Rhythmic IL-17 production by γδ T cells maintains adipose de novo lipogenesis

Nature. 2024 Dec;636(8041):206-214. doi: 10.1038/s41586-024-08131-3. Epub 2024 Oct 30.

Abstract

The circadian rhythm of the immune system helps to protect against pathogens1-3; however, the role of circadian rhythms in immune homeostasis is less well understood. Innate T cells are tissue-resident lymphocytes with key roles in tissue homeostasis4-7. Here we use single-cell RNA sequencing, a molecular-clock reporter and genetic manipulations to show that innate IL-17-producing T cells-including γδ T cells, invariant natural killer T cells and mucosal-associated invariant T cells-are enriched for molecular-clock genes compared with their IFNγ-producing counterparts. We reveal that IL-17-producing γδ (γδ17) T cells, in particular, rely on the molecular clock to maintain adipose tissue homeostasis, and exhibit a robust circadian rhythm for RORγt and IL-17A across adipose depots, which peaks at night. In mice, loss of the molecular clock in the CD45 compartment (Bmal1∆Vav1) affects the production of IL-17 by adipose γδ17 T cells, but not cytokine production by αβ or IFNγ-producing γδ (γδIFNγ) T cells. Circadian IL-17 is essential for de novo lipogenesis in adipose tissue, and mice with an adipocyte-specific deficiency in IL-17 receptor C (IL-17RC) have defects in de novo lipogenesis. Whole-body metabolic analysis in vivo shows that Il17a-/-Il17f-/- mice (which lack expression of IL-17A and IL-17F) have defects in their circadian rhythm for de novo lipogenesis, which results in disruptions to their whole-body metabolic rhythm and core-body-temperature rhythm. This study identifies a crucial role for IL-17 in whole-body metabolic homeostasis and shows that de novo lipogenesis is a major target of IL-17.

MeSH terms

  • ARNTL Transcription Factors / genetics
  • ARNTL Transcription Factors / metabolism
  • Adipose Tissue* / immunology
  • Adipose Tissue* / metabolism
  • Animals
  • Biological Clocks / genetics
  • Biological Clocks / immunology
  • Body Temperature
  • Circadian Rhythm* / genetics
  • Circadian Rhythm* / immunology
  • Homeostasis*
  • Interferon-gamma / metabolism
  • Interleukin-17* / genetics
  • Interleukin-17* / immunology
  • Interleukin-17* / metabolism
  • Leukocyte Common Antigens / metabolism
  • Lipogenesis*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / genetics
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / metabolism
  • Receptors, Antigen, T-Cell, gamma-delta* / metabolism
  • Receptors, Interleukin-17 / deficiency
  • Receptors, Interleukin-17 / metabolism
  • Single-Cell Gene Expression Analysis

Substances

  • Interferon-gamma
  • Interleukin-17
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • Receptors, Antigen, T-Cell, gamma-delta
  • Rorc protein, mouse
  • Il17a protein, mouse
  • Ptprc protein, mouse
  • Bmal1 protein, mouse
  • Receptors, Interleukin-17
  • Leukocyte Common Antigens
  • ARNTL Transcription Factors