Synergistic targeting and resistance to PARP inhibition in DNA damage repair-deficient pancreatic cancer

Gut. 2021 Apr;70(4):743-760. doi: 10.1136/gutjnl-2019-319970. Epub 2020 Sep 1.

Abstract

Objective: ATM serine/threonine kinase (ATM) is the most frequently mutated DNA damage response gene, involved in homologous recombination (HR), in pancreatic ductal adenocarcinoma (PDAC).

Design: Combinational synergy screening was performed to endeavour a genotype-tailored targeted therapy.

Results: Synergy was found on inhibition of PARP, ATR and DNA-PKcs (PAD) leading to synthetic lethality in ATM-deficient murine and human PDAC. Mechanistically, PAD-induced PARP trapping, replication fork stalling and mitosis defects leading to P53-mediated apoptosis. Most importantly, chemical inhibition of ATM sensitises human PDAC cells toward PAD with long-term tumour control in vivo. Finally, we anticipated and elucidated PARP inhibitor resistance within the ATM-null background via whole exome sequencing. Arising cells were aneuploid, underwent epithelial-mesenchymal-transition and acquired multidrug resistance (MDR) due to upregulation of drug transporters and a bypass within the DNA repair machinery. These functional observations were mirrored in copy number variations affecting a region on chromosome 5 comprising several of the upregulated MDR genes. Using these findings, we ultimately propose alternative strategies to overcome the resistance.

Conclusion: Analysis of the molecular susceptibilities triggered by ATM deficiency in PDAC allow elaboration of an efficient mutation-specific combinational therapeutic approach that can be also implemented in a genotype-independent manner by ATM inhibition.

Keywords: DNA damage; drug resistance; pancreas; pancreatic cancer; pancreatic tumours.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / drug therapy
  • Adenocarcinoma / genetics*
  • Animals
  • Apoptosis
  • Ataxia Telangiectasia Mutated Proteins / genetics*
  • Carcinoma, Pancreatic Ductal / drug therapy
  • Carcinoma, Pancreatic Ductal / genetics*
  • Cell Line, Tumor
  • Cell Survival
  • DNA Copy Number Variations
  • DNA Damage
  • DNA Repair
  • Drug Resistance, Multiple / genetics
  • Drug Synergism
  • Epithelial-Mesenchymal Transition
  • Genotype
  • Homologous Recombination*
  • Humans
  • Mice
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / genetics*
  • Poly(ADP-ribose) Polymerase Inhibitors / pharmacology*
  • Prognosis

Substances

  • Poly(ADP-ribose) Polymerase Inhibitors
  • ATM protein, human
  • Ataxia Telangiectasia Mutated Proteins