ATR-Chk1 signaling pathway and homologous recombinational repair protect cells from 5-fluorouracil cytotoxicity

DNA Repair (Amst). 2012 Mar 1;11(3):247-58. doi: 10.1016/j.dnarep.2011.11.005. Epub 2011 Dec 20.

Abstract

5-Fluorouracil (5-FU) has long been a mainstay antimetabolite chemotherapeutic drug for the treatment of major solid tumors, particularly colorectal cancer. 5-FU is processed intracellularly to yield active metabolites that compromise RNA and DNA metabolism. However, the mechanisms responsible for its cytotoxicity are not fully understood. From the phenotypic analysis of mutant chicken B lymphoma DT40 cells, we found that homologous recombinational repair (HRR), involving Rad54 and BRCA2, and the ATR-Chk1 signaling pathway, involving Rad9 and Rad17, significantly contribute to 5-FU tolerance. 5-FU induced γH2AX nuclear foci, which were colocalized with the key HRR factor Rad51, but not with DNA double-strand breaks (DSBs), in a dose-dependent manner as cells accumulated in the S phase. Inhibition of Chk1 kinase by UCN-01 increased 5-FU-induced γH2AX and enhanced 5-FU cytotoxicity not only in wild-type cells but also in Rad54- or BRCA2-deficient cells, suggesting that HRR and Chk1 kinase have non-overlapping roles in 5-FU tolerance. 5-FU-induced Chk1 phosphorylation was significantly impaired in Rad9- or Rad17-deficient cells, and severe γH2AX nuclear foci and DSBs were formed, which was followed by apoptosis. Finally, inhibition of Chk1 kinase by UCN-01 increased 5-FU-induced γH2AX nuclear foci and enhanced 5-FU cytotoxicity in Rad9- or Rad17-deficient cells. These results suggest that Rad9- and Rad17-independent activation of the ATR-Chk1 signaling pathway also significantly contributes to 5-FU tolerance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Cell Cycle Proteins / metabolism
  • Cell Death / drug effects
  • Cell Line, Tumor
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism*
  • Checkpoint Kinase 1
  • Chickens
  • Cytoprotection / drug effects*
  • DNA Breaks, Double-Stranded / drug effects
  • Fanconi Anemia Complementation Group D2 Protein / metabolism
  • Fluorouracil / pharmacology*
  • Histones / metabolism
  • Lymphoma, B-Cell / enzymology
  • Lymphoma, B-Cell / pathology
  • Mutation / genetics
  • Phosphorylation / drug effects
  • Protein Kinases / metabolism*
  • Protein Serine-Threonine Kinases / metabolism*
  • Recombinational DNA Repair / drug effects*
  • Signal Transduction / drug effects*
  • Staurosporine / analogs & derivatives
  • Staurosporine / pharmacology
  • Time Factors

Substances

  • Cell Cycle Proteins
  • Fanconi Anemia Complementation Group D2 Protein
  • Histones
  • rad9 protein
  • 7-hydroxystaurosporine
  • Protein Kinases
  • Checkpoint Kinase 1
  • Protein Serine-Threonine Kinases
  • Staurosporine
  • Fluorouracil