Nuclear Acetyl-CoA Production by ACLY Promotes Homologous Recombination

Mol Cell. 2017 Jul 20;67(2):252-265.e6. doi: 10.1016/j.molcel.2017.06.008. Epub 2017 Jul 6.

Abstract

While maintaining the integrity of the genome and sustaining bioenergetics are both fundamental functions of the cell, potential crosstalk between metabolic and DNA repair pathways is poorly understood. Since histone acetylation plays important roles in DNA repair and is sensitive to the availability of acetyl coenzyme A (acetyl-CoA), we investigated a role for metabolic regulation of histone acetylation during the DNA damage response. In this study, we report that nuclear ATP-citrate lyase (ACLY) is phosphorylated at S455 downstream of ataxia telangiectasia mutated (ATM) and AKT following DNA damage. ACLY facilitates histone acetylation at double-strand break (DSB) sites, impairing 53BP1 localization and enabling BRCA1 recruitment and DNA repair by homologous recombination. ACLY phosphorylation and nuclear localization are necessary for its role in promoting BRCA1 recruitment. Upon PARP inhibition, ACLY silencing promotes genomic instability and cell death. Thus, the spatial and temporal control of acetyl-CoA production by ACLY participates in the mechanism of DNA repair pathway choice.

Keywords: ATP-citrate lyase; DNA damage; DNA repair; acetyl-CoA; histone acetylation; homologous recombination; metabolism; non-homologous end joining; nucleus.

MeSH terms

  • A549 Cells
  • ATP Citrate (pro-S)-Lyase / genetics
  • ATP Citrate (pro-S)-Lyase / metabolism*
  • Acetyl Coenzyme A / metabolism*
  • Acetylation
  • Animals
  • BRCA1 Protein / genetics
  • BRCA1 Protein / metabolism*
  • Cell Nucleus / drug effects
  • Cell Nucleus / enzymology*
  • DNA Breaks, Double-Stranded*
  • Female
  • G2 Phase Cell Cycle Checkpoints
  • Genomic Instability
  • Glucose / metabolism
  • HCT116 Cells
  • HeLa Cells
  • Histones / metabolism
  • Humans
  • Melanoma, Experimental / enzymology
  • Melanoma, Experimental / genetics
  • Melanoma, Experimental / pathology
  • Mice, Inbred C57BL
  • Phosphorylation
  • Poly(ADP-ribose) Polymerase Inhibitors / pharmacology
  • Protein Binding
  • Protein Processing, Post-Translational
  • RNA Interference
  • Recombinational DNA Repair* / drug effects
  • S Phase Cell Cycle Checkpoints
  • Serine
  • Time Factors
  • Transfection
  • Tumor Suppressor p53-Binding Protein 1 / metabolism

Substances

  • BRCA1 Protein
  • BRCA1 protein, human
  • Histones
  • Poly(ADP-ribose) Polymerase Inhibitors
  • TP53BP1 protein, human
  • Tumor Suppressor p53-Binding Protein 1
  • Serine
  • Acetyl Coenzyme A
  • ATP Citrate (pro-S)-Lyase
  • Glucose