IL-6-induced FOXO1 activity determines the dynamics of metabolism in CD8 T cells cross-primed by liver sinusoidal endothelial cells

Cell Rep. 2022 Feb 15;38(7):110389. doi: 10.1016/j.celrep.2022.110389.

Abstract

Liver sinusoidal endothelial cells (LSECs) are liver-resident antigen (cross)-presenting cells that generate memory CD8 T cells, but metabolic properties of LSECs and LSEC-primed CD8 T cells remain understudied. Here, we report that high-level mitochondrial respiration and constitutive low-level glycolysis support LSEC scavenger and sentinel functions. LSECs fail to increase glycolysis and co-stimulation after TLR4 activation, indicating absence of metabolic and functional maturation compared with immunogenic dendritic cells. LSEC-primed CD8 T cells show a transient burst of oxidative phosphorylation and glycolysis. Mechanistically, co-stimulatory IL-6 signaling ensures high FOXO1 expression in LSEC-primed CD8 T cells, curtails metabolic activity associated with T cell activation, and is indispensable for T cell functionality after re-activation. Thus, distinct immunometabolic features characterize non-immunogenic LSECs compared with immunogenic dendritic cells and LSEC-primed CD8 T cells with memory features compared with effector CD8 T cells. This reveals local features of metabolism and function of T cells in the liver.

Keywords: glycolysis; immune cell metabolism; liver immune tolerance; memory T cells; mitochondrial respiration; non-professional antigen-presenting cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / metabolism*
  • Cell Differentiation / genetics
  • Cell Respiration
  • Cross-Priming / immunology*
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism*
  • Endothelial Cells / ultrastructure
  • Forkhead Box Protein O1 / metabolism*
  • Glycolysis
  • Interleukin-6 / metabolism*
  • Liver / cytology*
  • Male
  • Metabolomics
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / metabolism
  • Oxidative Phosphorylation
  • Signal Transduction
  • Toll-Like Receptor 4 / metabolism
  • Transcription, Genetic

Substances

  • Forkhead Box Protein O1
  • Foxo1 protein, mouse
  • Interleukin-6
  • Toll-Like Receptor 4