PXR Activation Relieves Deoxynivalenol-Induced Liver Oxidative Stress Via Malat1 LncRNA m6A Demethylation

Adv Sci (Weinh). 2024 Jul;11(25):e2308742. doi: 10.1002/advs.202308742. Epub 2024 Apr 24.

Abstract

Deoxynivalenol (DON) is a prevalent toxin causing severe liver damage through hepatocellular oxidative stress. However, the underlying mechanisms and effective therapeutic approaches remain unknown. Here, the unique role of the xenobiotic metabolism factor pregnane X receptor (PXR) in mediating DON-induced hepatocellular oxidative stress is investigated. Treatment with the PXR agonist 3-indole-propionic acid (IPA) alleviates DON-induced oxidative stress and liver injury both in vitro and in vivo. Mechanistically, it is discovered for the first time that PXR agonist IPA directly transactivates the m6A demethylase FTO expression, leading to site-specific demethylation and decreased abundance of YTHDC1-bound Malat1 lncRNA at single-nucleotide resolution. The diminished m6A modification of Malat1 lncRNA reduces its stability and augments antioxidant pathways governed by NRF2, consequently mitigating DON-induced liver injury. Furthermore, Malat1 knockout mice exhibit decreased DON-induced liver injury, emphasizing the role of Malat1 lncRNA in oxidative stress. Collectively, the findings establish that PXR-mediated m6A-dependent Malat1 lncRNA expression determines hepatocyte oxidative stress via m6A demethylase FTO, providing valuable insights into the potential mechanisms underlying DON-induced liver injury and offers potential therapeutic strategies for its treatment.

Keywords: Malat1 lncRNA; N6‐methyladenosine; deoxynivalenol; indole‐3‐propionic acid; pregnane X receptor.

MeSH terms

  • Animals
  • Demethylation*
  • Disease Models, Animal
  • Humans
  • Liver / drug effects
  • Liver / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Oxidative Stress* / drug effects
  • Oxidative Stress* / genetics
  • Pregnane X Receptor* / genetics
  • Pregnane X Receptor* / metabolism
  • RNA, Long Noncoding* / genetics
  • RNA, Long Noncoding* / metabolism
  • Trichothecenes* / toxicity

Substances

  • RNA, Long Noncoding
  • Trichothecenes
  • Pregnane X Receptor
  • deoxynivalenol
  • Malat1 long non-coding RNA, mouse
  • MALAT1 long non-coding RNA, human