Defective autophagy in CD4 T cells drives liver fibrosis via type 3 inflammation

Nat Commun. 2025 Apr 24;16(1):3860. doi: 10.1038/s41467-025-59218-y.

Abstract

Conventional CD4 T cells represent a major source of inflammatory mediators that drive progression of chronic liver disease to fibrosis and to end-stage cirrhosis. Identification of T cell pathways that limits the inflammatory response could thus have therapeutic relevance. Here we show, using both human samples and mouse models, that autophagy is deficient in CD4 T cells from patients with advanced fibrosis, and that loss of autophagy following genomic deletion of ATG5 in T cells is associated with the emergence of pathogenic IL-17A + IFN-γ + Th17 T cells that drive liver fibrosis in mice. Mechanistically, liver CD4 T cells lacking autophagy display a Th17 glycolytic phenotype associated with enhanced type 3 cytokine (i.e., IL-17A and GM-CSF) release, shifting hepatic myofibroblasts, hepatocytes and macrophages toward a proinflammatory phenotype. We also show that autophagy can be rescued in CD4 T cells from patients with extensive liver fibrosis, leading to decreased frequency of pathogenic Th17 cells and reduced GM-CSF levels; in addition, limited fibrosis is observed in mice in which Rubicon, a negative regulator of autophagy, is deleted specifically in their T cells. Our findings thus implicate autophagy in CD4 T cells as a key therapeutic target to control inflammation-driven fibrosis during chronic liver injury.

MeSH terms

  • Animals
  • Autophagy* / genetics
  • Autophagy* / immunology
  • Autophagy-Related Protein 5 / genetics
  • Autophagy-Related Protein 5 / metabolism
  • CD4-Positive T-Lymphocytes* / immunology
  • CD4-Positive T-Lymphocytes* / metabolism
  • Disease Models, Animal
  • Female
  • Granulocyte-Macrophage Colony-Stimulating Factor / immunology
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • Hepatocytes / immunology
  • Hepatocytes / metabolism
  • Humans
  • Inflammation* / immunology
  • Inflammation* / pathology
  • Interferon-gamma / metabolism
  • Interleukin-17 / immunology
  • Interleukin-17 / metabolism
  • Liver / immunology
  • Liver / pathology
  • Liver Cirrhosis* / immunology
  • Liver Cirrhosis* / metabolism
  • Liver Cirrhosis* / pathology
  • Macrophages / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myofibroblasts / immunology
  • Myofibroblasts / metabolism
  • Th17 Cells / immunology
  • Th17 Cells / metabolism

Substances

  • Autophagy-Related Protein 5
  • Interleukin-17
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Atg5 protein, mouse
  • Interferon-gamma
  • ATG5 protein, human