Sleeping Beauty Insertional Mutagenesis Reveals Important Genetic Drivers of Central Nervous System Embryonal Tumors

Cancer Res. 2019 Mar 1;79(5):905-917. doi: 10.1158/0008-5472.CAN-18-1261. Epub 2019 Jan 23.

Abstract

Medulloblastoma and central nervous system primitive neuroectodermal tumors (CNS-PNET) are aggressive, poorly differentiated brain tumors with limited effective therapies. Using Sleeping Beauty (SB) transposon mutagenesis, we identified novel genetic drivers of medulloblastoma and CNS-PNET. Cross-species gene expression analyses classified SB-driven tumors into distinct medulloblastoma and CNS-PNET subgroups, indicating they resemble human Sonic hedgehog and group 3 and 4 medulloblastoma and CNS neuroblastoma with FOXR2 activation. This represents the first genetically induced mouse model of CNS-PNET and a rare model of group 3 and 4 medulloblastoma. We identified several putative proto-oncogenes including Arhgap36, Megf10, and Foxr2. Genetic manipulation of these genes demonstrated a robust impact on tumorigenesis in vitro and in vivo. We also determined that FOXR2 interacts with N-MYC, increases C-MYC protein stability, and activates FAK/SRC signaling. Altogether, our study identified several promising therapeutic targets in medulloblastoma and CNS-PNET. SIGNIFICANCE: A transposon-induced mouse model identifies several novel genetic drivers and potential therapeutic targets in medulloblastoma and CNS-PNET.

Publication types

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

MeSH terms

  • Animals
  • Brain Neoplasms / genetics*
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology
  • Cell Transformation, Neoplastic / genetics
  • Cerebellar Neoplasms / genetics*
  • Cerebellar Neoplasms / metabolism
  • Cerebellar Neoplasms / pathology
  • DNA Transposable Elements / genetics
  • Female
  • Forkhead Transcription Factors / genetics
  • GTPase-Activating Proteins / biosynthesis
  • GTPase-Activating Proteins / genetics
  • Humans
  • Male
  • Medulloblastoma / genetics*
  • Medulloblastoma / metabolism
  • Medulloblastoma / pathology
  • Membrane Proteins / genetics
  • Mice
  • Mice, Nude
  • Mutagenesis, Insertional / methods
  • Neural Stem Cells / metabolism
  • Neural Stem Cells / pathology
  • Neuroectodermal Tumors, Primitive / genetics*
  • Neuroectodermal Tumors, Primitive / metabolism
  • Neuroectodermal Tumors, Primitive / pathology
  • Prognosis

Substances

  • ARHGAP36 protein, human
  • DNA Transposable Elements
  • FOXR2 protein, human
  • Forkhead Transcription Factors
  • Foxr2 protein, mouse
  • GTPase-Activating Proteins
  • MEGF10, human
  • Megf10 protein, mouse
  • Membrane Proteins