Targeting DNA double strand break repair with hyperthermia and DNA-PKcs inhibition to enhance the effect of radiation treatment

Oncotarget. 2016 Oct 4;7(40):65504-65513. doi: 10.18632/oncotarget.11798.

Abstract

Radiotherapy is based on the induction of lethal DNA damage, primarily DNA double-strand breaks (DSB). Efficient DSB repair via Non-Homologous End Joining or Homologous Recombination can therefore undermine the efficacy of radiotherapy. By suppressing DNA-DSB repair with hyperthermia (HT) and DNA-PKcs inhibitor NU7441 (DNA-PKcsi), we aim to enhance the effect of radiation.The sensitizing effect of HT for 1 hour at 42°C and DNA-PKcsi [1 μM] to radiation treatment was investigated in cervical and breast cancer cells, primary breast cancer sphere cells (BCSCs) enriched for cancer stem cells, and in an in vivo human tumor model. A significant radio-enhancement effect was observed for all cell types when DNA-PKcsi and HT were applied separately, and when both were combined, HT and DNA-PKcsi enhanced radio-sensitivity to an even greater extent. Strikingly, combined treatment resulted in significantly lower survival rates, 2 to 2.5 fold increase in apoptosis, more residual DNA-DSB 6 h post treatment and a G2-phase arrest. In addition, tumor growth analysis in vivo showed significant reduction in tumor growth and elevated caspase-3 activity when radiation was combined with HT and DNA-PKcsi compared to radiation alone. Importantly, no toxic side effects of HT or DNA-PKcsi were found.In conclusion, inhibiting DNA-DSB repair using HT and DNA-PKcsi before radiotherapy leads to enhanced cytotoxicity in cancer cells. This effect was even noticed in the more radio-resistant BCSCs, which are clearly sensitized by combined treatment. Therefore, the addition of HT and DNA-PKcsi to conventional radiotherapy is promising and might contribute to more efficient tumor control and patient outcome.

Keywords: DNA repair; double-strand breaks; hyperthermia; radiation oncology.

MeSH terms

  • Animals
  • Breast Neoplasms / pathology
  • Breast Neoplasms / therapy*
  • Chromones / pharmacology*
  • DNA Breaks, Double-Stranded
  • DNA Damage
  • DNA End-Joining Repair
  • DNA Repair
  • DNA-Activated Protein Kinase / antagonists & inhibitors*
  • Female
  • Homologous Recombination
  • Humans
  • Hyperthermia, Induced*
  • Mice
  • Mice, Nude
  • Morpholines / pharmacology*
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / pathology
  • Neoplastic Stem Cells / radiation effects*
  • Radiation Tolerance
  • Radiation-Sensitizing Agents / pharmacology*
  • Radiotherapy
  • Tumor Cells, Cultured
  • Uterine Cervical Neoplasms / pathology
  • Uterine Cervical Neoplasms / therapy*

Substances

  • 8-dibenzothiophen-4-yl-2-morpholin-4-yl-chromen-4-one
  • Chromones
  • Morpholines
  • Radiation-Sensitizing Agents
  • DNA-Activated Protein Kinase