The Nr4a family regulates intrahepatic Treg proliferation and liver fibrosis in MASLD models

J Clin Invest. 2024 Oct 15;134(23):e175305. doi: 10.1172/JCI175305.

Abstract

Metabolic dysfunction-associated steatotic hepatitis (MASH) is a chronic progressive liver disease that is highly prevalent worldwide. MASH is characterized by hepatic steatosis, inflammation, fibrosis, and liver damage, which eventually result in liver dysfunction due to cirrhosis or hepatocellular carcinoma. However, the cellular and molecular mechanisms underlying MASH progression remain largely unknown. Here, we found an increase of the Nr4a family of orphan nuclear receptor expression in intrahepatic T cells from mice with diet-induced MASH. Loss of Nr4a1 and Nr4a2 in T cell (dKO) ameliorated liver cell death and fibrosis, thereby mitigating liver dysfunction in MASH mice. dKO resulted in reduction of infiltrated macrophages and Th1/Th17 cells, whereas it led to a massive accumulation of Tregs in the liver of MASH mice. Combined single-cell RNA transcriptomic and TCR sequencing analysis revealed that intrahepatic dKO Tregs exhibited enhanced T cell immunoreceptor with Ig and ITIM domains (TIGIT) and IL-10 expression and were clonally expanded during MASH progression. Mechanistically, we found that dKO Tregs expressed high levels of basic leucine zipper ATF-like transcription factor (Batf), which promotes Treg cell proliferation and function upon TCR stimulation. Collectively, our findings not only provide an insight into the impact of intrahepatic Treg cells on MASH pathogenesis, but also suggest a therapeutic potential of targeting of the Nr4a family to treat the disease.

Keywords: Fibrosis; Immunology; T cell development; T cells.

MeSH terms

  • Animals
  • Cell Proliferation*
  • Disease Models, Animal
  • Fatty Liver / genetics
  • Fatty Liver / immunology
  • Fatty Liver / metabolism
  • Fatty Liver / pathology
  • Humans
  • Liver / immunology
  • Liver / metabolism
  • Liver / pathology
  • Liver Cirrhosis* / genetics
  • Liver Cirrhosis* / immunology
  • Liver Cirrhosis* / metabolism
  • Liver Cirrhosis* / pathology
  • Male
  • Mice
  • Mice, Knockout*
  • Nuclear Receptor Subfamily 4, Group A, Member 1* / deficiency
  • Nuclear Receptor Subfamily 4, Group A, Member 1* / genetics
  • Nuclear Receptor Subfamily 4, Group A, Member 1* / immunology
  • Nuclear Receptor Subfamily 4, Group A, Member 1* / metabolism
  • Nuclear Receptor Subfamily 4, Group A, Member 2* / genetics
  • Nuclear Receptor Subfamily 4, Group A, Member 2* / metabolism
  • T-Lymphocytes, Regulatory* / immunology
  • T-Lymphocytes, Regulatory* / pathology

Substances

  • Nuclear Receptor Subfamily 4, Group A, Member 1
  • Nr4a1 protein, mouse
  • Nuclear Receptor Subfamily 4, Group A, Member 2
  • Nr4a2 protein, mouse