Transient ATM kinase inhibition disrupts DNA damage-induced sister chromatid exchange

Sci Signal. 2010 Jun 1;3(124):ra44. doi: 10.1126/scisignal.2000758.

Abstract

Cells derived from ataxia telangiectasia (A-T) patients exhibit defective cell cycle checkpoints because of mutations in the gene encoding ATM (ataxia telangiectasia mutated). After exposure to ionizing radiation (IR), A-T cells exhibit sensitivity to IR-induced cellular damage that results in increased chromosome aberrations and cell death (radiosensitivity). ATM is a member of a family of kinases that become activated in response to DNA damage. We showed that even transient inhibition of ATM kinase for 1 hour, initiated 15 minutes after cellular irradiation, resulted in an accumulation of persistent chromosome aberrations and increased cell death. Using reversible inhibitors of DNA-PK (DNA-dependent protein kinase), another kinase involved in responding to DNA damage, and ATM, we showed that these two kinases acted through distinct DNA repair mechanisms: ATM resolved DNA damage through a mechanism involving sister chromatid exchange (SCE), whereas DNA-PK acted through nonhomologous end joining. Furthermore, because DNA damage-induced SCE occurred in A-T fibroblasts that lack functional ATM protein, and the inhibitors of ATM kinase had no effect on DNA damage-induced SCE in A-T fibroblasts, we showed that the consequences of short-term inhibition of the kinase activity of ATM and adaptation to ATM protein disruption were distinct. This suggests that A-T fibroblasts have adapted to the loss of ATM and have alternative mechanisms to initiate SCE.

MeSH terms

  • Ataxia Telangiectasia Mutated Proteins
  • Cell Cycle Proteins* / antagonists & inhibitors
  • Cell Cycle Proteins* / metabolism
  • Cell Death / drug effects
  • Cell Death / radiation effects
  • Cell Line, Transformed
  • Chromosome Aberrations / drug effects
  • Chromosome Aberrations / radiation effects
  • Chromosomes, Human / metabolism*
  • DNA Damage* / drug effects
  • DNA Damage* / radiation effects
  • DNA-Activated Protein Kinase / antagonists & inhibitors
  • DNA-Activated Protein Kinase / metabolism
  • DNA-Binding Proteins* / antagonists & inhibitors
  • DNA-Binding Proteins* / metabolism
  • Fibroblasts / enzymology*
  • Gamma Rays / adverse effects*
  • Humans
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Serine-Threonine Kinases* / antagonists & inhibitors
  • Protein Serine-Threonine Kinases* / metabolism
  • Radiation Tolerance / drug effects
  • Radiation Tolerance / radiation effects
  • Sister Chromatid Exchange* / drug effects
  • Sister Chromatid Exchange* / radiation effects
  • Tumor Suppressor Proteins* / antagonists & inhibitors
  • Tumor Suppressor Proteins* / metabolism

Substances

  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Protein Kinase Inhibitors
  • Tumor Suppressor Proteins
  • ATM protein, human
  • Ataxia Telangiectasia Mutated Proteins
  • DNA-Activated Protein Kinase
  • Protein Serine-Threonine Kinases