Rifampicin-induced ER stress and excessive cytoplasmic vacuolization instigate hepatotoxicity via alternate programmed cell death paraptosis in vitro and in vivo

Life Sci. 2023 Nov 15:333:122164. doi: 10.1016/j.lfs.2023.122164. Epub 2023 Oct 10.

Abstract

Aims: Rifampicin-induced hepatotoxicity is a primary cause of drug-induced liver injury (DILI), posing a significant challenge to its continued clinical application. Moreover, the mechanism underlying rifampicin-induced hepatotoxicity remains unclear.

Main methods: Human hepatocyte line-17 (HHL-17) cells were treated with an increasing dose of rifampicin for 24 h, and male Wistar rats were given rifampicin [150 mg/kg body weight (bw)] orally for 28 days. Viability assay, protein expression, and cell death assays were analyzed in vitro. Moreover, liver serum markers, body/organ weight, H&E staining, protein expression, etc., were assayed in vivo.

Key findings: Rifampicin induced a dose-dependent hepatotoxicity in HHL-17 cells (IC50; 600 μM), and increased the serum levels of liver injury markers, e.g., alanine transaminase (ALT) and aspartate transaminase (AST) in rats. Rifampicin-induced cell death was non-apoptotic and non-necroptotic both in vitro and in vivo. Further, excessive cellular vacuolization and reduced expression of Alix protein confirmed the induction of paraptosis both in vitro and in vivo. In addition, a significant increase in the endoplasmic reticulum (ER) stress markers (e.g., BiP, CHOP, and total polyubiquitinated proteins) was detected, demonstrating the induction of ER stress and altered protein homeostasis. Interestingly, rifampicin-induced hepatotoxicity was associated with the inhibition of autophagy and enhanced reactive oxygen species (ROS) generation in HHL-17 cells. Furthermore, inhibition of protein synthesis by cycloheximide (CHX) suppressed paraptosis by alleviating rifampicin-induced ER stress and ROS generation.

Significance: Rifampicin-induced hepatotoxicity involves ER stress-driven paraptosis as a novel mechanism of its toxicity that may be targeted to protect liver cells from rifampicin toxicity.

Keywords: Cycloheximide; Drug-induced liver injury; Endoplasmic reticulum stress; Hepatotoxicity; Paraptosis; Rifampicin.

MeSH terms

  • Animals
  • Apoptosis
  • Chemical and Drug Induced Liver Injury* / etiology
  • Endoplasmic Reticulum Stress
  • Humans
  • Male
  • Rats
  • Rats, Wistar
  • Reactive Oxygen Species / metabolism
  • Rifampin* / toxicity

Substances

  • Rifampin
  • Reactive Oxygen Species