Cannabidiol mitigates radiation-induced intestine ferroptosis via facilitating the heterodimerization of RUNX3 with CBFβ thereby promoting transactivation of GPX4

Free Radic Biol Med. 2024 Sep:222:288-303. doi: 10.1016/j.freeradbiomed.2024.05.047. Epub 2024 Jun 1.

Abstract

Radiation enteritis remains a major challenge for radiotherapy against abdominal and pelvic malignancies. Nevertheless, there is no approved effective therapy to alleviate irradiation (IR)-induced gastrointestinal (GI) toxicity. In the current study, Cannabidiol (CBD) was found to mitigate intestinal injury by GPX4-mediated ferroptosis resistance upon IR exposure. RNA-sequencing was employed to investigate the underlying mechanism involved in the radio-protective effect of CBD, wherein runt-related transcription factor 3 (RUNX3) and its target genes were changed significantly. Further experiment showed that the transactivation of GPX4 triggered by the direct binding of RUNX3 to its promoter region, or by stimulating the transcriptional activity of NF-κB via RUNX3-mediated LILRB3 upregulation was critical for the anti-ferroptotic effect of CBD upon IR injury. Specially, CBD was demonstrated to be a molecular glue skeleton facilitating the heterodimerization of RUNX3 with its transcriptional chaperone core-biding factor β (CBFβ) thereby promoting their nuclear localization and the subsequent transactivation of GPX4 and LILRB3. In short, our study provides an alternative strategy to counteract IR-induced enteritis during the radiotherapy on abdominal/pelvic neoplasms.

Keywords: Cannabidiol; Ferroptosis; GPX4 transactivation; Heterodimerization with CBFβ; RUNX3; Radiation enteritis.

MeSH terms

  • Animals
  • Cannabidiol* / pharmacology
  • Core Binding Factor Alpha 3 Subunit* / genetics
  • Core Binding Factor Alpha 3 Subunit* / metabolism
  • Core Binding Factor beta Subunit* / genetics
  • Core Binding Factor beta Subunit* / metabolism
  • Ferroptosis* / drug effects
  • Ferroptosis* / genetics
  • Humans
  • Intestines / pathology
  • Intestines / radiation effects
  • Mice
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / genetics
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / metabolism
  • Protein Multimerization / drug effects
  • Transcriptional Activation* / drug effects

Substances

  • Cannabidiol
  • Phospholipid Hydroperoxide Glutathione Peroxidase
  • Core Binding Factor Alpha 3 Subunit
  • Core Binding Factor beta Subunit
  • NF-kappa B