MCL-1 Depletion Impairs DNA Double-Strand Break Repair and Reinitiation of Stalled DNA Replication Forks

Mol Cell Biol. 2017 Jan 19;37(3):e00535-16. doi: 10.1128/MCB.00535-16. Print 2017 Feb 1.

Abstract

Myeloid cell leukemia 1 (MCL-1) is a prosurvival BCL-2 protein family member highly expressed in hematopoietic stem cells (HSCs) and regulated by growth factor signals that manifest antiapoptotic activity. Here we report that depletion of MCL-1 but not its isoform MCL-1S increases genomic instability and cell sensitivity to ionizing radiation (IR)-induced death. MCL-1 association with genomic DNA increased postirradiation, and the protein colocalized with 53BP1 foci. Postirradiation, MCL-1-depleted cells exhibited decreased γ-H2AX foci, decreased phosphorylation of ATR, and higher levels of residual 53BP1 and RIF1 foci, suggesting that DNA double-strand break (DSB) repair by homologous recombination (HR) was compromised. Consistent with this model, MCL-1-depleted cells had a reduced frequency of IR-induced BRCA1, RPA, and Rad51 focus formation, decreased DNA end resection, and decreased HR repair in the DR-GFP DSB repair model. Similarly, after HU induction of stalled replication forks in MCL-1-depleted cells, there was a decreased ability to subsequently restart DNA synthesis, which is normally dependent upon HR-mediated resolution of collapsed forks. Therefore, the present data support a model whereby MCL-1 depletion increases 53BP1 and RIF1 colocalization at DSBs, which inhibits BRCA1 recruitment, and sensitizes cells to DSBs from IR or stalled replication forks that require HR for repair.

Keywords: 53BP1; BCL-2; DSB repair; HR; ICL; MCL-1; apoptosis.

Publication types

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

MeSH terms

  • Cell Nucleus / metabolism
  • Cell Nucleus / radiation effects
  • Cell Survival / radiation effects
  • Chromatin / metabolism
  • Chromosome Aberrations
  • DNA Breaks, Double-Stranded* / radiation effects
  • DNA Repair / radiation effects
  • DNA Replication* / radiation effects
  • Genomic Instability / radiation effects
  • Homologous Recombination / radiation effects
  • Humans
  • Models, Biological
  • Myeloid Cell Leukemia Sequence 1 Protein / metabolism*
  • Radiation, Ionizing
  • Stress, Physiological / radiation effects
  • Tumor Suppressor p53-Binding Protein 1 / metabolism

Substances

  • Chromatin
  • MCL1 protein, human
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Tumor Suppressor p53-Binding Protein 1