PKA-mediated Gli2 and Gli3 phosphorylation is inhibited by Hedgehog signaling in cilia and reduced in Talpid3 mutant

Dev Biol. 2017 Sep 1;429(1):147-157. doi: 10.1016/j.ydbio.2017.06.035. Epub 2017 Jul 1.

Abstract

Hedgehog (Hh) signaling is thought to occur in primary cilia, but the molecular basis of Gli2 and Gli3 activation by Hh signaling in cilia is unknown. Similarly, how ciliary gene mutations result in reduced Gli3 processing that generates a repressor is also not clear. Here we show that Hh signaling inhibits Gli2 and Gli3 phosphorylation by protein kinase A (PKA) in cilia. The cilia related gene Talpid3 (Ta3) mutation results in the reduced processing and phosphorylation of Gli2 and Gli3. Interestingly, Ta3 interacts and colocalizes with PKA regulatory subunit PKARIIβ at centrioles in the cell. The centriolar localization and PKA binding regions are located in the N- and C-terminal regions of Ta3, respectively. PKARIIβ fails to localize at centrioles in some Ta3 mutant cells. Therefore, our study provides the direct evidence that Gli2 and Gli3 are dephosphorylated and activated in cilia and that impaired Gli2 and Gli3 processing in Ta3 mutant is at least in part due to a decrease in Gli2 and Gli3 phosphorylation.

Keywords: Cilia; Gli2; Gli3; Hedgehog; PKA; Talpid3.

MeSH terms

  • A Kinase Anchor Proteins / metabolism
  • Animals
  • Antibodies / metabolism
  • Cell Cycle Proteins / genetics*
  • Cell Cycle Proteins / metabolism
  • Centrosome / metabolism
  • Cilia / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Hedgehog Proteins / metabolism*
  • Kruppel-Like Transcription Factors / metabolism*
  • Mice, Inbred C57BL
  • Microtubule-Associated Proteins / metabolism
  • Mutation / genetics
  • Nerve Tissue Proteins / metabolism*
  • Organogenesis*
  • Phosphopeptides / metabolism
  • Phosphorylation
  • Protein Binding
  • Protein Processing, Post-Translational
  • Signal Transduction*
  • Zinc Finger Protein Gli2
  • Zinc Finger Protein Gli3

Substances

  • A Kinase Anchor Proteins
  • Akap9 protein, mouse
  • Antibodies
  • Cell Cycle Proteins
  • Gli2 protein, mouse
  • Gli3 protein, mouse
  • Hedgehog Proteins
  • Kruppel-Like Transcription Factors
  • Microtubule-Associated Proteins
  • Nerve Tissue Proteins
  • Phosphopeptides
  • Talpid3 protein, mouse
  • Zinc Finger Protein Gli2
  • Zinc Finger Protein Gli3
  • Cyclic AMP-Dependent Protein Kinases