αE-catenin inhibits a Src-YAP1 oncogenic module that couples tyrosine kinases and the effector of Hippo signaling pathway

Genes Dev. 2016 Apr 1;30(7):798-811. doi: 10.1101/gad.274951.115. Epub 2016 Mar 24.

Abstract

Cell-cell adhesion protein αE-catenin inhibits skin squamous cell carcinoma (SCC) development; however, the mechanisms responsible for this function are not completely understood. We report here that αE-catenin inhibits β4 integrin-mediated activation of SRC tyrosine kinase.SRCis the first discovered oncogene, but the protein substrate critical for SRC-mediated transformation has not been identified. We found that YAP1, the pivotal effector of the Hippo signaling pathway, is a direct SRC phosphorylation target, and YAP1 phosphorylation at three sites in its transcription activation domain is necessary for SRC-YAP1-mediated transformation. We uncovered a marked increase in this YAP1 phosphorylation in human and mouse SCC tumors with low/negative expression of αE-catenin. We demonstrate that the tumor suppressor function of αE-catenin involves negative regulation of the β4 integrin-SRC signaling pathway and that SRC-mediated phosphorylation and activation of YAP1 are an alternative to the canonical Hippo signaling pathway that directly connect oncogenic tyrosine kinase signaling with YAP1.

Keywords: SCC; SRC; YAP1; keratinocytes; skin; αE-catenin.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Carcinoma, Squamous Cell / enzymology
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / physiopathology*
  • Cell Cycle Proteins
  • Cell Nucleus / metabolism
  • Cell Proliferation
  • Cell Transformation, Neoplastic / genetics
  • Cells, Cultured
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Keratinocytes / cytology
  • Keratinocytes / pathology
  • Mice
  • Oncogene Protein pp60(v-src) / metabolism*
  • Phosphoproteins / metabolism*
  • Phosphorylation
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Transport
  • Protein-Tyrosine Kinases / metabolism*
  • Signal Transduction*
  • YAP-Signaling Proteins
  • alpha Catenin / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Cell Cycle Proteins
  • Phosphoproteins
  • YAP-Signaling Proteins
  • Yap1 protein, mouse
  • alpha Catenin
  • Protein-Tyrosine Kinases
  • Oncogene Protein pp60(v-src)
  • Protein Serine-Threonine Kinases