A Polar and Nucleotide-Dependent Mechanism of Action for RAD51 Paralogs in RAD51 Filament Remodeling

Mol Cell. 2016 Dec 1;64(5):926-939. doi: 10.1016/j.molcel.2016.10.020. Epub 2016 Nov 17.

Abstract

Central to homologous recombination in eukaryotes is the RAD51 recombinase, which forms helical nucleoprotein filaments on single-stranded DNA (ssDNA) and catalyzes strand invasion with homologous duplex DNA. Various regulatory proteins assist this reaction including the RAD51 paralogs. We recently discovered that a RAD51 paralog complex from C. elegans, RFS-1/RIP-1, functions predominantly downstream of filament assembly by binding and remodeling RAD-51-ssDNA filaments to a conformation more proficient for strand exchange. Here, we demonstrate that RFS-1/RIP-1 acts by shutting down RAD-51 dissociation from ssDNA. Using stopped-flow experiments, we show that RFS-1/RIP-1 confers this dramatic stabilization by capping the 5' end of RAD-51-ssDNA filaments. Filament end capping propagates a stabilizing effect with a 5'→3' polarity approximately 40 nucleotides along individual filaments. Finally, we discover that filament capping and stabilization are dependent on nucleotide binding, but not hydrolysis by RFS-1/RIP-1. These data define the mechanism of RAD51 filament remodeling by RAD51 paralogs.

Keywords: DNA repair; Rad51; Rad51 paralogs; filaments; genome stability; homologous recombination.

Publication types

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

MeSH terms

  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • DNA, Single-Stranded / genetics
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism*
  • Intermediate Filaments / genetics
  • Intermediate Filaments / metabolism*
  • Multiprotein Complexes / metabolism
  • Protein Binding
  • Rad51 Recombinase / genetics
  • Rad51 Recombinase / metabolism*
  • Recombinational DNA Repair

Substances

  • Caenorhabditis elegans Proteins
  • Carrier Proteins
  • DNA, Single-Stranded
  • DNA-Binding Proteins
  • Multiprotein Complexes
  • RFS-1 protein, C elegans
  • RIP-1 protein, C elegans
  • Rad51 Recombinase
  • rad-51 protein, C elegans