Nuclear ATP-citrate lyase regulates chromatin-dependent activation and maintenance of the myofibroblast gene program

Nat Cardiovasc Res. 2024 Jul;3(7):869-882. doi: 10.1038/s44161-024-00502-3. Epub 2024 Jul 5.

Abstract

Differentiation of cardiac fibroblasts to myofibroblasts is necessary for matrix remodeling and fibrosis in heart failure. We previously reported that mitochondrial calcium signaling drives α-ketoglutarate-dependent histone demethylation, promoting myofibroblast formation. Here we investigate the role of ATP-citrate lyase (ACLY), a key enzyme for acetyl-CoA biosynthesis, in histone acetylation regulating myofibroblast fate and persistence in cardiac fibrosis. We show that inactivation of ACLY prevents myofibroblast differentiation and reverses myofibroblasts towards quiescence. Genetic deletion of Acly in post-activated myofibroblasts prevents fibrosis and preserves cardiac function in pressure-overload heart failure. TGFβ stimulation enhances ACLY nuclear localization and ACLY-SMAD2/3 interaction, and increases H3K27ac at fibrotic gene loci. Pharmacological inhibition of ACLY or forced nuclear expression of a dominant-negative ACLY mutant prevents myofibroblast formation and H3K27ac. Our data indicate that nuclear ACLY activity is necessary for myofibroblast differentiation and persistence by maintaining histone acetylation at TGFβ-induced myofibroblast genes. These findings provide targets to prevent and reverse pathological fibrosis.

MeSH terms

  • ATP Citrate (pro-S)-Lyase* / genetics
  • ATP Citrate (pro-S)-Lyase* / metabolism
  • Acetylation / drug effects
  • Animals
  • Cell Differentiation* / drug effects
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cells, Cultured
  • Chromatin / metabolism
  • Disease Models, Animal
  • Fibrosis* / metabolism
  • Gene Expression Regulation / drug effects
  • Histones* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myofibroblasts* / drug effects
  • Myofibroblasts* / metabolism
  • Signal Transduction
  • Smad2 Protein* / genetics
  • Smad2 Protein* / metabolism
  • Smad3 Protein / genetics
  • Smad3 Protein / metabolism
  • Transforming Growth Factor beta / metabolism

Substances

  • ATP Citrate (pro-S)-Lyase
  • Histones
  • Smad2 Protein
  • Smad3 Protein
  • Smad2 protein, mouse
  • Smad3 protein, mouse
  • Chromatin
  • Transforming Growth Factor beta