FANCM promotes PARP inhibitor resistance by minimizing ssDNA gap formation and counteracting resection inhibition

Cell Rep. 2024 Jul 23;43(7):114464. doi: 10.1016/j.celrep.2024.114464. Epub 2024 Jul 8.

Abstract

Poly(ADP-ribose) polymerase inhibitors (PARPis) exhibit remarkable anticancer activity in tumors with homologous recombination (HR) gene mutations. However, the role of other DNA repair proteins in PARPi-induced lethality remains elusive. Here, we reveal that FANCM promotes PARPi resistance independent of the core Fanconi anemia (FA) complex. FANCM-depleted cells retain HR proficiency, acting independently of BRCA1 in response to PARPis. FANCM depletion leads to increased DNA damage in the second S phase after PARPi exposure, driven by elevated single-strand DNA (ssDNA) gap formation behind replication forks in the first S phase. These gaps arise from both 53BP1- and primase and DNA directed polymerase (PRIMPOL)-dependent mechanisms. Notably, FANCM-depleted cells also exhibit reduced resection of collapsed forks, while 53BP1 deletion restores resection and mitigates PARPi sensitivity. Our results suggest that FANCM counteracts 53BP1 to repair PARPi-induced DNA damage. Furthermore, FANCM depletion leads to increased chromatin bridges and micronuclei formation after PARPi treatment, elucidating the mechanism underlying extensive cell death in FANCM-depleted cells.

Keywords: 53BP1; CP: Molecular biology; DNA end resection; FANCM; PARP inhibitor; homologous recombination; single-stranded DNA gap.

MeSH terms

  • BRCA1 Protein / genetics
  • BRCA1 Protein / metabolism
  • Cell Line, Tumor
  • DNA Damage
  • DNA Helicases / genetics
  • DNA Helicases / metabolism
  • DNA Repair / drug effects
  • DNA, Single-Stranded* / metabolism
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics
  • Homologous Recombination / drug effects
  • Humans
  • Poly(ADP-ribose) Polymerase Inhibitors* / pharmacology
  • Tumor Suppressor p53-Binding Protein 1* / genetics
  • Tumor Suppressor p53-Binding Protein 1* / metabolism

Substances

  • Poly(ADP-ribose) Polymerase Inhibitors
  • FANCM protein, human
  • DNA, Single-Stranded
  • Tumor Suppressor p53-Binding Protein 1
  • DNA Helicases
  • TP53BP1 protein, human
  • BRCA1 Protein