Ewing sarcoma inhibition by disruption of EWSR1-FLI1 transcriptional activity and reactivation of p53

J Pathol. 2014 Aug;233(4):415-24. doi: 10.1002/path.4378. Epub 2014 Jun 27.

Abstract

Translocations involving ETS-transcription factors, most commonly leading to the EWSR1-FLI1 fusion protein, are the hallmark of Ewing sarcoma. Despite knowledge of this driving molecular event, an effective therapeutic strategy is lacking. To test potential treatment regimes, we established a novel Ewing sarcoma zebrafish engraftment model allowing time-effective, dynamic quantification of Ewing sarcoma progression and tumour burden in vivo, applicable for screening of single and combined compounds. In Ewing sarcoma the tumour-suppressor gene TP53 is commonly found to be wild-type, thus providing an attractive target for treatment. Here, we study TP53 wild-type (EW7, CADO-ES1 and TC32) and TP53-deleted (SK-N-MC) Ewing sarcoma cell lines to investigate the potentiating effect of p53 reactivation by Nutlin-3 on treatment with YK-4-279 to block transcriptional activity of EWSR1-FLI1 protein. Blocking EWSR1-FLI1 transcriptional activity reduced Ewing sarcoma tumour cell burden irrespective of TP53 status. We show that simultaneous YK-4-279 treatment with Nutlin-3 to stabilize p53 resulted in an additive inhibition of TP53 wild-type Ewing sarcoma cell burden, whilst not affecting TP53-deleted Ewing sarcoma cells. Improved inhibition of proliferation and migration by combinatorial treatment was confirmed in vivo by zebrafish engraftments. Mechanistically, both compounds together additively induced apoptosis of tumour cells in vivo by engaging distinct pathways. We propose reactivation of the p53 pathway in combination with complementary targeted therapy by EWSR1-FLI1 transcriptional activity disruption as a valuable strategy against p53 wild-type Ewing sarcoma.

Keywords: Ewing sarcoma; anti-cancer drug screen; drug synergism; molecular targeted therapy; p53; tumour growth; zebrafish.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Bone Neoplasms / genetics
  • Bone Neoplasms / physiopathology
  • Bone Neoplasms / prevention & control*
  • Cell Line, Tumor
  • Cells, Cultured
  • Disease Models, Animal
  • Drug Synergism
  • Heterografts
  • Humans
  • Imidazoles / pharmacology
  • Indoles / pharmacology
  • Piperazines / pharmacology
  • RNA-Binding Protein EWS
  • RNA-Binding Proteins / drug effects
  • RNA-Binding Proteins / genetics*
  • Sarcoma, Ewing / genetics
  • Sarcoma, Ewing / physiopathology
  • Sarcoma, Ewing / prevention & control*
  • Signal Transduction / drug effects
  • Transcription, Genetic / drug effects
  • Transcription, Genetic / genetics
  • Transcription, Genetic / physiology*
  • Tumor Suppressor Protein p53 / drug effects
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / physiology*
  • Zebrafish
  • Zebrafish Proteins / drug effects
  • Zebrafish Proteins / genetics*

Substances

  • Antineoplastic Agents
  • Ewsr1a protein, zebrafish
  • Imidazoles
  • Indoles
  • Piperazines
  • RNA-Binding Protein EWS
  • RNA-Binding Proteins
  • Tumor Suppressor Protein p53
  • YK 4-279
  • Zebrafish Proteins
  • nutlin 3