Tonic type 2 immunity is a critical tissue checkpoint controlling autoimmunity in the skin

Cell Rep. 2024 Jul 23;43(7):114364. doi: 10.1016/j.celrep.2024.114364. Epub 2024 Jun 18.

Abstract

Immunoregulatory mechanisms established in the lymphoid organs are vital for preventing autoimmunity. However, the presence of similar mechanisms in non-lymphoid tissues remains unclear. Through transcriptomic and lipidomic analyses, we find a negative association between psoriasis and fatty acid metabolism, as well as Th2 signature. Homeostatic expression of liver X receptor (LXR) and peroxisome proliferator-activated receptor gamma (PPARγ) is essential for maintaining fatty acid metabolism and for conferring resistance to psoriasis in mice. Perturbation of signal transducer and activator of transcription 6 (STAT6) diminishes the homeostatic levels of LXR and PPARγ. Furthermore, mice lacking STAT6, interleukin 4 receptor alpha (IL-4Rα), or IL-13, but not IL-4, exhibit increased susceptibility to psoriasis. Under steady state, innate lymphoid cells (ILCs) are the primary producers of IL-13. In human skin, inhibiting tonic type 2 immunity exacerbates psoriasis-like inflammation and IL-17A, while activating LXR or PPARγ inhibits them. Hence, we propose that tonic type 2 immunity, driven by IL-13-producing ILCs, represents a crucial tissue checkpoint that represses autoimmunity and maintains lipid homeostasis in the skin.

Keywords: CP: Immunology; LXR; PPARγ; fatty acid metabolism; psoriasis; tonic type 2 immunity.

MeSH terms

  • Animals
  • Autoimmunity*
  • Female
  • Humans
  • Immunity, Innate
  • Interleukin-13 / metabolism
  • Liver X Receptors* / metabolism
  • Lymphocytes / immunology
  • Lymphocytes / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • PPAR gamma* / metabolism
  • Psoriasis / immunology
  • Psoriasis / metabolism
  • Psoriasis / pathology
  • STAT6 Transcription Factor / metabolism
  • Skin* / immunology
  • Skin* / metabolism
  • Skin* / pathology

Substances

  • Liver X Receptors
  • PPAR gamma
  • Interleukin-13
  • STAT6 Transcription Factor