GPX4 restricts ferroptosis of NKp46+ILC3s to control intestinal inflammation

Cell Death Dis. 2024 Sep 19;15(9):687. doi: 10.1038/s41419-024-07060-3.

Abstract

Group 3 innate lymphoid cells (ILC3s) are essential for both pathogen defense and tissue homeostasis in the intestine. Dysfunction of ILC3s could lead to increased susceptibility to intestinal inflammation. However, the precise mechanisms governing the maintenance of intestinal ILC3s are yet to be fully elucidated. Here, we demonstrated that ferroptosis is vital for regulating the survival of intestinal ILC3. Ferroptosis-related genes, including GPX4, a key regulator of ferroptosis, were found to be upregulated in intestinal mucosal ILC3s from ulcerative colitis patients. Deletion of GPX4 resulted in a decrease in NKp46+ILC3 cell numbers, impaired production of IL-22 and IL-17A, and exacerbated intestinal inflammation in a T cell-independent manner. Our mechanistic studies revealed that GPX4-mediated ferroptosis in NKp46+ILC3 cells was regulated by the LCN2-p38-ATF4-xCT signaling pathway. Mice lacking LCN2 in ILC3s or administration of a p38 pathway inhibitor exhibited similar phenotypes of ILC3 and colitis to those observed in GPX4 conditional knock-out mice. These observations provide novel insights into therapeutic strategies for intestinal inflammation by modulating ILC3 ferroptosis.

MeSH terms

  • Animals
  • Antigens, Ly / metabolism
  • Colitis, Ulcerative / genetics
  • Colitis, Ulcerative / metabolism
  • Colitis, Ulcerative / pathology
  • Female
  • Ferroptosis* / genetics
  • Humans
  • Immunity, Innate
  • Inflammation* / metabolism
  • Inflammation* / pathology
  • Interleukin-22
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / pathology
  • Intestines / pathology
  • Lymphocytes / immunology
  • Lymphocytes / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Natural Cytotoxicity Triggering Receptor 1* / genetics
  • Natural Cytotoxicity Triggering Receptor 1* / metabolism
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / genetics
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / metabolism
  • Signal Transduction

Substances

  • Antigens, Ly
  • glutathione peroxidase 4, mouse
  • Interleukin-22
  • Natural Cytotoxicity Triggering Receptor 1
  • NCR1 protein, human
  • Ncr1 protein, mouse
  • Phospholipid Hydroperoxide Glutathione Peroxidase