ACLY and ACSS2 link nutrient-dependent chromatin accessibility to CD8 T cell effector responses

J Exp Med. 2024 Sep 2;221(9):e20231820. doi: 10.1084/jem.20231820. Epub 2024 Aug 16.

Abstract

Coordination of cellular metabolism is essential for optimal T cell responses. Here, we identify cytosolic acetyl-CoA production as an essential metabolic node for CD8 T cell function in vivo. We show that CD8 T cell responses to infection depend on acetyl-CoA derived from citrate via the enzyme ATP citrate lyase (ACLY). However, ablation of ACLY triggers an alternative, acetate-dependent pathway for acetyl-CoA production mediated by acyl-CoA synthetase short-chain family member 2 (ACSS2). Mechanistically, acetate fuels both the TCA cycle and cytosolic acetyl-CoA production, impacting T cell effector responses, acetate-dependent histone acetylation, and chromatin accessibility at effector gene loci. When ACLY is functional, ACSS2 is not required, suggesting acetate is not an obligate metabolic substrate for CD8 T cell function. However, loss of ACLY renders CD8 T cells dependent on acetate (via ACSS2) to maintain acetyl-CoA production and effector function. Together, ACLY and ACSS2 coordinate cytosolic acetyl-CoA production in CD8 T cells to maintain chromatin accessibility and T cell effector function.

MeSH terms

  • ATP Citrate (pro-S)-Lyase* / genetics
  • ATP Citrate (pro-S)-Lyase* / metabolism
  • Acetate-CoA Ligase / genetics
  • Acetate-CoA Ligase / metabolism
  • Acetates* / metabolism
  • Acetyl Coenzyme A* / metabolism
  • Acetylation
  • Animals
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • Chromatin* / metabolism
  • Cytosol / metabolism
  • Histones / metabolism
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Knockout

Substances

  • Chromatin
  • Acetyl Coenzyme A
  • ATP Citrate (pro-S)-Lyase
  • Acetates
  • ACSS2 protein, mouse
  • Acetate-CoA Ligase
  • Histones