PUBLICATION

Origin of Ewing sarcoma by embryonic reprogramming of neural crest to mesoderm

Authors
Vasileva, E., Arata, C., Luo, Y., Burgos, R., Crump, J.G., Amatruda, J.F.
ID
ZDB-PUB-251011-10
Date
2025
Source
Cell Reports : 116376116376 (Journal)
Registered Authors
Amatruda, James F., Crump, Gage DeKoeyer, Vasileva, Elena
Keywords
CP: Cancer, CP: Developmental biology, ETS factors, Ewing sarcoma, cell reprogramming, development, fin development, mesoderm, neural crest cells, pediatric oncology, single-cell analysis, zebrafish genetic models
Datasets
GEO:GSE280398, GEO:GSE306234
MeSH Terms
  • Animals
  • Cellular Reprogramming*
  • Humans
  • Mesoderm*/embryology
  • Mesoderm*/metabolism
  • Mesoderm*/pathology
  • Neural Crest*/embryology
  • Neural Crest*/metabolism
  • Neural Crest*/pathology
  • Oncogene Proteins, Fusion/genetics
  • Oncogene Proteins, Fusion/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*/metabolism
  • Sarcoma, Ewing*/pathology
  • Zebrafish/embryology
  • Zebrafish/genetics
  • Zebrafish Proteins/genetics
  • Zebrafish Proteins/metabolism
PubMed
41072418 Full text @ Cell Rep.
Abstract
Ewing sarcoma is a malignant small round blue cell tumor caused by chromosomal translocations that generate aberrant fusion oncogenes, most frequently EWSR1::FLI1. The cell of origin and mechanisms of EWSR1::FLI1-driven transformation have remained unresolved, largely due to the lack of a representative animal model. Using a zebrafish genetic Ewing sarcoma model, we provide evidence for a neural crest origin of this cancer. Neural crest-derived cells uniquely tolerate expression of EWSR1::FLI1, and targeted expression of EWSR1::FLI1 in these cells generates lethal Ewing sarcomas. Single-cell analysis of tumor initiation shows that EWSR1::FLI1 reprograms neural crest-derived cells to a mesoderm-like state, strikingly resulting in ectopic fins throughout the body. By profiling chromatin accessibility and genome-wide EWSR1::FLI1 binding, we find that the fusion oncogene hijacks developmental enhancers for neural crest to mesoderm reprogramming during cancer initiation. These findings show how a single mutation profoundly alters embryonic cell fate decisions to initiate a devastating childhood cancer.
Genes / Markers
Figures
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Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping