Protein kinase Cα-mediated phosphorylation of Twist1 at Ser-144 prevents Twist1 ubiquitination and stabilizes it

J Biol Chem. 2019 Mar 29;294(13):5082-5093. doi: 10.1074/jbc.RA118.005921. Epub 2019 Feb 7.

Abstract

Twist1 is a basic helix-loop-helix transcription factor that plays a key role in embryonic development, and its expression is down-regulated in adult cells. However, Twist1 is highly expressed during cancer development, conferring a proliferative, migratory, and invasive phenotype to malignant cells. Twist1 expression can be regulated post-translationally by phosphorylation or ubiquitination events. We report in this study a previously unknown and relevant Twist1 phosphorylation site that controls its stability. To identify candidate phosphorylation sites in Twist1, we first conducted an in silico analysis of the Twist1 protein, which yielded several potential sites. Because most of these sites were predicted to be phosphorylated by protein kinase C (PKC), we overexpressed PKCα in several cell lines and found that it phosphorylates Twist1 on Ser-144. Using a combination of immunoblotting, immunoprecipitation, protein overexpression, and CRISPR/Cas9-mediated PKCα knockout experiments, we observed that PKCα-mediated Twist1 phosphorylation at Ser-144 inhibits Twist1 ubiquitination and consequently stabilizes it. These results provide evidence for a direct association between PKCα and Twist1 and yield critical insights into the PKCα/Twist1 signaling axis that governs cancer aggressiveness.

Keywords: NetphosK3.1; PKCalpha; Twist1; embryonic development; epithelial-mesenchymal transition (EMT); ovarian cancer; phosphorylation; post-transcriptional regulation; ubiquitylation (ubiquitination).

Publication types

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

MeSH terms

  • Epithelial-Mesenchymal Transition
  • HEK293 Cells
  • Humans
  • Models, Molecular
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / metabolism*
  • Phosphorylation
  • Protein Interaction Domains and Motifs
  • Protein Kinase C-alpha / metabolism*
  • Protein Stability
  • Twist-Related Protein 1 / chemistry
  • Twist-Related Protein 1 / metabolism*
  • Ubiquitination*

Substances

  • Nuclear Proteins
  • TWIST1 protein, human
  • Twist-Related Protein 1
  • PRKCA protein, human
  • Protein Kinase C-alpha