The Aurora-A-Twist1 axis promotes highly aggressive phenotypes in pancreatic carcinoma

J Cell Sci. 2017 Mar 15;130(6):1078-1093. doi: 10.1242/jcs.196790. Epub 2017 Feb 6.

Abstract

We uncovered a crucial role for the Aurora kinase A (AURKA)-Twist1 axis in promoting epithelial-to-mesenchymal transition (EMT) and chemoresistance in pancreatic cancer. Twist1 is the first EMT-specific target of AURKA that was identified using an innovative screen. AURKA phosphorylates Twist1 at three sites, which results in its multifaceted regulation - AURKA inhibits its ubiquitylation, increases its transcriptional activity and favors its homodimerization. Twist1 reciprocates and prevents AURKA degradation, thereby triggering a feedback loop. Ablation of either AURKA or Twist1 completely inhibits EMT, highlighting both proteins as central players in EMT progression. Phosphorylation-dead Twist1 serves as a dominant-negative and fully reverses the EMT phenotype induced by Twist1, underscoring the crucial role of AURKA-mediated phosphorylation in mediating Twist1-induced malignancy. Likewise, Twist1-overexpressing BxPC3 cells formed large tumors in vivo, whereas expression of phosphorylation-dead Twist1 fully abrogated this effect. Furthermore, immunohistochemical analysis of pancreatic cancer specimens revealed a 3-fold higher level of Twist1 compared to that seen in healthy normal tissues. This is the first study that links Twist1 in a feedback loop with its activating kinase, which indicates that concurrent inhibition of AURKA and Twist1 will be synergistic in inhibiting pancreatic tumorigenesis and metastasis.

Keywords: AURKA; Drug discovery; EMT; Pancreatic cancer; Therapy; Twist1.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Aurora Kinase A / metabolism*
  • Biomarkers, Tumor / metabolism
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Cell Line, Tumor
  • Cell Movement
  • Cell Survival
  • Drug Resistance, Neoplasm
  • Epithelial-Mesenchymal Transition
  • Feedback, Physiological
  • Female
  • Humans
  • Mice, Nude
  • Neoplasm Invasiveness
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology
  • Nuclear Proteins / metabolism*
  • Pancreatic Neoplasms / metabolism*
  • Pancreatic Neoplasms / pathology*
  • Phenotype
  • Phosphorylation
  • Protein Multimerization
  • Protein Stability
  • Protein Transport
  • Proteolysis
  • Subcellular Fractions / metabolism
  • Substrate Specificity
  • Twist-Related Protein 1 / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • Biomarkers, Tumor
  • Nuclear Proteins
  • TWIST1 protein, human
  • Twist-Related Protein 1
  • Aurora Kinase A