Wnt/β-catenin Signaling Contributes to Tumor Malignancy and Is Targetable in Gastrointestinal Stromal Tumor

Mol Cancer Ther. 2017 Sep;16(9):1954-1966. doi: 10.1158/1535-7163.MCT-17-0139. Epub 2017 Jun 13.

Abstract

Gastrointestinal stromal tumor (GIST) is the most common type of sarcoma and usually harbors either a KIT or PDGFRA mutation. However, the molecular basis for tumor malignancy is not well defined. Although the Wnt/β-catenin signaling pathway is important in a variety of cancers, its role in GIST is uncertain. Through analysis of nearly 150 human GIST specimens, we found that some human GISTs expressed β-catenin and contained active, dephosphorylated nuclear β-catenin. Furthermore, advanced human GISTs expressed reduced levels of the Wnt antagonist DKK4. Accordingly, in human GIST T1 cells, Wnt stimulation increased β-catenin-mediated transcriptional activity in a reporter assay as well as transcription of the downstream target genes Axin2 and CCND1 In contrast, DKK4 overexpression in GIST T1 cells reduced Wnt/β-catenin signaling. In addition, we showed that nuclear β-catenin stability was partially regulated by the E3 ligase COP1, as demonstrated with coimmunoprecipitation and COP1 knockdown. Three molecular inhibitors of the Wnt/β-catenin pathway demonstrated antitumor efficacy in various GIST models, both in vitro and in vivo Notably, the tankyrase inhibitor G007-LK alone had substantial activity against tumors of genetically engineered KitV558Δ/+ mice, and the effect was increased by the addition of the Kit inhibitor imatinib mesylate. Collectively, our findings demonstrate that Wnt/β-catenin signaling is a novel therapeutic target for selected untreated or imatinib-resistant GISTs. Mol Cancer Ther; 16(9); 1954-66. ©2017 AACR.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Cell Line, Tumor
  • Disease Models, Animal
  • Gastrointestinal Stromal Tumors / drug therapy
  • Gastrointestinal Stromal Tumors / metabolism*
  • Gastrointestinal Stromal Tumors / pathology*
  • Humans
  • Imatinib Mesylate / pharmacology
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Mice
  • Mice, Transgenic
  • Molecular Targeted Therapy
  • Neoplasm Grading
  • Neoplasm Staging
  • Ubiquitin-Protein Ligases / metabolism
  • Wnt Signaling Pathway* / drug effects
  • Wnt3A Protein / metabolism
  • Xenograft Model Antitumor Assays
  • beta Catenin / metabolism

Substances

  • Antineoplastic Agents
  • DKK4 protein, human
  • Intercellular Signaling Peptides and Proteins
  • Wnt3A Protein
  • beta Catenin
  • Imatinib Mesylate
  • COP1 protein, human
  • Ubiquitin-Protein Ligases