FANCD2-FANCI surveys DNA and recognizes double- to single-stranded junctions

Nature. 2024 Aug;632(8027):1165-1173. doi: 10.1038/s41586-024-07770-w. Epub 2024 Jul 31.

Abstract

DNA crosslinks block DNA replication and are repaired by the Fanconi anaemia pathway. The FANCD2-FANCI (D2-I) protein complex is central to this process as it initiates repair by coordinating DNA incisions around the lesion1. However, D2-I is also known to have a more general role in DNA repair and in protecting stalled replication forks from unscheduled degradation2-4. At present, it is unclear how DNA crosslinks are recognized and how D2-I functions in replication fork protection. Here, using single-molecule imaging, we show that D2-I is a sliding clamp that binds to and diffuses on double-stranded DNA. Notably, sliding D2-I stalls on encountering single-stranded-double-stranded (ss-ds) DNA junctions, structures that are generated when replication forks stall at DNA lesions5. Using cryogenic electron microscopy, we determined structures of D2-I on DNA that show that stalled D2-I makes specific interactions with the ss-dsDNA junction that are distinct from those made by sliding D2-I. Thus, D2-I surveys dsDNA and, when it reaches an ssDNA gap, it specifically clamps onto ss-dsDNA junctions. Because ss-dsDNA junctions are found at stalled replication forks, D2-I can identify sites of DNA damage. Therefore, our data provide a unified molecular mechanism that reconciles the roles of D2-I in the recognition and protection of stalled replication forks in several DNA repair pathways.

MeSH terms

  • Animals
  • Cell Extracts
  • Cryoelectron Microscopy
  • DNA Damage*
  • DNA Repair*
  • DNA Replication*
  • DNA* / chemistry
  • DNA* / metabolism
  • DNA* / ultrastructure
  • DNA, Single-Stranded* / chemistry
  • DNA, Single-Stranded* / metabolism
  • DNA, Single-Stranded* / ultrastructure
  • Diffusion
  • Fanconi Anemia Complementation Group D2 Protein* / chemistry
  • Fanconi Anemia Complementation Group D2 Protein* / metabolism
  • Fanconi Anemia Complementation Group D2 Protein* / ultrastructure
  • Fanconi Anemia Complementation Group Proteins* / chemistry
  • Fanconi Anemia Complementation Group Proteins* / metabolism
  • Fanconi Anemia Complementation Group Proteins* / ultrastructure
  • Female
  • Humans
  • Models, Molecular
  • Protein Binding
  • Single Molecule Imaging
  • Xenopus laevis

Substances

  • Cell Extracts
  • DNA
  • DNA, Single-Stranded
  • FANCD2 protein, human
  • FANCI protein, human
  • Fanconi Anemia Complementation Group D2 Protein
  • Fanconi Anemia Complementation Group Proteins