Cancer-specific epigenome identifies oncogenic hijacking by nuclear factor I family proteins for medulloblastoma progression

Dev Cell. 2024 Sep 9;59(17):2302-2319.e12. doi: 10.1016/j.devcel.2024.05.013. Epub 2024 Jun 3.

Abstract

Normal cells coordinate proliferation and differentiation by precise tuning of gene expression based on the dynamic shifts of the epigenome throughout the developmental timeline. Although non-mutational epigenetic reprogramming is an emerging hallmark of cancer, the epigenomic shifts that occur during the transition from normal to malignant cells remain elusive. Here, we capture the epigenomic changes that occur during tumorigenesis in a prototypic embryonal brain tumor, medulloblastoma. By comparing the epigenomes of the different stages of transforming cells in mice, we identify nuclear factor I family of transcription factors, known to be cell fate determinants in development, as oncogenic regulators in the epigenomes of precancerous and cancerous cells. Furthermore, genetic and pharmacological inhibition of NFIB validated a crucial role of this transcription factor by disrupting the cancer epigenome in medulloblastoma. Thus, this study exemplifies how epigenomic changes contribute to tumorigenesis via non-mutational mechanisms involving developmental transcription factors.

Keywords: brain tumor; cerebellar granule cell; cerebellum; epigenome; medulloblastoma; mouse model; nuclear factor I.

MeSH terms

  • Animals
  • Carcinogenesis / genetics
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Cell Differentiation / genetics
  • Cell Proliferation / genetics
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / metabolism
  • Cerebellar Neoplasms / genetics
  • Cerebellar Neoplasms / metabolism
  • Cerebellar Neoplasms / pathology
  • Disease Progression
  • Epigenesis, Genetic
  • Epigenome*
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Medulloblastoma* / genetics
  • Medulloblastoma* / metabolism
  • Medulloblastoma* / pathology
  • Mice
  • NFI Transcription Factors* / genetics
  • NFI Transcription Factors* / metabolism

Substances

  • NFI Transcription Factors
  • Nfib protein, mouse