Cdh1 regulates craniofacial development via APC-dependent ubiquitination and activation of Goosecoid

Cell Res. 2016 Jun;26(6):699-712. doi: 10.1038/cr.2016.51. Epub 2016 Apr 29.

Abstract

Craniofacial anomalies (CFAs) characterized by birth defects of skull and facial bones are the most frequent congenital disease. Genomic analysis has identified multiple genes responsible for CFAs; however, the underlying genetic mechanisms for the majority of CFAs remain largely unclear. Our previous study revealed that the Wwp2 E3 ubiquitin ligase facilitates craniofacial development in part through inducing monoubiquitination and activation of the paired-like homeobox transcription factor, Goosecoid (Gsc). Here we report that Gsc is also ubiquitinated and activated by the APC(Cdh1) E3 ubiquitin ligase, leading to transcriptional activation of various Gsc target genes crucial for craniofacial development. Consistenly, neural crest-specific Cdh1-knockout mice display similar bone malformation as Wwp2-deficient mice in the craniofacial region, characterized by a domed skull, a short snout and a twisted nasal bone. Mechanistically, like Wwp2-deficient mice, mice with Cdh1 deficiency in neural crest cells exhibit reduced Gsc/Sox6 transcriptional activities. Simultaneous deletion of Cdh1 and Wwp2 results in a more severe craniofacial defect compared with single gene deletion, suggesting a synergistic augmentation of Gsc activity by these two E3 ubiquitin ligases. Hence, our study reveals a novel role for Cdh1 in craniofacial development through promoting APC-dependent non-proteolytic ubiquitination and activation of Gsc.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Anaphase-Promoting Complex-Cyclosome / metabolism*
  • Animals
  • Cdh1 Proteins / metabolism*
  • Face / embryology*
  • Goosecoid Protein / chemistry
  • Goosecoid Protein / metabolism*
  • HeLa Cells
  • Heterozygote
  • Humans
  • Male
  • Mice, Knockout
  • Protein Binding
  • SOXD Transcription Factors / metabolism
  • Signal Transduction
  • Skull / embryology*
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination*

Substances

  • Cdh1 Proteins
  • Fzr1 protein, mouse
  • Goosecoid Protein
  • Gsc protein, mouse
  • SOXD Transcription Factors
  • Wwp2 protein, mouse
  • Anaphase-Promoting Complex-Cyclosome
  • Ubiquitin-Protein Ligases