Positioning loss of PARP1 activity as the central toxic event in BRCA-deficient cancer

DNA Repair (Amst). 2024 Dec:144:103775. doi: 10.1016/j.dnarep.2024.103775. Epub 2024 Oct 19.

Abstract

The mechanisms by which poly(ADP-ribose) polymerase 1 (PARP1) inhibitors (PARPi)s inflict replication stress and/or DNA damage are potentially numerous. PARPi toxicity could derive from loss of its catalytic activity and/or its physical trapping of PARP1 onto DNA that perturbs not only PARP1 function in DNA repair and DNA replication, but also obstructs compensating pathways. The combined disruption of PARP1 with either of the hereditary breast and ovarian cancer genes, BRCA1 or BRCA2 (BRCA), results in synthetic lethality. This has driven the development of PARP inhibitors as therapies for BRCA-mutant cancers. In this review, we focus on recent findings that highlight loss of PARP1 catalytic activity, rather than PARPi-induced allosteric trapping, as central to PARPi efficacy in BRCA deficient cells. However, we also review findings that PARP-trapping is an effective strategy in other genetic deficiencies. Together, we conclude that the mechanism-of-action of PARP inhibitors is not unilateral; with loss of activity or enhanced trapping differentially killing depending on the genetic context. Therefore, effectively targeting cancer cells requires an intricate understanding of their key underlying vulnerabilities.

Keywords: BRCA cancers; DNA repair; DNA replication; PARP1 inhibitors; Replication forks; Replication gaps.

Publication types

  • Review

MeSH terms

  • Animals
  • BRCA1 Protein* / genetics
  • BRCA1 Protein* / metabolism
  • BRCA2 Protein / genetics
  • BRCA2 Protein / metabolism
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism
  • DNA Damage
  • DNA Repair
  • DNA Replication
  • Female
  • Humans
  • Neoplasms / drug therapy
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Ovarian Neoplasms / drug therapy
  • Ovarian Neoplasms / genetics
  • Ovarian Neoplasms / metabolism
  • Poly (ADP-Ribose) Polymerase-1* / antagonists & inhibitors
  • Poly (ADP-Ribose) Polymerase-1* / genetics
  • Poly (ADP-Ribose) Polymerase-1* / metabolism
  • Poly(ADP-ribose) Polymerase Inhibitors* / pharmacology

Substances

  • Poly(ADP-ribose) Polymerase Inhibitors
  • Poly (ADP-Ribose) Polymerase-1
  • BRCA1 Protein
  • PARP1 protein, human
  • BRCA2 Protein
  • BRCA1 protein, human
  • BRCA2 protein, human