Hepatocellular RECK as a Critical Regulator of Metabolic Dysfunction-associated Steatohepatitis Development

Cell Mol Gastroenterol Hepatol. 2024;18(3):101365. doi: 10.1016/j.jcmgh.2024.101365. Epub 2024 May 24.

Abstract

Background & aims: Reversion-inducing cysteine-rich protein with Kazal motifs (RECK) is an extracellular matrix regulator with anti-fibrotic effects. However, its expression and role in metabolic dysfunction-associated steatohepatitis (MASH) and hepatic fibrosis are poorly understood.

Methods: We generated a novel transgenic mouse model with RECK overexpression specifically in hepatocytes to investigate its role in Western diet (WD)-induced liver disease. Proteomic analysis and in vitro studies were performed to mechanistically link RECK to hepatic inflammation and fibrosis.

Results: Our results show that RECK expression is significantly decreased in liver biopsies from human patients diagnosed with MASH and correlated negatively with severity of metabolic dysfunction-associated steatotic liver disease (MASLD) and fibrosis. Similarly, RECK expression is downregulated in WD-induced MASH in wild-type mice. Hepatocyte-specific RECK overexpression significantly reduced hepatic pathology in WD-induced liver injury. Proteomic analysis highlighted changes in extracellular matrix and cell-signaling proteins. In vitro mechanistic studies linked RECK induction to reduced ADAM10 (a disintegrin and metalloproteinase domain-containing protein 10) and ADAM17 activity, amphiregulin release, epidermal growth factor receptor activation, and stellate cell activation.

Conclusion: Our in vivo and mechanistic in vitro studies reveal that RECK is a novel upstream regulator of inflammation and fibrosis in the diseased liver, its induction is hepatoprotective, and thus highlights its potential as a novel therapeutic in MASH.

Keywords: Amphiregulin; Epidermal Growth Factor Receptor; Extracellular Matrix; Fatty Liver Disease; MASH; MASLD; NAFLD; NASH; Reversion-inducing Cysteine-rich Protein With Kazal Motifs; Steatosis.

MeSH terms

  • ADAM10 Protein / genetics
  • ADAM10 Protein / metabolism
  • ADAM17 Protein / genetics
  • ADAM17 Protein / metabolism
  • Amphiregulin / genetics
  • Amphiregulin / metabolism
  • Amyloid Precursor Protein Secretases / metabolism
  • Animals
  • Disease Models, Animal*
  • ErbB Receptors / metabolism
  • Fatty Liver / metabolism
  • Fatty Liver / pathology
  • GPI-Linked Proteins* / genetics
  • GPI-Linked Proteins* / metabolism
  • Hepatocytes* / metabolism
  • Hepatocytes* / pathology
  • Humans
  • Liver / metabolism
  • Liver / pathology
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / pathology
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Transgenic*
  • Non-alcoholic Fatty Liver Disease / etiology
  • Non-alcoholic Fatty Liver Disease / metabolism
  • Non-alcoholic Fatty Liver Disease / pathology
  • Proteomics
  • Signal Transduction

Substances

  • GPI-Linked Proteins
  • RECK protein, human
  • Reck protein, mouse
  • ADAM10 Protein
  • ADAM17 Protein
  • Amyloid Precursor Protein Secretases
  • ErbB Receptors
  • Adam10 protein, mouse
  • Membrane Proteins
  • Amphiregulin