Oncogenic IDH mutations increase heterochromatin-related replication stress without impacting homologous recombination

Mol Cell. 2023 Jul 6;83(13):2347-2356.e8. doi: 10.1016/j.molcel.2023.05.026. Epub 2023 Jun 12.

Abstract

Oncogenic mutations in isocitrate dehydrogenases 1 and 2 (IDH1/2) produce 2-hydroxyglutarate (2HG), which inhibits dioxygenases that modulate chromatin dynamics. The effects of 2HG have been reported to sensitize IDH tumors to poly-(ADP-ribose) polymerase (PARP) inhibitors. However, unlike PARP-inhibitor-sensitive BRCA1/2 tumors, which exhibit impaired homologous recombination, IDH-mutant tumors have a silent mutational profile and lack signatures associated with impaired homologous recombination. Instead, 2HG-producing IDH mutations lead to a heterochromatin-dependent slowing of DNA replication accompanied by increased replication stress and DNA double-strand breaks. This replicative stress manifests as replication fork slowing, but the breaks are repaired without a significant increase in mutation burden. Faithful resolution of replicative stress in IDH-mutant cells is dependent on poly-(ADP-ribosylation). Treatment with PARP inhibitors increases DNA replication but results in incomplete DNA repair. These findings demonstrate a role for PARP in the replication of heterochromatin and further validate PARP as a therapeutic target in IDH-mutant tumors.

Keywords: PARP; dioxygenase; heterochromatin; isocitrate dehydrogenase; oncometabolite; replication stress.

MeSH terms

  • BRCA1 Protein* / genetics
  • BRCA2 Protein / genetics
  • Heterochromatin / genetics
  • Homologous Recombination / genetics
  • Humans
  • Isocitrate Dehydrogenase / genetics
  • Mutation
  • Neoplasms* / drug therapy
  • Neoplasms* / genetics
  • Poly(ADP-ribose) Polymerase Inhibitors / pharmacology

Substances

  • BRCA1 protein, human
  • BRCA1 Protein
  • Heterochromatin
  • Poly(ADP-ribose) Polymerase Inhibitors
  • BRCA2 protein, human
  • BRCA2 Protein
  • Isocitrate Dehydrogenase