Oleanolic acid alleviates ANIT-induced cholestatic liver injury by activating Fxr and Nrf2 pathways to ameliorate disordered bile acids homeostasis

Phytomedicine. 2022 Jul 20:102:154173. doi: 10.1016/j.phymed.2022.154173. Epub 2022 May 14.

Abstract

Background: Cholestasis is a clinical syndrome with high incidence and few effective treatments. Oleanolic acid (OA) is a triterpenoid compound with anti-cholestatic effects. Studies using bile duct ligation or lithocholic acid modeling have shown that the alleviating effect of OA on cholerosis is related to the regulation of nuclear factor erythroid 2 related factor (Nrf2) or farnesoid X receptor (Fxr).

Purpose: This study aims to investigate the underlying mechanism of OA against alpha-naphthylisothiocyanate (ANIT)-induced cholestatic liver injury based on Nrf2 and Fxr dual signaling pathways.

Methods: The ANIT-induced rats model was used with or without OA treatment. Serum biochemical indexes, liver histopathological changes and glutathione level were examined. Bile acids (BAs) targeted metabolomics based on UHPLC-MS/MS were performed. siRNA, RT-qPCR and western blot analysis were used to prove the role of Fxr and Nrf2 pathway in OA's anti-cholestatic liver injury in vivo and in vitro.

Results: OA significantly alleviated ANIT-induced liver injury in rats, reduced primary bile acids, accelerated metabolism of BAs and reduced the intrahepatic accumulation of BAs. The expressions of bile salt export pump (Bsep), Na+-taurocholic cotransport polypeptide (Ntcp), UDP-glucuronyl transferase 1a1 (Ugt1a1) and Fxr in rat liver were markedly up-regulated, the activation of Nrf2 was promoted, and the expression of cholesterol 7α-hydroxylase (Cyp7a1) was decreased after OA treatment. Moreover, Fxr or Nrf2 silencing attenuated the regulation of OA on BAs homeostasis related transporters and enzymes in rat primary hepatocytes.

Conclusion: OA may regulate BAs-related transporters and metabolic enzymes by activating Fxr and Nrf2 pathways, thus alleviating the cholestatic liver injury induced by ANIT.

Keywords: Farnesoid x receptor; Intrahepatic cholestasis; Nuclear factor erythroid 2-related factor 2; Oleanolic acid; Targeted metabolomics.

MeSH terms

  • 1-Naphthylisothiocyanate / toxicity
  • Animals
  • Bile Acids and Salts / metabolism
  • Chemical and Drug Induced Liver Injury* / drug therapy
  • Cholestasis* / chemically induced
  • Cholestasis* / drug therapy
  • Homeostasis
  • Liver
  • NF-E2-Related Factor 2 / metabolism
  • Oleanolic Acid* / pharmacology
  • Rats
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Tandem Mass Spectrometry

Substances

  • 1-Naphthylisothiocyanate
  • Bile Acids and Salts
  • NF-E2-Related Factor 2
  • Oleanolic Acid
  • Receptors, Cytoplasmic and Nuclear