Cisplatin-selected resistance is associated with increased motility and stem-like properties via activation of STAT3/Snail axis in atypical teratoid/rhabdoid tumor cells

Oncotarget. 2015 Jan 30;6(3):1750-68. doi: 10.18632/oncotarget.2737.

Abstract

Atypical teratoid/rhabdoid tumor (ATRT) is a malignant pediatric brain tumor with great recurrence after complete surgery and chemotherapy. Here, we demonstrate that cisplatin treatment selects not only for resistance but also for a more oncogenic phenotype characterized by high self-renewal and invasive capabilities. These phenomena are likely due to STAT3 upregulatoin which occurred simultaneously with higher expression of Snail, an activator of epithelial-mesenchymal transition (EMT), in ATRT-CisR cells. STAT3 knockdown effectively suppressed Snail expression and blocked motility and invasion in ATRT-CisR cells, while overexpressing Snail reversed these effects. Chromatin immunoprecipitation assay indicated that STAT3 directly bound to Snail promoter. Moreover, STAT3 knockdown effectively suppressed cancer stem-like properties, synergistically enhanced the chemotherapeutic effect, and significantly improved survival rate in ATRT-CisR-transplanted immunocompromised mice. Finally, immunohistochemistrical analysis showed that STAT3 and Snail were coexpressed at high levels in recurrent ATRT tissues. Thus, the STAT3/Snail pathway plays an important role in oncogenic resistance, rendering cells not only drug-resistant but also increasingly oncogenic (invasion, EMT and recurrence). Therefore, the STAT3/Snail could be a target for ATRT treatment.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology*
  • Cell Line, Tumor
  • Cell Movement / physiology*
  • Cisplatin / pharmacology*
  • Drug Resistance, Neoplasm
  • Female
  • Heterografts
  • Humans
  • Male
  • Mice
  • Mice, SCID
  • Rhabdoid Tumor / drug therapy
  • Rhabdoid Tumor / metabolism
  • Rhabdoid Tumor / pathology*
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction
  • Snail Family Transcription Factors
  • Transcription Factors / metabolism*

Substances

  • Antineoplastic Agents
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Snail Family Transcription Factors
  • Transcription Factors
  • Cisplatin