Structural basis for a Polθ helicase small-molecule inhibitor revealed by cryo-EM

Nat Commun. 2024 Aug 14;15(1):7003. doi: 10.1038/s41467-024-51351-4.

Abstract

DNA polymerase theta (Polθ) is a DNA helicase-polymerase protein that facilitates DNA repair and is synthetic lethal with homology-directed repair (HDR) factors. Thus, Polθ is a promising precision oncology drug-target in HDR-deficient cancers. Here, we characterize the binding and mechanism of action of a Polθ helicase (Polθ-hel) small-molecule inhibitor (AB25583) using cryo-EM. AB25583 exhibits 6 nM IC50 against Polθ-hel, selectively kills BRCA1/2-deficient cells, and acts synergistically with olaparib in cancer cells harboring pathogenic BRCA1/2 mutations. Cryo-EM uncovers predominantly dimeric Polθ-hel:AB25583 complex structures at 3.0-3.2 Å. The structures reveal a binding-pocket deep inside the helicase central-channel, which underscores the high specificity and potency of AB25583. The cryo-EM structures in conjunction with biochemical data indicate that AB25583 inhibits the ATPase activity of Polθ-hel helicase via an allosteric mechanism. These detailed structural data and insights about AB25583 inhibition pave the way for accelerating drug development targeting Polθ-hel in HDR-deficient cancers.

MeSH terms

  • Adenosine Triphosphatases / antagonists & inhibitors
  • Adenosine Triphosphatases / metabolism
  • BRCA1 Protein / chemistry
  • BRCA1 Protein / genetics
  • BRCA1 Protein / metabolism
  • BRCA2 Protein / chemistry
  • BRCA2 Protein / genetics
  • BRCA2 Protein / metabolism
  • Cell Line, Tumor
  • Cryoelectron Microscopy*
  • DNA Helicases* / antagonists & inhibitors
  • DNA Helicases* / chemistry
  • DNA Helicases* / genetics
  • DNA Helicases* / metabolism
  • DNA Polymerase theta*
  • DNA-Directed DNA Polymerase* / chemistry
  • DNA-Directed DNA Polymerase* / genetics
  • DNA-Directed DNA Polymerase* / metabolism
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Models, Molecular
  • Phthalazines / chemistry
  • Phthalazines / pharmacology
  • Piperazines / chemistry
  • Piperazines / pharmacology
  • Protein Binding

Substances

  • DNA Helicases
  • DNA-Directed DNA Polymerase
  • DNA Polymerase theta
  • BRCA2 Protein
  • BRCA1 Protein
  • Piperazines
  • Phthalazines
  • olaparib
  • BRCA2 protein, human
  • BRCA1 protein, human
  • Enzyme Inhibitors
  • Adenosine Triphosphatases