DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities

Mol Cell. 2014 Jan 9;53(1):7-18. doi: 10.1016/j.molcel.2013.11.003. Epub 2013 Dec 5.

Abstract

MRE11 within the MRE11-RAD50-NBS1 (MRN) complex acts in DNA double-strand break repair (DSBR), detection, and signaling; yet, how its endo- and exonuclease activities regulate DSBR by nonhomologous end-joining (NHEJ) versus homologous recombination (HR) remains enigmatic. Here, we employed structure-based design with a focused chemical library to discover specific MRE11 endo- or exonuclease inhibitors. With these inhibitors, we examined repair pathway choice at DSBs generated in G2 following radiation exposure. While nuclease inhibition impairs radiation-induced replication protein A (RPA) chromatin binding, suggesting diminished resection, the inhibitors surprisingly direct different repair outcomes. Endonuclease inhibition promotes NHEJ in lieu of HR, while exonuclease inhibition confers a repair defect. Collectively, the results describe nuclease-specific MRE11 inhibitors, define distinct nuclease roles in DSB repair, and support a mechanism whereby MRE11 endonuclease initiates resection, thereby licensing HR followed by MRE11 exonuclease and EXO1/BLM bidirectional resection toward and away from the DNA end, which commits to HR.

Publication types

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

MeSH terms

  • Cell Line
  • Chromatin / genetics
  • Chromatin / metabolism
  • DNA Breaks, Double-Stranded*
  • DNA End-Joining Repair*
  • DNA Repair Enzymes / genetics
  • DNA Repair Enzymes / metabolism
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Enzyme Inhibitors / chemistry*
  • Exodeoxyribonucleases / genetics
  • Exodeoxyribonucleases / metabolism
  • G2 Phase*
  • Gamma Rays / adverse effects
  • Humans
  • MRE11 Homologue Protein
  • Recombinational DNA Repair*
  • Replication Protein A / genetics
  • Replication Protein A / metabolism

Substances

  • Chromatin
  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • MRE11 protein, human
  • Replication Protein A
  • EXO1 protein, human
  • Exodeoxyribonucleases
  • MRE11 Homologue Protein
  • DNA Repair Enzymes

Associated data

  • PDB/4NZV
  • PDB/4O24
  • PDB/4O43
  • PDB/4O4K
  • PDB/4O5G
  • PDB/PFM01
  • PDB/PFM03
  • PDB/PFM39