Two-ended recombination at a Flp-nickase-broken replication fork

Mol Cell. 2025 Jan 2;85(1):78-90.e3. doi: 10.1016/j.molcel.2024.11.006. Epub 2024 Dec 3.

Abstract

Replication fork collision with a DNA nick can generate a one-ended break, fostering genomic instability. The opposing fork's collision with the nick could form a second DNA end, enabling conservative repair by homologous recombination (HR). To study mechanisms of nickase-induced HR, we developed the Flp recombinase "step arrest" nickase in mammalian cells. A Flp-nick induces two-ended, BRCA2/RAD51-dependent short tract gene conversion (STGC), BRCA2/RAD51-independent long tract gene conversion, and discoordinated two-ended invasions. HR pathways induced by a replication-independent break and the Flp-nickase differ in their dependence on BRCA1, MRE11, and CtIP. To determine the origin of the second DNA end during Flp-nickase-induced STGC, we blocked the opposing fork using a Tus/Ter replication fork barrier (RFB). Flp-nickase-induced STGC remained robust and two ended. Thus, a single replication fork's collision with a Flp-nick triggers two-ended HR, possibly reflecting replicative bypass of lagging strand nicks. This response may limit genomic instability during replication of nicked DNA.

Keywords: BRCA1; Camptothecin; DNA nick; DNA-protein crosslink; Flp recombinase; Tus/Ter; break-induced replication; homologous recombination; replication fork breakage; replication stress.

MeSH terms

  • BRCA1 Protein / genetics
  • BRCA1 Protein / metabolism
  • BRCA2 Protein* / genetics
  • BRCA2 Protein* / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • DNA Nucleotidyltransferases* / genetics
  • DNA Nucleotidyltransferases* / metabolism
  • DNA Replication*
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Deoxyribonuclease I / genetics
  • Deoxyribonuclease I / metabolism
  • Endodeoxyribonucleases
  • Gene Conversion
  • Genomic Instability
  • Homologous Recombination
  • Humans
  • MRE11 Homologue Protein / genetics
  • MRE11 Homologue Protein / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Rad51 Recombinase* / genetics
  • Rad51 Recombinase* / metabolism

Substances

  • Rad51 Recombinase
  • FLP recombinase
  • DNA Nucleotidyltransferases
  • BRCA2 Protein
  • DNA-Binding Proteins
  • Deoxyribonuclease I
  • MRE11 Homologue Protein
  • RAD51 protein, human
  • BRCA2 protein, human
  • MRE11 protein, human
  • BRCA1 Protein
  • RBBP8 protein, human
  • Carrier Proteins
  • Nuclear Proteins
  • BRCA1 protein, human
  • Endodeoxyribonucleases