LINC complexes promote homologous recombination in part through inhibition of nonhomologous end joining

J Cell Biol. 2016 Dec 19;215(6):801-821. doi: 10.1083/jcb.201604112. Epub 2016 Dec 12.

Abstract

The Caenorhabditis elegans SUN domain protein, UNC-84, functions in nuclear migration and anchorage in the soma. We discovered a novel role for UNC-84 in DNA damage repair and meiotic recombination. Loss of UNC-84 leads to defects in the loading and disassembly of the recombinase RAD-51. Similar to mutations in Fanconi anemia (FA) genes, unc-84 mutants and human cells depleted of Sun-1 are sensitive to DNA cross-linking agents, and sensitivity is rescued by the inactivation of nonhomologous end joining (NHEJ). UNC-84 also recruits FA nuclease FAN-1 to the nucleoplasm, suggesting that UNC-84 both alters the extent of repair by NHEJ and promotes the processing of cross-links by FAN-1. UNC-84 interacts with the KASH protein ZYG-12 for DNA damage repair. Furthermore, the microtubule network and interaction with the nucleoskeleton are important for repair, suggesting that a functional linker of nucleoskeleton and cytoskeleton (LINC) complex is required. We propose that LINC complexes serve a conserved role in DNA repair through both the inhibition of NHEJ and the promotion of homologous recombination at sites of chromosomal breaks.

MeSH terms

  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Cycle Checkpoints / drug effects
  • Cell Cycle Checkpoints / radiation effects
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cell Nucleus / radiation effects
  • Cell Proliferation / drug effects
  • Cell Proliferation / radiation effects
  • Cisplatin / pharmacology
  • Cross-Linking Reagents / metabolism
  • DNA Damage
  • DNA End-Joining Repair* / drug effects
  • DNA End-Joining Repair* / radiation effects
  • Germ Cells / cytology
  • Germ Cells / drug effects
  • Germ Cells / metabolism
  • Germ Cells / radiation effects
  • Homologous Recombination* / drug effects
  • Homologous Recombination* / radiation effects
  • Humans
  • Hydroxyurea / pharmacology
  • Meiosis / drug effects
  • Meiosis / radiation effects
  • Membrane Proteins / metabolism
  • Microtubule-Associated Proteins / metabolism
  • Microtubules / drug effects
  • Microtubules / metabolism
  • Microtubules / radiation effects
  • Models, Biological
  • Multiprotein Complexes / metabolism*
  • Nuclear Proteins / metabolism
  • Polymerization / drug effects
  • Protein Binding / drug effects
  • Protein Binding / radiation effects
  • Protein Transport / drug effects
  • Protein Transport / radiation effects
  • Radiation, Ionizing

Substances

  • Caenorhabditis elegans Proteins
  • Cross-Linking Reagents
  • Membrane Proteins
  • Microtubule-Associated Proteins
  • Multiprotein Complexes
  • Nuclear Proteins
  • SUN1 protein, human
  • Cisplatin
  • Hydroxyurea