BET bromodomain inhibition potentiates radiosensitivity in models of H3K27-altered diffuse midline glioma

J Clin Invest. 2024 May 21;134(13):e174794. doi: 10.1172/JCI174794.

Abstract

Diffuse midline glioma (DMG) H3K27-altered is one of the most malignant childhood cancers. Radiation therapy remains the only effective treatment yet provides a 5-year survival rate of only 1%. Several clinical trials have attempted to enhance radiation antitumor activity using radiosensitizing agents, although none have been successful. Given this, there is a critical need for identifying effective therapeutics to enhance radiation sensitivity for the treatment of DMG. Using high-throughput radiosensitivity screening, we identified bromo- and extraterminal domain (BET) protein inhibitors as potent radiosensitizers in DMG cells. Genetic and pharmacologic inhibition of BET bromodomain activity reduced DMG cell proliferation and enhanced radiation-induced DNA damage by inhibiting DNA repair pathways. RNA-Seq and the CUT&RUN (cleavage under targets and release using nuclease) analysis showed that BET bromodomain inhibitors regulated the expression of DNA repair genes mediated by H3K27 acetylation at enhancers. BET bromodomain inhibitors enhanced DMG radiation response in patient-derived xenografts as well as genetically engineered mouse models. Together, our results highlight BET bromodomain inhibitors as potential radiosensitizer and provide a rationale for developing combination therapy with radiation for the treatment of DMG.

Keywords: Brain cancer; Epigenetics; Oncology; Therapeutics; Translation.

MeSH terms

  • Animals
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology
  • Brain Neoplasms / radiotherapy
  • Bromodomain Containing Proteins
  • Cell Line, Tumor
  • DNA Damage
  • DNA Repair / drug effects
  • Glioma / drug therapy
  • Glioma / genetics
  • Glioma / metabolism
  • Glioma / pathology
  • Glioma / radiotherapy
  • Histones* / genetics
  • Histones* / metabolism
  • Humans
  • Mice
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism
  • Proteins
  • Radiation Tolerance* / drug effects
  • Radiation Tolerance* / genetics
  • Radiation-Sensitizing Agents / pharmacology
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Histones
  • Radiation-Sensitizing Agents
  • bromodomain and extra-terminal domain protein, human
  • Transcription Factors
  • Neoplasm Proteins
  • Bromodomain Containing Proteins
  • Proteins