Comprehensive Transcriptomic Analysis of EWSR1::WT1 Targets Identifies CDK4/6 Inhibitors as an Effective Therapy for Desmoplastic Small Round Cell Tumors

Cancer Res. 2024 May 2;84(9):1426-1442. doi: 10.1158/0008-5472.CAN-23-3334.

Abstract

Desmoplastic small round cell tumors (DSRCT) are a type of aggressive, pediatric sarcoma characterized by the EWSR1::WT1 fusion oncogene. Targeted therapies for DSRCT have not been developed, and standard multimodal therapy is insufficient, leading to a 5-year survival rate of only 15% to 25%. Here, we depleted EWSR1::WT1 in DSRCT and established its essentiality in vivo. Transcriptomic analysis revealed that EWSR1::WT1 induces unique transcriptional alterations compared with WT1 and other fusion oncoproteins and that EWSR1::WT1 binding directly mediates gene upregulation. The E-KTS isoform of EWSR1::WT1 played a dominant role in transcription, and it bound to the CCND1 promoter and stimulated DSRCT growth through the cyclin D-CDK4/6-RB axis. Treatment with the CDK4/6 inhibitor palbociclib successfully reduced growth in two DSRCT xenograft models. As palbociclib has been approved by the FDA for the treatment of breast cancer, these findings demonstrate the sensitivity of DSRCT to palbociclib and support immediate clinical investigation of palbociclib for treating this aggressive pediatric cancer.

Significance: EWSR1::WT1 is essential for desmoplastic small round cell tumors and upregulates the cyclin D-CDK4/6-RB axis that can be targeted with palbociclib, providing a targeted therapeutic strategy for treating this deadly tumor type.

Publication types

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

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cyclin-Dependent Kinase 4* / antagonists & inhibitors
  • Cyclin-Dependent Kinase 4* / genetics
  • Cyclin-Dependent Kinase 6* / antagonists & inhibitors
  • Cyclin-Dependent Kinase 6* / genetics
  • 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
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Mice
  • Mice, Inbred NOD
  • Oncogene Proteins, Fusion* / genetics
  • Oncogene Proteins, Fusion* / metabolism
  • Piperazines* / pharmacology
  • Piperazines* / therapeutic use
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use
  • Pyridines* / pharmacology
  • Pyridines* / therapeutic use
  • RNA-Binding Protein EWS* / genetics
  • RNA-Binding Protein EWS* / metabolism
  • WT1 Proteins / genetics
  • WT1 Proteins / metabolism
  • Xenograft Model Antitumor Assays*

Substances

  • CDK4 protein, human
  • CDK6 protein, human
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6
  • EWSR1 protein, human
  • Oncogene Proteins, Fusion
  • palbociclib
  • Piperazines
  • Protein Kinase Inhibitors
  • Pyridines
  • RNA-Binding Protein EWS
  • WT1 protein, human
  • WT1 Proteins