KBM-mediated interactions with KU80 promote cellular resistance to DNA replication stress in CHO cells

DNA Repair (Amst). 2024 Aug:140:103710. doi: 10.1016/j.dnarep.2024.103710. Epub 2024 Jun 10.

Abstract

The KU heterodimer (KU70/80) is rapidly recruited to DNA double-strand breaks (DSBs) to regulate their processing and repair. Previous work has revealed that the amino-terminal von Willebrand-like (vWA-like) domain in KU80 harbours a conserved hydrophobic pocket that interacts with a short peptide motif known as the Ku-binding motif (KBM). The KBM is present in a variety of DNA repair proteins such as APLF, CYREN, and Werner protein (WRN). Here, to investigate the importance of KBM-mediated protein-protein interactions for KU80 function, we employed KU80-deficient Chinese Hamster Ovary (Xrs-6) cells transfected with RFP-tagged wild-type human KU80 or KU80 harbouring a mutant vWA-like domain (KU80L68R). Surprisingly, while mutant RFP-KU80L68R largely or entirely restored NHEJ efficiency and radiation resistance in KU80-deficient Xrs-6 cells, it failed to restore cellular resistance to DNA replication stress induced by camptothecin (CPT) or hydroxyurea (HU). Moreover, KU80-deficient Xrs-6 cells expressing RFP-KU80L68R accumulated pan-nuclear γH2AX in an S/G2-phase-dependent manner following treatment with CPT or HU, suggesting that the binding of KU80 to one or more KBM-containing proteins is required for the processing and/or repair of DNA ends that arise during DNA replication stress. Consistent with this idea, depletion of WRN helicase/exonuclease recapitulated the CPT-induced γH2AX phenotype, and did so epistatically with mutation of the KU80 vWA-like domain. These data identify a role for the KBM-binding by KU80 in the response and resistance of CHO cells to arrested and/or collapsed DNA replication forks, and implicate the KBM-mediated interaction of KU80 with WRN as a critical effector of this role.

Keywords: DNA-PK; Double-strand break; KU; KU binding motif; NHEJ; Replication stress.

MeSH terms

  • Animals
  • CHO Cells
  • Camptothecin / pharmacology
  • Cricetinae
  • Cricetulus*
  • DNA Breaks, Double-Stranded
  • DNA End-Joining Repair
  • DNA Replication*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Humans
  • Hydroxyurea / pharmacology
  • Ku Autoantigen* / genetics
  • Ku Autoantigen* / metabolism
  • Protein Binding
  • Werner Syndrome Helicase / genetics
  • Werner Syndrome Helicase / metabolism

Substances

  • Ku Autoantigen
  • DNA-Binding Proteins
  • Werner Syndrome Helicase
  • Camptothecin
  • WRN protein, human
  • Hydroxyurea
  • Xrcc6 protein, human