CA9 knockdown enhanced ionizing radiation-induced ferroptosis and radiosensitivity of hypoxic glioma cells

Int J Radiat Biol. 2023;99(12):1908-1924. doi: 10.1080/09553002.2023.2235433. Epub 2023 Jul 18.

Abstract

Purpose: Ferroptosis is a type of regulatory cell death, caused by excessive lipid peroxidation This study aimed to explore whether ionizing radiation could induce ferroptosis in glioma cells and whether carbonic anhydrase 9 (CA9) knockdown could enhance the killing effect of ionizing radiation on hypoxic glioma cells through ferroptosis.

Materials and methods: The protein levels of Acyl-CoA Synthetase Long Chain Family Member 4 (ACSL4) were detected by Western blot in glioma cells irradiated by different doses of X-ray. The relative mRNA levels of ferroptosis markers and intracellular iron-associated proteins were detected by Real-time qPCR. Lipid peroxidation of glioma cells was detected by oxidation-sensitive probe C11-BODIPY581/591 staining. CCK-8 Assay was used to detect cell viability after X-ray irradiation. Cloning formation assay was used to assess the radiosensitivity of glioma cells. The exposure of cell surface calreticulin was measured by immunofluorescence staining.

Results: X-ray induced lipid peroxidation and ferroptosis markers expression in U251 and GL261 glioma cells. Knockdown of CA9 in hypoxic glioma cells significantly altered the expression of iron regulation-related proteins and enhanced X-ray-induced ferroptosis and radiosensitivity. The ferroptosis inhibitor significantly improved the survival of cells irradiated by X-ray, while ferroptosis inducers (FINs) enhanced the lethal effect of X-ray on cells. Enhancing ferroptosis in glioma cells promoted the exposure and release of damage-associated molecular patterns (DAMPs).

Conclusions: Ionizing radiation can induce ferroptosis in glioma cells. CA9 knockdown can enhance the radiosensitivity of hypoxic glioma cells and overcome the resistance of ferroptosis under hypoxia. Enhancing ferroptosis will become a new idea to improve the efficacy of radiotherapy for glioma.

Keywords: DAMPs; Glioma; ferroptosis; hypoxia; radiosensitivity.

MeSH terms

  • Alarmins / metabolism
  • Animals
  • Carbonic Anhydrase IX* / genetics
  • Cell Line, Tumor
  • Ferroptosis*
  • Gene Knockdown Techniques
  • Glioma* / genetics
  • Glioma* / radiotherapy
  • Humans
  • Lipid Peroxidation
  • Long-Chain-Fatty-Acid-CoA Ligase
  • Mice
  • Radiation Tolerance*
  • Radiation, Ionizing
  • Tumor Hypoxia

Substances

  • Carbonic Anhydrase IX
  • Alarmins
  • Long-Chain-Fatty-Acid-CoA Ligase
  • CA9 protein, human