EWS-WT1 fusion isoforms establish oncogenic programs and therapeutic vulnerabilities in desmoplastic small round cell tumors

Nat Commun. 2024 Aug 28;15(1):7460. doi: 10.1038/s41467-024-51851-3.

Abstract

EWS fusion oncoproteins underlie several human malignancies including Desmoplastic Small Round Cell Tumor (DSRCT), an aggressive cancer driven by EWS-WT1 fusion proteins. Here we combine chromatin occupancy and 3D profiles to identify EWS-WT1-dependent gene regulation networks and target genes. We show that EWS-WT1 is a powerful chromatin activator controlling an oncogenic gene expression program that characterizes primary tumors. Similar to wild type WT1, EWS-WT1 has two isoforms that differ in their DNA binding domain and we find that they have distinct DNA binding profiles and are both required to generate viable tumors that resemble primary DSRCT. Finally, we identify candidate EWS-WT1 target genes with potential therapeutic implications, including CCND1, whose inhibition by the clinically-approved drug Palbociclib leads to marked tumor burden decrease in DSRCT PDXs in vivo. Taken together, our studies identify gene regulation programs and therapeutic vulnerabilities in DSRCT and provide a mechanistic understanding of the complex oncogenic activity of EWS-WT1.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Chromatin / metabolism
  • Cyclin D1* / genetics
  • Cyclin D1* / metabolism
  • Desmoplastic Small Round Cell Tumor* / drug therapy
  • Desmoplastic Small Round Cell Tumor* / genetics
  • Desmoplastic Small Round Cell Tumor* / metabolism
  • Desmoplastic Small Round Cell Tumor* / pathology
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Gene Regulatory Networks
  • Humans
  • Mice
  • Oncogene Proteins, Fusion* / genetics
  • Oncogene Proteins, Fusion* / metabolism
  • Piperazines / pharmacology
  • Protein Isoforms* / genetics
  • Protein Isoforms* / metabolism
  • Pyridines* / pharmacology
  • RNA-Binding Protein EWS* / genetics
  • RNA-Binding Protein EWS* / metabolism
  • WT1 Proteins / genetics
  • WT1 Proteins / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Oncogene Proteins, Fusion
  • RNA-Binding Protein EWS
  • Pyridines
  • Protein Isoforms
  • Cyclin D1
  • Piperazines
  • palbociclib
  • WT1 Proteins
  • CCND1 protein, human
  • EWS1-WT1 fusion protein, human
  • Chromatin
  • WT1 protein, human