ATR inhibition disrupts rewired homologous recombination and fork protection pathways in PARP inhibitor-resistant BRCA-deficient cancer cells

Genes Dev. 2017 Feb 1;31(3):318-332. doi: 10.1101/gad.290957.116. Epub 2017 Feb 27.

Abstract

Poly-(ADP-ribose) polymerase (PARP) inhibitors (PARPis) selectively kill BRCA1/2-deficient cells, but their efficacy in BRCA-deficient patients is limited by drug resistance. Here, we used derived cell lines and cells from patients to investigate how to overcome PARPi resistance. We found that the functions of BRCA1 in homologous recombination (HR) and replication fork protection are sequentially bypassed during the acquisition of PARPi resistance. Despite the lack of BRCA1, PARPi-resistant cells regain RAD51 loading to DNA double-stranded breaks (DSBs) and stalled replication forks, enabling two distinct mechanisms of PARPi resistance. Compared with BRCA1-proficient cells, PARPi-resistant BRCA1-deficient cells are increasingly dependent on ATR for survival. ATR inhibitors (ATRis) disrupt BRCA1-independent RAD51 loading to DSBs and stalled forks in PARPi-resistant BRCA1-deficient cells, overcoming both resistance mechanisms. In tumor cells derived from patients, ATRis also overcome the bypass of BRCA1/2 in fork protection. Thus, ATR inhibition is a unique strategy to overcome the PARPi resistance of BRCA-deficient cancers.

Keywords: ATR; BRCA-deficient cancer; PARP inhibitor.

Publication types

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

MeSH terms

  • Ataxia Telangiectasia Mutated Proteins / antagonists & inhibitors
  • BRCA1 Protein / deficiency
  • BRCA1 Protein / genetics
  • DNA Repair
  • DNA, Neoplasm
  • Drug Resistance, Neoplasm / genetics
  • Female
  • Homologous Recombination / drug effects
  • Homologous Recombination / genetics*
  • Humans
  • Ovarian Neoplasms / drug therapy
  • Ovarian Neoplasms / genetics*
  • Poly (ADP-Ribose) Polymerase-1 / antagonists & inhibitors*
  • Poly(ADP-ribose) Polymerase Inhibitors / pharmacology*
  • Tumor Cells, Cultured

Substances

  • BRCA1 Protein
  • BRCA1 protein, human
  • DNA, Neoplasm
  • Poly(ADP-ribose) Polymerase Inhibitors
  • PARP1 protein, human
  • Poly (ADP-Ribose) Polymerase-1
  • ATR protein, human
  • Ataxia Telangiectasia Mutated Proteins