Citrate metabolism controls the senescent microenvironment via the remodeling of pro-inflammatory enhancers

Cell Rep. 2024 Aug 27;43(8):114496. doi: 10.1016/j.celrep.2024.114496. Epub 2024 Jul 22.

Abstract

The senescent microenvironment and aged cells per se contribute to tissue remodeling, chronic inflammation, and age-associated dysfunction. However, the metabolic and epigenomic bases of the senescence-associated secretory phenotype (SASP) remain largely unknown. Here, we show that ATP-citrate lyase (ACLY), a key enzyme in acetyl-coenzyme A (CoA) synthesis, is essential for the pro-inflammatory SASP, independent of persistent growth arrest in senescent cells. Citrate-derived acetyl-CoA facilitates the action of SASP gene enhancers. ACLY-dependent de novo enhancers augment the recruitment of the chromatin reader BRD4, which causes SASP activation. Consistently, specific inhibitions of the ACLY-BRD4 axis suppress the STAT1-mediated interferon response, creating the pro-inflammatory microenvironment in senescent cells and tissues. Our results demonstrate that ACLY-dependent citrate metabolism represents a selective target for controlling SASP designed to promote healthy aging.

Keywords: ACLY; CP: Cell biology; CP: Metabolism; H3K27 acetylation; SASP; acetyl-CoA; citrate metabolism; senescence; senostatics.

MeSH terms

  • ATP Citrate (pro-S)-Lyase* / genetics
  • ATP Citrate (pro-S)-Lyase* / metabolism
  • Acetyl Coenzyme A / metabolism
  • Animals
  • Cellular Microenvironment
  • Cellular Senescence*
  • Citric Acid* / metabolism
  • Enhancer Elements, Genetic / genetics
  • Humans
  • Inflammation / metabolism
  • Inflammation / pathology
  • Mice
  • Mice, Inbred C57BL
  • Nuclear Proteins / metabolism
  • Transcription Factors* / metabolism

Substances

  • ATP Citrate (pro-S)-Lyase
  • Citric Acid
  • Transcription Factors
  • Acetyl Coenzyme A
  • Nuclear Proteins