Hepatocyte-specific SLC27A4 deletion ameliorates nonalcoholic fatty liver disease in mice via suppression of phosphatidylcholine-mediated PXR activation

Metabolism. 2025 Jan:162:156054. doi: 10.1016/j.metabol.2024.156054. Epub 2024 Nov 1.

Abstract

Background: The protein Solute carrier family 27 member 4 (SLC27A4) is crucial for fatty acid synthesis and β-oxidation, but its role in hepatic steatosis and nonalcoholic fatty liver disease (NAFLD) progression is not fully understood.

Methods: Mice with AAV-mediated overexpression of Slc27a4 in liver and hepatocytes-specific deletion of Slc27a4 were fed a standard chow diet, a high-fat diet (HFD), or a methionine and choline-deficient diet (MCD). Serum and liver tissues were collected and analyzed by biochemical assay, histology, lipidomic analysis, RNA-seq analysis, qPCR, western blot and immunofluorescence.

Results: This study found elevated expression of SLC27A4 in individuals with NAFLD and OAPA-treated MPHs cells, leading to increased lipid accumulation and diet-induced liver steatosis, inflammation, and fibrosis. Conversely, hepatocyte-specific deletion of Slc27a4 improved the development of both NAFLD and NASH. SLC27A4 overexpression resulted in increased hepatic pregnane X receptor (PXR) expression and accumulation of phosphatidylcholine (PC), which activates PXR signaling and inducing SLC27A4 expression. PXR overexpression hinders the protective impact of Slc27a4 deletion on lipid accumulation and inflammation, whereas its deficiency in mice reduces the effect of Slc27a4 overexpression on NAFLD development.

Conclusion: These results indicate that SLC27A4 plays a critical role of lipid accumulation and inflammation, and is implicated in the development of NAFLD progression, rendering it potentially actionable target for NAFLD treatment.

Keywords: Hepatocytes; NR1I2); Nonalcoholic fatty liver disease (NAFLD); Phosphatidylcholine (PC); Pregnane X receptor (PXR; Solute carrier family 27 member 4 (SLC27A4).

MeSH terms

  • Animals
  • Diet, High-Fat / adverse effects
  • Fatty Acid Transport Proteins / genetics
  • Fatty Acid Transport Proteins / metabolism
  • Hepatocytes* / metabolism
  • Humans
  • Liver / metabolism
  • Liver / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Non-alcoholic Fatty Liver Disease* / genetics
  • Non-alcoholic Fatty Liver Disease* / metabolism
  • Non-alcoholic Fatty Liver Disease* / pathology
  • Phosphatidylcholines* / metabolism
  • Pregnane X Receptor* / genetics
  • Pregnane X Receptor* / metabolism

Substances

  • Phosphatidylcholines
  • Pregnane X Receptor
  • Slc27a4 protein, mouse
  • Fatty Acid Transport Proteins