Bardoxolone methyl prevents metabolic dysfunction-associated steatohepatitis by inhibiting macrophage infiltration

Br J Pharmacol. 2024 Aug;181(15):2545-2565. doi: 10.1111/bph.16374. Epub 2024 Apr 10.

Abstract

Background and purpose: Bardoxolone methyl (2-cyano-3,12-dioxooleana-1,9(11)-dien-28-oic acid methyl ester, CDDO-Me) is a potent activator of nuclear factor erythroid 2-related factor 2 (Nrf2), which induces the expression of antioxidative-associated genes. CDDO-Me exerts protective effects against chronic inflammatory diseases in the kidneys and lungs. However, its pharmacological effects on metabolic dysfunction-associated steatohepatitis (MASH) caused by fat accumulation remain unknown. In this study, we examined the hepatoprotective effects of CDDO-Me in a diet-induced MASH mouse model and elucidated its pharmacological mechanisms using RNA-seq analysis.

Experimental approach: CDDO-Me was orally administered to mice fed a choline-deficient, L-amino acid-defined, high-fat diet (CDAHFD), and histological, biochemical, and transcriptomic analyses were performed on livers of mice that developed MASH.

Key results: CDDO-Me administration induced the expression of antioxidant genes and cholesterol transporters downstream of Nrf2 and significantly prevented the symptoms of MASH. Whole-transcriptome analysis revealed that CDDO-Me inhibited the inflammatory pathway that led to phagocyte recruitment, in addition to activating the Nrf2-dependent pathway. Among inflammatory pathways, CC chemokine ligands (CCL)3 and CCL4, which are downstream of NF-κB and are associated with the recruitment of macrophages expressing CC chemokine receptors (CCR)1 and CCR5, were released into the blood in MASH mice. However, CDDO-Me directly inhibited the expression of CCL3-CCR1 and CCL4-CCR5 in macrophages.

Conclusions and implications: Overall, we revealed the potent hepatoprotective effect of CDDO-Me in a MASH mouse model and demonstrated that its pharmacological effects were closely associated with a reduction of macrophage infiltration, through CCL3-CCR1 and CCL4-CCR5 inhibition, in addition to Nrf2-mediated hepatoprotective effects.

Keywords: CCL3; CCL4; CDDO‐Me; MASH; RNA‐seq; macrophage.

MeSH terms

  • Animals
  • Diet, High-Fat* / adverse effects
  • Fatty Liver / drug therapy
  • Fatty Liver / metabolism
  • Fatty Liver / prevention & control
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Macrophages* / drug effects
  • Macrophages* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • NF-E2-Related Factor 2 / metabolism
  • Oleanolic Acid* / analogs & derivatives
  • Oleanolic Acid* / pharmacology
  • Oleanolic Acid* / therapeutic use
  • Receptors, CCR1 / antagonists & inhibitors
  • Receptors, CCR1 / metabolism
  • Receptors, CCR5

Substances

  • Oleanolic Acid
  • bardoxolone methyl
  • NF-E2-Related Factor 2
  • Receptors, CCR1
  • Ccr1 protein, mouse
  • CCR5 protein, mouse
  • Receptors, CCR5