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    Area of Science:

    • Neuro-oncology
    • Developmental biology
    • Epigenetics

    Background:

    • ZFTA-RELA gene fusions are the most common genetic alteration in pediatric supratentorial ependymoma (EPN).
    • This fusion protein is sufficient to initiate tumor formation in mice, but its specific cellular targets during development remain unclear.

    Purpose of the Study:

    • To identify specific developmental cell lineage programs at risk of transformation by ZFTA-RELA.
    • To investigate the role of developmental chromatin accessibility in ZFTA-RELA driven ependymoma.

    Main Methods:

    • Combined single-cell ATAC and RNA-seq (scMultiome) analysis of developing mouse forebrain and ZFTA-RELA driven mouse and human ependymoma.
    • In vivo lineage tracing studies.

    Main Results:

    • Specific developmental lineage programs in radial glial cells, regulated by Plagl transcription factors, are susceptible to neoplastic transformation.
    • ZFTA-RELA binding leads to persistent chromatin accessibility and oncogene expression at specific loci.
    • Cross-species analysis revealed cell type heterogeneity in EPN, with intermediate progenitor-like cells forming a tumor hierarchy.
    • Dominant neoplastic clones were identified that drive tumor growth and establish the entire cellular hierarchy.

    Conclusions:

    • Developmental epigenomic states are critical for fusion oncoprotein-driven transformation in pediatric ependymoma.
    • Distinct lineage differentiation programs, influenced by chromatin accessibility, dictate oncogenic transformation risk.
    • Early progenitor-like cells establish the EPN tumor hierarchy, mirroring normal neural differentiation.