UBQLN4 Represses Homologous Recombination and Is Overexpressed in Aggressive Tumors

Cell. 2019 Jan 24;176(3):505-519.e22. doi: 10.1016/j.cell.2018.11.024. Epub 2019 Jan 3.

Abstract

Genomic instability can be a hallmark of both human genetic disease and cancer. We identify a deleterious UBQLN4 mutation in families with an autosomal recessive syndrome reminiscent of genome instability disorders. UBQLN4 deficiency leads to increased sensitivity to genotoxic stress and delayed DNA double-strand break (DSB) repair. The proteasomal shuttle factor UBQLN4 is phosphorylated by ATM and interacts with ubiquitylated MRE11 to mediate early steps of homologous recombination-mediated DSB repair (HRR). Loss of UBQLN4 leads to chromatin retention of MRE11, promoting non-physiological HRR activity in vitro and in vivo. Conversely, UBQLN4 overexpression represses HRR and favors non-homologous end joining. Moreover, we find UBQLN4 overexpressed in aggressive tumors. In line with an HRR defect in these tumors, UBQLN4 overexpression is associated with PARP1 inhibitor sensitivity. UBQLN4 therefore curtails HRR activity through removal of MRE11 from damaged chromatin and thus offers a therapeutic window for PARP1 inhibitor treatment in UBQLN4-overexpressing tumors.

Keywords: DNA damage; DNA double-strand break repair; UBQLN4 deficiency syndrome; cancer; genome instability syndrome; homologous recombination; non-homologous end joining; proteasomal degradation; targeted cancer therapy; ubiquitin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Carrier Proteins / genetics*
  • Carrier Proteins / metabolism
  • Chromatin / metabolism
  • DNA
  • DNA Breaks, Double-Stranded
  • DNA Damage / genetics
  • DNA End-Joining Repair
  • DNA-Binding Proteins / metabolism
  • Female
  • Genomic Instability
  • Germ-Line Mutation
  • Homologous Recombination
  • Humans
  • MRE11 Homologue Protein / genetics
  • MRE11 Homologue Protein / metabolism
  • Male
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Primary Cell Culture
  • Recombinational DNA Repair

Substances

  • Carrier Proteins
  • Chromatin
  • DNA-Binding Proteins
  • MRE11 protein, human
  • Nuclear Proteins
  • UBQLN4 protein, human
  • DNA
  • MRE11 Homologue Protein