TOX3 inhibits cancer cell migration and invasion via transcriptional regulation of SNAI1 and SNAI2 in clear cell renal cell carcinoma

Cancer Lett. 2019 May 1:449:76-86. doi: 10.1016/j.canlet.2019.02.020. Epub 2019 Feb 14.

Abstract

Studies on the mechanism of clear cell renal cell carcinoma (ccRCC) progression are lacking. In this study, TOX3 was identified as a novel cancer suppressor gene in ccRCC. Hypermethylation of CpG probes in the promoter region was associated with the functional loss of TOX3 in ccRCC cancer tissues. Downregulation of TOX3 mRNA was strongly associated with poor clinical outcomes in ccRCC. Immunohistochemistry confirmed TOX3 was downregulated in primary tumors without metastasis (n = 126) and further downregulated in primary metastatic tumors (n = 23) compared with adjacent noncancerous tissues (n = 92). In vitro, overexpression of TOX3 inhibited RCC cell growth, migration and invasion. Mechanistic investigations showed that TOX3 deficiency facilitates the epithelial-mesenchymal transition due to impairment of transcriptional repression of SNAIL members SNAI1 and SNAI2 and promotes cancer cell migration and invasion. In vivo, restoring TOX3 expression reduced lung metastatic lesions and prolonged survival of mice. TOX3 combined with SNAI1 or SNAI2 predicted overall survival in ccRCC patients. Blockage of this pathway could be a promising therapeutic target for advanced ccRCC.

Keywords: Clear cell renal cell carcinoma (ccRCC); Invasion; Migration; TOX3; Transcriptional regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / genetics*
  • Apoptosis Regulatory Proteins / metabolism*
  • Carcinoma, Renal Cell / genetics
  • Carcinoma, Renal Cell / metabolism
  • Carcinoma, Renal Cell / pathology*
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • DNA Methylation
  • Down-Regulation
  • Epithelial-Mesenchymal Transition
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Kidney Neoplasms / genetics
  • Kidney Neoplasms / metabolism
  • Kidney Neoplasms / pathology*
  • Male
  • Mice
  • Neoplasm Invasiveness
  • Neoplasm Transplantation
  • Prognosis
  • Snail Family Transcription Factors / genetics*
  • Trans-Activators / genetics*
  • Trans-Activators / metabolism*
  • Transcription, Genetic

Substances

  • Apoptosis Regulatory Proteins
  • SNAI1 protein, human
  • SNAI2 protein, human
  • Snail Family Transcription Factors
  • TOX3 protein, human
  • Trans-Activators