Mechanism and relevance of EWS/FLI-mediated transcriptional repression in Ewing sarcoma

Oncogene. 2013 Oct 17;32(42):5089-100. doi: 10.1038/onc.2012.525. Epub 2012 Nov 26.

Abstract

Ewing sarcoma provides an important model for transcription-factor-mediated oncogenic transformation because of its reliance on the ETS-type fusion oncoprotein EWS/FLI. EWS/FLI functions as a transcriptional activator and transcriptional activation is required for its oncogenic activity. Here, we demonstrate that a previously less-well characterized transcriptional repressive function of the EWS/FLI fusion is also required for the transformed phenotype of Ewing sarcoma. Through comparison of EWS/FLI transcriptional profiling and genome-wide localization data, we define the complement of EWS/FLI direct downregulated target genes. We demonstrate that LOX is a previously undescribed EWS/FLI-repressed target that inhibits the transformed phenotype of Ewing sarcoma cells. Mechanistic studies demonstrate that the NuRD co-repressor complex interacts with EWS/FLI, and that its associated histone deacetylase and LSD1 activities contribute to the repressive function. Taken together, these data reveal a previously unknown molecular function for EWS/FLI, demonstrate a more highly coordinated oncogenic transcriptional hierarchy mediated by EWS/FLI than previously suspected, and implicate a new paradigm for therapeutic intervention aimed at controlling NuRD activity in Ewing sarcoma tumors.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Neoplasms / genetics*
  • Bone Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Transformation, Neoplastic / genetics
  • Co-Repressor Proteins / genetics
  • Co-Repressor Proteins / metabolism
  • Gene Expression Regulation, Neoplastic*
  • Genes, Tumor Suppressor
  • Histone Deacetylases / metabolism
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism
  • Humans
  • Mi-2 Nucleosome Remodeling and Deacetylase Complex / genetics
  • Mi-2 Nucleosome Remodeling and Deacetylase Complex / metabolism
  • Mice, Nude
  • Oncogene Proteins, Fusion / genetics*
  • Oncogene Proteins, Fusion / metabolism
  • Protein Structure, Tertiary
  • Protein-Lysine 6-Oxidase / genetics
  • Protein-Lysine 6-Oxidase / metabolism
  • Proto-Oncogene Protein c-fli-1 / genetics*
  • Proto-Oncogene Protein c-fli-1 / metabolism
  • RNA-Binding Protein EWS / genetics*
  • RNA-Binding Protein EWS / metabolism
  • Sarcoma, Ewing / genetics*
  • Sarcoma, Ewing / pathology
  • Transcription, Genetic
  • Xenograft Model Antitumor Assays

Substances

  • Co-Repressor Proteins
  • EWS-FLI fusion protein
  • Oncogene Proteins, Fusion
  • Proto-Oncogene Protein c-fli-1
  • RNA-Binding Protein EWS
  • Histone Demethylases
  • Protein-Lysine 6-Oxidase
  • KDM1A protein, human
  • Histone Deacetylases
  • Mi-2 Nucleosome Remodeling and Deacetylase Complex