IL-33 activates mTORC1 and modulates glycolytic metabolism in CD8+ T cells

Immunology. 2022 Jan;165(1):61-73. doi: 10.1111/imm.13404. Epub 2021 Aug 31.

Abstract

Interleukin (IL)-33, a member in the IL-1 family, plays a central role in innate and adaptive immunity; however, how IL-33 mediates cytotoxic T-cell regulation and the downstream signals remain elusive. In this study, we found increased mouse IL-33 expression in CD8+ T cells following cell activation via anti-CD3/CD28 stimulation in vitro or lymphocytic choriomeningitis virus (LCMV) infection in vivo. Our cell adoptive transfer experiment demonstrated that extracellular, but not nuclear, IL-33 contributed to the activation and proliferation of CD8+ , but not CD4+ T effector cells in LCMV infection. Importantly, IL-33 induced mTORC1 activation in CD8+ T cells as evidenced by increased phosphorylated S6 ribosomal protein (p-S6) levels both in vitro and in vivo. Meanwhile, this IL-33-induced CD8+ T-cell activation was suppressed by mTORC1 inhibitors. Furthermore, IL-33 elevated glucose uptake and lactate production in CD8+ T cells in both dose- and time-dependent manners. The results of glycolytic rate assay demonstrated the increased glycolytic capacity of IL-33-treated CD8+ T cells compared with that of control cells. Our mechanistic study further revealed the capacity of IL-33 in promoting the expression of glucose transporter 1 (Glut1) and glycolytic enzymes via mTORC1, leading to accelerated aerobic glucose metabolism Warburg effect and increased effector T-cell activation. Together, our data provide new insights into IL-33-mediated regulation of CD8+ T cells, which might be beneficial for therapeutic strategies of inflammatory and infectious diseases in the future.

Keywords: CD8; Glut1; IL-33; T cells; glycolytic metabolism; mTORC1.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism*
  • Disease Models, Animal
  • Disease Susceptibility
  • Energy Metabolism
  • Glucose / metabolism*
  • Glycolysis
  • Host-Pathogen Interactions / genetics
  • Host-Pathogen Interactions / immunology
  • Interleukin-33 / genetics
  • Interleukin-33 / metabolism*
  • Lactic Acid / biosynthesis
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology
  • Mechanistic Target of Rapamycin Complex 1 / metabolism*
  • Mice
  • Mice, Knockout
  • Signal Transduction

Substances

  • Interleukin-33
  • Lactic Acid
  • Mechanistic Target of Rapamycin Complex 1
  • Glucose