Autophosphorylation transforms DNA-PK from protecting to processing DNA ends

Mol Cell. 2022 Jan 6;82(1):177-189.e4. doi: 10.1016/j.molcel.2021.11.025. Epub 2021 Dec 21.

Abstract

The DNA-dependent protein kinase (DNA-PK) initially protects broken DNA ends but then promotes their processing during non-homologous end joining (NHEJ). Before ligation by NHEJ, DNA hairpin ends generated during V(D)J recombination must be opened by the Artemis nuclease, together with autophosphorylated DNA-PK. Structures of DNA-PK bound to DNA before and after phosphorylation, and in complex with Artemis and a DNA hairpin, reveal an essential functional switch. When bound to open DNA ends in its protection mode, DNA-PK is inhibited for cis-autophosphorylation of the so-called ABCDE cluster but activated for phosphorylation of other targets. In contrast, DNA hairpin ends promote cis-autophosphorylation. Phosphorylation of four Thr residues in ABCDE leads to gross structural rearrangement of DNA-PK, widening the DNA binding groove for Artemis recruitment and hairpin cleavage. Meanwhile, Artemis locks DNA-PK into the kinase-inactive state. Kinase activity and autophosphorylation of DNA-PK are regulated by different DNA ends, feeding forward to coordinate NHEJ events.

Keywords: Artemis; DNA-PKcs; Ku70; Ku80; NHEJ; SCID; V(D)J recombination; hairpin.

Publication types

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

MeSH terms

  • DNA Damage*
  • DNA End-Joining Repair*
  • DNA, Neoplasm / genetics
  • DNA, Neoplasm / metabolism*
  • DNA-Activated Protein Kinase / genetics
  • DNA-Activated Protein Kinase / metabolism*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Endonucleases / genetics
  • Endonucleases / metabolism
  • Enzyme Activation
  • Female
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Ku Autoantigen / genetics
  • Ku Autoantigen / metabolism
  • Nucleic Acid Conformation
  • Phosphorylation
  • Protein Binding
  • Uterine Cervical Neoplasms / enzymology*
  • Uterine Cervical Neoplasms / genetics
  • Uterine Cervical Neoplasms / pathology

Substances

  • DNA, Neoplasm
  • DNA-Binding Proteins
  • DNA-Activated Protein Kinase
  • PRKDC protein, human
  • DCLRE1C protein, human
  • Endonucleases
  • XRCC5 protein, human
  • Xrcc6 protein, human
  • Ku Autoantigen