Molecular dissection of the mechanism by which EWS/FLI expression compromises actin cytoskeletal integrity and cell adhesion in Ewing sarcoma

Mol Biol Cell. 2014 Sep 15;25(18):2695-709. doi: 10.1091/mbc.E14-01-0007. Epub 2014 Jul 23.

Abstract

Ewing sarcoma is the second-most-common bone cancer in children. Driven by an oncogenic chromosomal translocation that results in the expression of an aberrant transcription factor, EWS/FLI, the disease is typically aggressive and micrometastatic upon presentation. Silencing of EWS/FLI in patient-derived tumor cells results in the altered expression of hundreds to thousands of genes and is accompanied by dramatic morphological changes in cytoarchitecture and adhesion. Genes encoding focal adhesion, extracellular matrix, and actin regulatory proteins are dominant targets of EWS/FLI-mediated transcriptional repression. Reexpression of genes encoding just two of these proteins, zyxin and α5 integrin, is sufficient to restore cell adhesion and actin cytoskeletal integrity comparable to what is observed when the EWS/FLI oncogene expression is compromised. Using an orthotopic xenograft model, we show that EWS/FLI-induced repression of α5 integrin and zyxin expression promotes tumor progression by supporting anchorage-independent cell growth. This selective advantage is paired with a tradeoff in which metastatic lung colonization is compromised.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bone Neoplasms / metabolism*
  • Bone Neoplasms / pathology
  • Cell Adhesion*
  • Cell Line, Tumor
  • Cytoskeleton / metabolism*
  • Gene Expression
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Integrin alphaV / metabolism
  • Lung / pathology
  • Lung Neoplasms / metabolism*
  • Lung Neoplasms / secondary
  • Male
  • Mice, Inbred NOD
  • Mice, SCID
  • Neoplasm Transplantation
  • Oncogene Proteins, Fusion / metabolism*
  • Proto-Oncogene Protein c-fli-1 / metabolism*
  • RNA-Binding Protein EWS / metabolism*
  • Sarcoma, Ewing / metabolism*
  • Sarcoma, Ewing / pathology
  • Zyxin / metabolism

Substances

  • EWS-FLI fusion protein
  • Integrin alphaV
  • Oncogene Proteins, Fusion
  • Proto-Oncogene Protein c-fli-1
  • RNA-Binding Protein EWS
  • ZYX protein, human
  • Zyxin