LRET-derived HADDOCK structural models describe the conformational heterogeneity required for DNA cleavage by the Mre11-Rad50 DNA damage repair complex

Elife. 2022 Jan 27:11:e69579. doi: 10.7554/eLife.69579.

Abstract

The Mre11-Rad50-Nbs1 protein complex is one of the first responders to DNA double-strand breaks. Studies have shown that the catalytic activities of the evolutionarily conserved Mre11-Rad50 (MR) core complex depend on an ATP-dependent global conformational change that takes the macromolecule from an open, extended structure in the absence of ATP to a closed, globular structure when ATP is bound. We have previously identified an additional 'partially open' conformation using luminescence resonance energy transfer (LRET) experiments. Here, a combination of LRET and the molecular docking program HADDOCK was used to further investigate this partially open state and identify three conformations of MR in solution: closed, partially open, and open, which are in addition to the extended, apo conformation. Mutants disrupting specific Mre11-Rad50 interactions within each conformation were used in nuclease activity assays on a variety of DNA substrates to help put the three states into a functional perspective. LRET data collected on MR bound to DNA demonstrate that the three conformations also exist when nuclease substrates are bound. These models were further supported with small-angle X-ray scattering data, which corroborate the presence of multiple states in solution. Together, the data suggest a mechanism for the nuclease activity of the MR complex along the DNA.

Keywords: DNA damage repair; DNA double-strand break repair; Mre11-Rad50; P. furiosus; biochemistry; chemical biology; lanthanide resonance energy transfer; molecular biophysics; structural biology.

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

  • DNA / metabolism
  • DNA Breaks, Double-Stranded
  • DNA Cleavage*
  • DNA Repair*
  • DNA-Binding Proteins / metabolism
  • Luminescent Measurements
  • Molecular Docking Simulation
  • Protein Conformation
  • Pyrococcus furiosus / chemistry
  • Thermotoga maritima / chemistry

Substances

  • DNA-Binding Proteins
  • DNA

Associated data

  • Dryad/10.5061/dryad.qfttdz0h6