FBXL12 degrades FANCD2 to regulate replication recovery and promote cancer cell survival under conditions of replication stress

Mol Cell. 2023 Oct 19;83(20):3720-3739.e8. doi: 10.1016/j.molcel.2023.07.026. Epub 2023 Aug 16.

Abstract

Fanconi anemia (FA) signaling, a key genomic maintenance pathway, is activated in response to replication stress. Here, we report that phosphorylation of the pivotal pathway protein FANCD2 by CHK1 triggers its FBXL12-dependent proteasomal degradation, facilitating FANCD2 clearance at stalled replication forks. This promotes efficient DNA replication under conditions of CYCLIN E- and drug-induced replication stress. Reconstituting FANCD2-deficient fibroblasts with phosphodegron mutants failed to re-establish fork progression. In the absence of FBXL12, FANCD2 becomes trapped on chromatin, leading to replication stress and excessive DNA damage. In human cancers, FBXL12, CYCLIN E, and FA signaling are positively correlated, and FBXL12 upregulation is linked to reduced survival in patients with high CYCLIN E-expressing breast tumors. Finally, depletion of FBXL12 exacerbated oncogene-induced replication stress and sensitized cancer cells to drug-induced replication stress by WEE1 inhibition. Collectively, our results indicate that FBXL12 constitutes a vulnerability and a potential therapeutic target in CYCLIN E-overexpressing cancers.

Keywords: CYCLIN E; DNA damage; FANCD2; FBXL12; Fanconi anemia; SCF ubiquitin ligase; cancer vulnerability; replication stress; therapeutic target.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Survival / genetics
  • Chromatin / genetics
  • Cyclin E / genetics
  • Cyclin E / metabolism
  • DNA Damage
  • DNA Repair
  • DNA Replication / genetics
  • Fanconi Anemia Complementation Group D2 Protein / genetics
  • Fanconi Anemia Complementation Group D2 Protein / metabolism
  • Fanconi Anemia* / metabolism
  • Humans
  • Neoplasms* / genetics

Substances

  • Chromatin
  • Cyclin E
  • FANCD2 protein, human
  • Fanconi Anemia Complementation Group D2 Protein
  • Fbxl12 protein, human