SOX10 mediates glioblastoma cell-state plasticity

EMBO Rep. 2024 Nov;25(11):5113-5140. doi: 10.1038/s44319-024-00258-8. Epub 2024 Sep 16.

Abstract

Phenotypic plasticity is a cause of glioblastoma therapy failure. We previously showed that suppressing the oligodendrocyte-lineage regulator SOX10 promotes glioblastoma progression. Here, we analyze SOX10-mediated phenotypic plasticity and exploit it for glioblastoma therapy design. We show that low SOX10 expression is linked to neural stem-cell (NSC)-like glioblastoma cell states and is a consequence of temozolomide treatment in animal and cell line models. Single-cell transcriptome profiling of Sox10-KD tumors indicates that Sox10 suppression is sufficient to induce tumor progression to an aggressive NSC/developmental-like phenotype, including a quiescent NSC-like cell population. The quiescent NSC state is induced by temozolomide and Sox10-KD and reduced by Notch pathway inhibition in cell line models. Combination treatment using Notch and HDAC/PI3K inhibitors extends the survival of mice carrying Sox10-KD tumors, validating our experimental therapy approach. In summary, SOX10 suppression mediates glioblastoma progression through NSC/developmental cell-state transition, including the induction of a targetable quiescent NSC state. This work provides a rationale for the design of tumor therapies based on single-cell phenotypic plasticity analysis.

Keywords: SOX10; Glioblastoma; Phenotypic Plasticity; Therapy Resistance; Tumor Cell Quiescence.

MeSH terms

  • Animals
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Plasticity / drug effects
  • Cell Plasticity / genetics
  • Gene Expression Regulation, Neoplastic
  • Glioblastoma* / genetics
  • Glioblastoma* / metabolism
  • Glioblastoma* / pathology
  • Humans
  • Mice
  • Neural Stem Cells / drug effects
  • Neural Stem Cells / metabolism
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism
  • SOXE Transcription Factors* / genetics
  • SOXE Transcription Factors* / metabolism
  • Signal Transduction
  • Single-Cell Analysis
  • Temozolomide* / pharmacology

Substances

  • SOXE Transcription Factors
  • Temozolomide
  • SOX10 protein, human
  • Receptors, Notch