Protein kinase A-dependent pSer(675) -β-catenin, a novel signaling defect in a mouse model of congenital hepatic fibrosis

Hepatology. 2013 Nov;58(5):1713-23. doi: 10.1002/hep.26554. Epub 2013 Sep 30.

Abstract

Genetically determined loss of fibrocystin function causes congenital hepatic fibrosis (CHF), Caroli disease (CD), and autosomal recessive polycystic kidney disease (ARPKD). Cystic dysplasia of the intrahepatic bile ducts and progressive portal fibrosis characterize liver pathology in CHF/CD. At a cellular level, several functional morphological and signaling changes have been reported including increased levels of 3'-5'-cyclic adenosine monophosphate (cAMP). In this study we addressed the relationships between increased cAMP and β-catenin. In cholangiocytes isolated and cultured from Pkhd1(del4/del4) mice, stimulation of cAMP/PKA signaling (forskolin 10 μM) stimulated Ser(675) -phosphorylation of β-catenin, its nuclear localization, and its transcriptional activity (western blot and TOP flash assay, respectively) along with a down-regulation of E-cadherin expression (immunocytochemistry and western blot); these changes were inhibited by the PKA blocker, PKI (1 μM). The Rho-GTPase, Rac-1, was also significantly activated by cAMP in Pkhd1(del4/del4) cholangiocytes. Rac-1 inhibition blocked cAMP-dependent nuclear translocation and transcriptional activity of pSer(675) -β-catenin. Cell migration (Boyden chambers) was significantly higher in cholangiocytes obtained from Pkhd1(del4/del4) and was inhibited by: (1) PKI, (2) silencing β-catenin (siRNA), and (3) the Rac-1 inhibitor NSC 23766.

Conclusion: These data show that in fibrocystin-defective cholangiocytes, cAMP/PKA signaling stimulates pSer(675) -phosphorylation of β-catenin and Rac-1 activity. In the presence of activated Rac-1, pSer(675) -β-catenin is translocated to the nucleus, becomes transcriptionally active, and is responsible for increased motility of Pkhd1(del4/del4) cholangiocytes. β-Catenin-dependent changes in cell motility may be central to the pathogenesis of the disease and represent a potential therapeutic target.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • Bile Ducts / cytology
  • Cell Movement
  • Cyclic AMP / physiology
  • Cyclic AMP-Dependent Protein Kinases / physiology*
  • Disease Models, Animal
  • Genetic Diseases, Inborn / etiology*
  • Genetic Diseases, Inborn / metabolism
  • Liver Cirrhosis / etiology*
  • Liver Cirrhosis / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Neuropeptides / physiology
  • Receptors, Cell Surface / physiology
  • Signal Transduction*
  • beta Catenin / metabolism*
  • rac1 GTP-Binding Protein / physiology

Substances

  • CTNNB1 protein, mouse
  • Neuropeptides
  • Pkhd1 protein, mouse
  • Rac1 protein, mouse
  • Receptors, Cell Surface
  • beta Catenin
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • rac1 GTP-Binding Protein

Supplementary concepts

  • Hepatic Fibrosis, Congenital