DNA methyltransferase inhibitors induce a BRCAness phenotype that sensitizes NSCLC to PARP inhibitor and ionizing radiation

Proc Natl Acad Sci U S A. 2019 Nov 5;116(45):22609-22618. doi: 10.1073/pnas.1903765116. Epub 2019 Oct 7.

Abstract

A minority of cancers have breast cancer gene (BRCA) mutations that confer sensitivity to poly (ADP-ribose) polymerase (PARP) inhibitors (PARPis), but the role for PARPis in BRCA-proficient cancers is not well established. This suggests the need for novel combination therapies to expand the use of these drugs. Recent reports that low doses of DNA methyltransferase inhibitors (DNMTis) plus PARPis enhance PARPi efficacy in BRCA-proficient AML subtypes, breast, and ovarian cancer open up the possibility that this strategy may apply to other sporadic cancers. We identify a key mechanistic aspect of this combination therapy in nonsmall cell lung cancer (NSCLC): that the DNMTi component creates a BRCAness phenotype through downregulating expression of key homologous recombination and nonhomologous end-joining (NHEJ) genes. Importantly, from a translational perspective, the above changes in DNA repair processes allow our combinatorial PARPi and DNMTi therapy to robustly sensitize NSCLC cells to ionizing radiation in vitro and in vivo. Our combinatorial approach introduces a biomarker strategy and a potential therapy paradigm for treating BRCA-proficient cancers like NSCLC.

Keywords: DNA repair; homologous recombination defect; lung cancer; nonhomologous end-joining; poly (ADP-ribose) polymerase inhibitors.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents
  • BRCA1 Protein / genetics
  • BRCA2 Protein / genetics
  • Carcinoma, Non-Small-Cell Lung / drug therapy*
  • Carcinoma, Non-Small-Cell Lung / genetics
  • Carcinoma, Non-Small-Cell Lung / metabolism
  • Carcinoma, Non-Small-Cell Lung / radiotherapy*
  • Cell Line, Tumor
  • Combined Modality Therapy
  • DNA Modification Methylases / antagonists & inhibitors*
  • DNA Modification Methylases / metabolism
  • DNA Repair / drug effects
  • DNA Repair / radiation effects
  • Drug Therapy, Combination
  • Enzyme Inhibitors / administration & dosage*
  • Female
  • Homologous Recombination / drug effects
  • Homologous Recombination / radiation effects
  • Humans
  • Lung Neoplasms / drug therapy*
  • Lung Neoplasms / genetics
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / radiotherapy*
  • Male
  • Mice
  • Phthalazines / administration & dosage
  • Poly(ADP-ribose) Polymerase Inhibitors / administration & dosage*
  • Radiation, Ionizing

Substances

  • Antineoplastic Agents
  • BRCA1 Protein
  • BRCA2 Protein
  • Enzyme Inhibitors
  • Phthalazines
  • Poly(ADP-ribose) Polymerase Inhibitors
  • talazoparib
  • DNA Modification Methylases