Amphiregulin from regulatory T cells promotes liver fibrosis and insulin resistance in non-alcoholic steatohepatitis

Immunity. 2024 Feb 13;57(2):303-318.e6. doi: 10.1016/j.immuni.2024.01.009. Epub 2024 Feb 2.

Abstract

Production of amphiregulin (Areg) by regulatory T (Treg) cells promotes repair after acute tissue injury. Here, we examined the function of Treg cells in non-alcoholic steatohepatitis (NASH), a setting of chronic liver injury. Areg-producing Treg cells were enriched in the livers of mice and humans with NASH. Deletion of Areg in Treg cells, but not in myeloid cells, reduced NASH-induced liver fibrosis. Chronic liver damage induced transcriptional changes associated with Treg cell activation. Mechanistically, Treg cell-derived Areg activated pro-fibrotic transcriptional programs in hepatic stellate cells via epidermal growth factor receptor (EGFR) signaling. Deletion of Areg in Treg cells protected mice from NASH-dependent glucose intolerance, which also was dependent on EGFR signaling on hepatic stellate cells. Areg from Treg cells promoted hepatocyte gluconeogenesis through hepatocyte detection of hepatic stellate cell-derived interleukin-6. Our findings reveal a maladaptive role for Treg cell-mediated tissue repair functions in chronic liver disease and link liver damage to NASH-dependent glucose intolerance.

Keywords: NASH; Tregs; insulin resistance; liver fibrosis; non-alcoholic steatohepatitis; regulatory T cells.

MeSH terms

  • Amphiregulin / genetics
  • Amphiregulin / metabolism
  • Animals
  • ErbB Receptors / metabolism
  • Glucose Intolerance* / metabolism
  • Glucose Intolerance* / pathology
  • Humans
  • Insulin Resistance*
  • Liver / metabolism
  • Liver Cirrhosis / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Non-alcoholic Fatty Liver Disease* / pathology
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Amphiregulin
  • ErbB Receptors
  • AREG protein, human
  • Areg protein, mouse