SMCHD1 promotes ATM-dependent DNA damage signaling and repair of uncapped telomeres

EMBO J. 2020 Apr 1;39(7):e102668. doi: 10.15252/embj.2019102668. Epub 2020 Feb 21.

Abstract

Structural maintenance of chromosomes flexible hinge domain-containing protein 1 (SMCHD1) has been implicated in X-chromosome inactivation, imprinting, and DNA damage repair, and mutations in SMCHD1 can cause facioscapulohumeral muscular dystrophy. More recently, SMCHD1 has also been identified as a component of telomeric chromatin. Here, we report that SMCHD1 is required for DNA damage signaling and non-homologous end joining (NHEJ) at unprotected telomeres. Co-depletion of SMCHD1 and the shelterin subunit TRF2 reduced telomeric 3'-overhang removal in time-course experiments, as well as the number of chromosome end fusions. SMCHD1-deficient cells displayed reduced ATM S1981 phosphorylation and diminished formation of γH2AX foci and of 53BP1-containing telomere dysfunction-induced foci (TIFs), indicating defects in DNA damage checkpoint signaling. Removal of TPP1 and subsequent activation of ATR signaling rescued telomere fusion events in TRF2-depleted SMCHD1 knockout cells. Together, these data indicate that SMCHD1 depletion reduces telomere fusions in TRF2-depleted cells due to defects in ATM-dependent checkpoint signaling and that SMCHD1 mediates DNA damage response activation upstream of ATM phosphorylation at uncapped telomeres.

Keywords: ATM; DNA damage response; SMCHD1; non-homologous end joining; telomeres.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ataxia Telangiectasia Mutated Proteins / metabolism*
  • Chromosomal Proteins, Non-Histone / genetics*
  • Chromosomal Proteins, Non-Histone / metabolism*
  • DNA Damage
  • DNA End-Joining Repair
  • Epistasis, Genetic
  • Gene Knockout Techniques
  • HeLa Cells
  • Humans
  • Phosphorylation
  • Shelterin Complex / genetics
  • Shelterin Complex / metabolism
  • Signal Transduction
  • Telomere / metabolism*
  • Telomere-Binding Proteins / genetics
  • Telomere-Binding Proteins / metabolism
  • Telomeric Repeat Binding Protein 2 / genetics*
  • Tumor Suppressor p53-Binding Protein 1 / metabolism

Substances

  • ACD protein, human
  • Chromosomal Proteins, Non-Histone
  • SMCHD1 protein, human
  • Shelterin Complex
  • TERF2 protein, human
  • TP53BP1 protein, human
  • Telomere-Binding Proteins
  • Telomeric Repeat Binding Protein 2
  • Tumor Suppressor p53-Binding Protein 1
  • ATM protein, human
  • Ataxia Telangiectasia Mutated Proteins