Inhibition of DNA repair as a mechanism of enhanced radioresponse of head and neck carcinoma cells by a selective cyclooxygenase-2 inhibitor, celecoxib

Int J Radiat Oncol Biol Phys. 2005 Oct 1;63(2):520-8. doi: 10.1016/j.ijrobp.2005.06.007.

Abstract

Purpose: Previously, we reported that inhibitors of cyclooxygenase-2 (COX-2) enzyme enhanced murine and human tumor cell response to radiation in vitro and in vivo. However, the molecular mechanisms mediating the effects of COX-2 inhibitors are not clear. The present study was designed to investigate the ability of celecoxib, a selective COX-2 inhibitor, to sensitize human head-and-neck cancer cell line, HN5, to radiation, and examine its effects on DNA repair, which may be a potential mechanism of radiosensitization.

Methods and materials: Cells were assessed for the effect of celecoxib (5-50 microM), by 3-[4,5-dimethylthiozol-2-yl]-2,5-diphenyltetrazolium bromide assay for growth inhibition and by clonogenic cell survival assay for the radiosensitizing effect. Kinase assay and Western analysis were conducted to assess the effect of celecoxib on DNA-dependent protein kinase catalytic subunit (PKcs) and Ku proteins. Electrophoretic mobility shift assays (EMSA) were performed to determine the DNA-binding activity of Ku/DNA-PKcs protein complex and nuclear factor kappa B (NFkappaB).

Results: Celecoxib (10 and 50 microM, for 2 days) inhibited the HN5 cell growth and significantly enhanced the cell radiosensitivity in a dose-dependent manner. It also reduced the shoulder region on the radiation-survival curve, suggesting that inhibition of DNA repair processes may have occurred. Western blot analysis demonstrated that celecoxib downregulated the expression of Ku70 protein and inhibited the kinase activity of DNA-PKcs, which are involved in the double-stranded DNA-break repair machinery. By EMSA, it was further shown that celecoxib reduced DNA-binding activity of Ku/DNA-PKcs protein complex. In addition, celecoxib inhibited the constitutively active NFkappaB and the radiation-induced NFkappaB in HN5 cells, suggesting that NFkappaB may play a role in mediating the effects of celecoxib.

Conclusions: Celecoxib strongly enhanced the sensitivity of HN5 carcinoma cells to radiation, which, mechanistically, can be attributed to the inhibition of DNA repair processes in radiation-damaged cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Blotting, Western
  • Celecoxib
  • Cell Line, Tumor / drug effects
  • Cyclooxygenase Inhibitors / therapeutic use*
  • DNA / metabolism
  • DNA Repair / drug effects*
  • DNA-Activated Protein Kinase
  • DNA-Binding Proteins / analysis
  • DNA-Binding Proteins / metabolism
  • Down-Regulation
  • Head and Neck Neoplasms / pathology
  • Head and Neck Neoplasms / radiotherapy*
  • Humans
  • NF-kappa B / metabolism
  • Nuclear Proteins
  • Protein Serine-Threonine Kinases / analysis
  • Protein Serine-Threonine Kinases / metabolism
  • Pyrazoles / therapeutic use*
  • Radiation-Sensitizing Agents / therapeutic use*
  • Sulfonamides / therapeutic use*

Substances

  • Cyclooxygenase Inhibitors
  • DNA-Binding Proteins
  • NF-kappa B
  • Nuclear Proteins
  • Pyrazoles
  • Radiation-Sensitizing Agents
  • Sulfonamides
  • DNA
  • DNA-Activated Protein Kinase
  • PRKDC protein, human
  • Protein Serine-Threonine Kinases
  • Celecoxib