The malate shuttle detoxifies ammonia in exhausted T cells by producing 2-ketoglutarate

Nat Immunol. 2023 Nov;24(11):1921-1932. doi: 10.1038/s41590-023-01636-5. Epub 2023 Oct 9.

Abstract

The malate shuttle is traditionally understood to maintain NAD+/NADH balance between the cytosol and mitochondria. Whether the malate shuttle has additional functions is unclear. Here we show that chronic viral infections induce CD8+ T cell expression of GOT1, a central enzyme in the malate shuttle. Got1 deficiency decreased the NAD+/NADH ratio and limited antiviral CD8+ T cell responses to chronic infection; however, increasing the NAD+/NADH ratio did not restore T cell responses. Got1 deficiency reduced the production of the ammonia scavenger 2-ketoglutarate (2-KG) from glutaminolysis and led to a toxic accumulation of ammonia in CD8+ T cells. Supplementation with 2-KG assimilated and detoxified ammonia in Got1-deficient T cells and restored antiviral responses. These data indicate that the major function of the malate shuttle in CD8+ T cells is not to maintain the NAD+/NADH balance but rather to detoxify ammonia and enable sustainable ammonia-neutral glutamine catabolism in CD8+ T cells during chronic infection.

MeSH terms

  • Ammonia
  • Antiviral Agents
  • CD8-Positive T-Lymphocytes / metabolism
  • Humans
  • Ketoglutaric Acids* / metabolism
  • Malates / metabolism
  • NAD* / metabolism
  • Oxidation-Reduction
  • Persistent Infection

Substances

  • NAD
  • Ketoglutaric Acids
  • Ammonia
  • malic acid
  • Malates
  • Antiviral Agents