Prostaglandin promotion of osteocyte gap junction function through transcriptional regulation of connexin 43 by glycogen synthase kinase 3/beta-catenin signaling

Mol Cell Biol. 2010 Jan;30(1):206-19. doi: 10.1128/MCB.01844-08.

Abstract

Gap junction intercellular communication in osteocytes plays an important role in bone remodeling in response to mechanical loading; however, the responsible molecular mechanisms remain largely unknown. Here, we show that phosphoinositide-3 kinase (PI3K)/Akt signaling activated by fluid flow shear stress and prostaglandin E(2) (PGE(2)) had a stimulatory effect on both connexin 43 (Cx43) mRNA and protein expression. PGE(2) inactivated glycogen synthase kinase 3 (GSK-3) and promoted nuclear localization and accumulation of beta-catenin. Knockdown of beta-catenin expression resulted in a reduction in Cx43 protein. Furthermore, the chromatin immunoprecipitation (ChIP) assay demonstrated an association of beta-catenin with the Cx43 promoter, suggesting that beta-catenin could regulate Cx43 expression at the level of gene transcription. We have previously reported that PGE(2) activates cyclic AMP (cAMP)-protein kinase A (PKA) signaling and increases Cx43 and gap junctions. Interestingly, the activation of PI3K/Akt appeared to be independent of the activation of PKA, whereas both PI3K/Akt and PKA signaling inactivated GSK-3 and increased beta-catenin translocation. Together, these results suggest that shear stress, through PGE(2) release, activates both PI3K/Akt and cAMP-PKA signaling, which converge through the inactivation of GSK-3, leading to the increase in nuclear accumulation of beta-catenin. beta-Catenin binds to the Cx43 promoter, stimulating Cx43 expression and functional gap junctions between osteocytes.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • Cell Line
  • Cell Nucleus / metabolism
  • Connexin 43 / genetics
  • Connexin 43 / metabolism*
  • Cyclic AMP / physiology
  • Cyclic AMP-Dependent Protein Kinases / physiology
  • Dinoprostone / physiology*
  • Gap Junctions / physiology*
  • Glycogen Synthase Kinase 3 / physiology*
  • Mice
  • Osteocytes / physiology*
  • Phosphatidylinositol 3-Kinases / physiology
  • Proto-Oncogene Proteins c-akt / physiology
  • Signal Transduction
  • Transcription, Genetic*
  • beta Catenin / biosynthesis
  • beta Catenin / physiology*

Substances

  • CTNNB1 protein, mouse
  • Connexin 43
  • GJA1 protein, mouse
  • beta Catenin
  • Cyclic AMP
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-akt
  • Cyclic AMP-Dependent Protein Kinases
  • Glycogen Synthase Kinase 3
  • Dinoprostone