Targeting the WEE1 kinase strengthens the antitumor activity of imatinib via promoting KIT autophagic degradation in gastrointestinal stromal tumors

Gastric Cancer. 2020 Jan;23(1):39-51. doi: 10.1007/s10120-019-00977-1. Epub 2019 Jun 13.

Abstract

Background: Activating mutation of KIT or PDGFRA is the primary molecular mechanism for gastrointestinal stromal tumors (GISTs). Although imatinib has a revolutionary effect on GIST therapeutics, the benefits are not durable. Increasing reports have demonstrated that cell cycle checkpoint plays critical roles in GIST. Here, we explore the role of WEE1 kinase in GIST progression.

Methods: Oncomine public database, western blotting, and immunohistochemistry were used to analyze WEE1 expression in GISTs. Using MTT assays, colony formation analysis, and flow cytometry, we examined the role of WEE1 in GIST cells and the antitumor activity of the inhibitor MK1775 alone, or in combination with imatinib. Cycloheximide chase assay and pharmacological inhibition of autophagy and proteasome pathway were performed to analyze KIT expression. Additionally, autophagic markers Beclin1 and LC3B were detected by western blotting.

Results: Upregulated WEE1 expression was observed in GIST tissues and correlated with tumor size, mitotic count, and risk grade. Inhibition of WEE1 significantly suppressed GIST cell proliferation, induced apoptosis and cell cycle arrest. Imatinib and MK1775 co-treatment markedly enhanced the antitumor activity. Targeting WEE1 decreased the expression of KIT expression. Moreover, WEE1 stabilized KIT protein and KIT reduction observed upon WEE1 inhibition could be reversed by pharmacological inhibition of autophagy, but not proteasome pathway. WEE1 inhibition also increased Beclin1 expression and LC3B II/I ratio in GIST cells.

Conclusions: Our data suggest that WEE1 plays a pivotal role in GIST proliferation. WEE1 inhibition could promote KIT autophagic degradation and, therefore, targeting WEE1 might represent a novel strategy for GIST therapies.

Keywords: Antitumor; Autophagic degradation; Gastrointestinal stromal tumors; MK1775; WEE1.

MeSH terms

  • Aged
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Apoptosis / drug effects
  • Autophagy / drug effects
  • Cell Cycle Proteins / antagonists & inhibitors
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Female
  • Gastrointestinal Neoplasms / drug therapy*
  • Gastrointestinal Stromal Tumors / drug therapy*
  • Gene Expression Regulation, Enzymologic / drug effects
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Imatinib Mesylate / administration & dosage
  • Imatinib Mesylate / pharmacology*
  • Male
  • Middle Aged
  • Molecular Targeted Therapy
  • Protein Kinase Inhibitors / pharmacology
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Protein-Tyrosine Kinases / genetics
  • Protein-Tyrosine Kinases / metabolism*
  • Proto-Oncogene Proteins c-kit / metabolism*
  • Pyrazoles / administration & dosage
  • Pyrazoles / pharmacology
  • Pyrimidinones / administration & dosage
  • Pyrimidinones / pharmacology

Substances

  • Cell Cycle Proteins
  • Protein Kinase Inhibitors
  • Pyrazoles
  • Pyrimidinones
  • Imatinib Mesylate
  • KIT protein, human
  • Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins c-kit
  • WEE1 protein, human
  • adavosertib