative polymerase chain reaction assay. Caco-2 cells were used to investigate inflammatory responses and AhR-dependent autophagy.

Key results: APS improved intestinal barrier function in inflammatory injury in colitis mice. APS triggered autophagic flow; however, knockout of Becn1 in the gut increased susceptibility to colitis, leading to diminished epithelial barrier function and severe intestinal inflammation, impairing the protective effects of APS. Mechanistically, APS-triggered autophagy depends on AhR expression. Activated AhR binds to the promoter Becn1 to operate transcription of genes involved in anti-inflammation and intestinal barrier repair, while deactivation of AhR correlated with intestinal inflammation and the therapeutic function of APS.

Conclusions and implications: APS protects colitis mice by targeting autophagy, especially as the AhR stimulates the repair of damaged intestinal barrier functions.

Keywords: Astragalus polysaccharide; aryl hydrocarbon receptor; autophagy; experimental colitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy
  • Caco-2 Cells
  • Colitis* / chemically induced
  • Colitis* / drug therapy
  • Colitis* / prevention & control
  • Dextran Sulfate
  • Disease Models, Animal
  • Humans
  • Inflammation
  • Mice
  • Mice, Inbred C57BL
  • Polysaccharides / pharmacology
  • Polysaccharides / therapeutic use
  • Receptors, Aryl Hydrocarbon* / genetics

Substances

  • Dextran Sulfate
  • Polysaccharides
  • Receptors, Aryl Hydrocarbon