β-catenin signaling in murine liver zonation and regeneration: a Wnt-Wnt situation!

Hepatology. 2014 Sep;60(3):964-76. doi: 10.1002/hep.27082. Epub 2014 Jul 25.

Abstract

Liver-specific β-catenin knockout (β-Catenin-LKO) mice have revealed an essential role of β-catenin in metabolic zonation where it regulates pericentral gene expression and in initiating liver regeneration (LR) after partial hepatectomy (PH), by regulating expression of Cyclin-D1. However, what regulates β-catenin activity in these events remains an enigma. Here we investigate to what extent β-catenin activation is Wnt-signaling-dependent and the potential cell source of Wnts. We studied liver-specific Lrp5/6 KO (Lrp-LKO) mice where Wnt-signaling was abolished in hepatocytes while the β-catenin gene remained intact. Intriguingly, like β-catenin-LKO mice, Lrp-LKO exhibited a defect in metabolic zonation observed as a lack of glutamine synthetase (GS), Cyp1a2, and Cyp2e1. Lrp-LKO also displayed a significant delay in initiation of LR due to the absence of β-catenin-TCF4 association and lack of Cyclin-D1. To address the source of Wnt proteins in liver, we investigated conditional Wntless (Wls) KO mice, which lacked the ability to secrete Wnts from either liver epithelial cells (Wls-LKO), or macrophages including Kupffer cells (Wls-MKO), or endothelial cells (Wls-EKO). While Wls-EKO was embryonic lethal precluding further analysis in adult hepatic homeostasis and growth, Wls-LKO and Wls-MKO were viable but did not show any defect in hepatic zonation. Wls-LKO showed normal initiation of LR; however, Wls-MKO showed a significant but temporal deficit in LR that was associated with decreased β-catenin-TCF4 association and diminished Cyclin-D1 expression.

Conclusion: Wnt-signaling is the major upstream effector of β-catenin activity in pericentral hepatocytes and during LR. Hepatocytes, cholangiocytes, or macrophages are not the source of Wnts in regulating hepatic zonation. However, Kupffer cells are a major contributing source of Wnt secretion necessary for β-catenin activation during LR.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adherens Junctions / physiology
  • Animals
  • Female
  • Gene Expression Regulation
  • Hepatectomy
  • Kupffer Cells / chemistry
  • Kupffer Cells / metabolism
  • Kupffer Cells / physiology
  • Liver / cytology
  • Liver / metabolism
  • Liver / physiology
  • Liver Regeneration / physiology*
  • Male
  • Mice
  • Mice, Knockout
  • Signal Transduction / genetics
  • Signal Transduction / physiology*
  • Wnt Proteins / physiology*
  • beta Catenin / deficiency
  • beta Catenin / genetics
  • beta Catenin / physiology*

Substances

  • Wnt Proteins
  • beta Catenin