Acute Hypoxia Does Not Alter Tumor Sensitivity to FLASH Radiation Therapy

Int J Radiat Oncol Biol Phys. 2024 Aug 1;119(5):1493-1505. doi: 10.1016/j.ijrobp.2024.02.015. Epub 2024 Feb 20.

Abstract

Purpose: Tumor hypoxia is a major cause of treatment resistance, especially to radiation therapy at conventional dose rate (CONV), and we wanted to assess whether hypoxia does alter tumor sensitivity to FLASH.

Methods and materials: We engrafted several tumor types (glioblastoma [GBM], head and neck cancer, and lung adenocarcinoma) subcutaneously in mice to provide a reliable and rigorous way to modulate oxygen supply via vascular clamping or carbogen breathing. We irradiated tumors using a single 20-Gy fraction at either CONV or FLASH, measured oxygen tension, monitored tumor growth, and sampled tumors for bulk RNAseq and pimonidazole analysis. Next, we inhibited glycolysis with trametinib in GBM tumors to enhance FLASH efficacy.

Results: Using various subcutaneous tumor models, and in contrast to CONV, FLASH retained antitumor efficacy under acute hypoxia. These findings show that in addition to normal tissue sparing, FLASH could overcome hypoxia-mediated tumor resistance. Follow-up molecular analysis using RNAseq profiling uncovered a FLASH-specific profile in human GBM that involved cell-cycle arrest, decreased ribosomal biogenesis, and a switch from oxidative phosphorylation to glycolysis. Glycolysis inhibition by trametinib enhanced FLASH efficacy in both normal and clamped conditions.

Conclusions: These data provide new and specific insights showing the efficacy of FLASH in a radiation-resistant context, proving an additional benefit of FLASH over CONV.

MeSH terms

  • Animals
  • Carbon Dioxide
  • Cell Cycle Checkpoints / radiation effects
  • Cell Line, Tumor
  • Glioblastoma* / metabolism
  • Glioblastoma* / radiotherapy
  • Glycolysis*
  • Head and Neck Neoplasms / radiotherapy
  • Humans
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / pathology
  • Lung Neoplasms / radiotherapy
  • Mice
  • Nitroimidazoles
  • Oxidative Phosphorylation
  • Oxygen / metabolism
  • Pyridones* / pharmacology
  • Pyridones* / therapeutic use
  • Pyrimidinones* / pharmacology
  • Pyrimidinones* / therapeutic use
  • Radiation Tolerance*
  • Tumor Hypoxia*

Substances

  • Pyrimidinones
  • trametinib
  • Pyridones
  • Nitroimidazoles
  • carbogen
  • pimonidazole
  • Oxygen
  • Carbon Dioxide