Treatment regimen determines whether an HIF-1 inhibitor enhances or inhibits the effect of radiation therapy

Br J Cancer. 2009 Mar 10;100(5):747-57. doi: 10.1038/sj.bjc.6604939. Epub 2009 Feb 17.

Abstract

Hypoxia-inducible factor-1 (HIF-1) has been reported to promote tumour radioresistance; therefore, it is recognised as an excellent target during radiation therapy. However, the inhibition of HIF-1 in unsuitable timing can suppress rather than enhance the effect of radiation therapy because its anti-angiogenic effect increases the radioresistant hypoxic fraction. In this study, we imaged changes of HIF-1 activity after treatment with radiation and/or an HIF-1 inhibitor, YC-1, and optimised their combination. Hypoxic tumour cells were reoxygenated 6 h postirradiation, leading to von Hippel-Lindau (VHL)-dependent proteolysis of HIF-1alpha and a resultant decrease in HIF-1 activity. The activity then increased as HIF-1alpha accumulated in the reoxygenated regions 24 h postirradiation. Meanwhile, YC-1 temporarily but significantly suppressed HIF-1 activity, leading to a decrease in microvessel density and an increase in tumour hypoxia. On treatment with YC-1 and then radiation, the YC-1-mediated increase in tumour hypoxia suppressed the effect of radiation therapy, whereas on treatment in the reverse order, YC-1 suppressed the postirradiation upregulation of HIF-1 activity and consequently delayed tumour growth. These results indicate that treatment regimen determines whether an HIF-1 inhibitor enhances or inhibits the therapeutic effect of radiation, and the suppression of the postirradiation upregulation of HIF-1 activity is important for the best therapeutic benefit.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Hypoxia / drug effects
  • Cell Hypoxia / radiation effects
  • Furans / pharmacology
  • Furans / therapeutic use
  • HeLa Cells
  • Humans
  • Hypoxia-Inducible Factor 1 / antagonists & inhibitors*
  • Hypoxia-Inducible Factor 1 / metabolism
  • Indazoles / pharmacology
  • Indazoles / therapeutic use
  • Mice
  • Mice, SCID
  • Neoplasms / metabolism
  • Neoplasms / radiotherapy*
  • Oxygen Consumption / drug effects
  • Oxygen Consumption / radiation effects
  • Radiation Tolerance / drug effects*
  • Radiation-Protective Agents / pharmacology
  • Radiation-Protective Agents / therapeutic use
  • Radiation-Sensitizing Agents / pharmacology
  • Radiation-Sensitizing Agents / therapeutic use*
  • Treatment Outcome
  • Tumor Cells, Cultured
  • Xenograft Model Antitumor Assays

Substances

  • Furans
  • Hypoxia-Inducible Factor 1
  • Indazoles
  • Radiation-Protective Agents
  • Radiation-Sensitizing Agents
  • 3-(5'-hydroxymethyl-2'-furyl)-1-benzylindazole