Immune suppression by human thymus-derived effector Tregs relies on glucose/lactate-fueled fatty acid synthesis

Cell Rep. 2024 Sep 24;43(9):114681. doi: 10.1016/j.celrep.2024.114681. Epub 2024 Aug 23.

Abstract

Regulatory T cells (Tregs) suppress pro-inflammatory conventional T cell (Tconv) responses. As lipids impact cell signaling and function, we compare the lipid composition of CD4+ thymus-derived (t)Tregs and Tconvs. Lipidomics reveal constitutive enrichment of neutral lipids in Tconvs and phospholipids in tTregs. TNFR2-co-stimulated effector tTregs and Tconvs are both glycolytic, but only in tTregs are glycolysis and the tricarboxylic acid (TCA) cycle linked to a boost in fatty acid (FA) synthesis (FAS), supported by relevant gene expression. FA chains in tTregs are longer and more unsaturated than in Tconvs. In contrast to Tconvs, tTregs effectively use either lactate or glucose for FAS and rely on this process for proliferation. FASN and SCD1, enzymes responsible for FAS and FA desaturation, prove essential for the ability of tTregs to suppress Tconvs. These data illuminate how effector tTregs can thrive in inflamed or cancerous tissues with limiting glucose but abundant lactate levels.

Keywords: (regulatory) T cell; CP: Immunology; CP: Metabolism; costimulation; fatty acids; glycolysis; immune suppression; isotopologue tracing; lactate; lipidomics; mass spectrometry; metabolism.

MeSH terms

  • Citric Acid Cycle
  • Fatty Acid Synthase, Type I / metabolism
  • Fatty Acids* / metabolism
  • Glucose* / metabolism
  • Glycolysis
  • Humans
  • Lactic Acid* / biosynthesis
  • Lactic Acid* / metabolism
  • Receptors, Tumor Necrosis Factor, Type II / metabolism
  • Stearoyl-CoA Desaturase* / metabolism
  • T-Lymphocytes, Regulatory* / immunology
  • T-Lymphocytes, Regulatory* / metabolism
  • Thymus Gland / immunology
  • Thymus Gland / metabolism

Substances

  • Glucose
  • Fatty Acids
  • Lactic Acid
  • Stearoyl-CoA Desaturase
  • SCD1 protein, human
  • Fatty Acid Synthase, Type I
  • FASN protein, human
  • Receptors, Tumor Necrosis Factor, Type II