Inactivation of Ezh2 Upregulates Gfi1 and Drives Aggressive Myc-Driven Group 3 Medulloblastoma

Cell Rep. 2017 Mar 21;18(12):2907-2917. doi: 10.1016/j.celrep.2017.02.073.

Abstract

The most aggressive of four medulloblastoma (MB) subgroups are cMyc-driven group 3 (G3) tumors, some of which overexpress EZH2, the histone H3K27 mono-, di-, and trimethylase of polycomb-repressive complex 2. Ezh2 has a context-dependent role in different cancers as an oncogene or tumor suppressor and retards tumor progression in a mouse model of G3 MB. Engineered deletions of Ezh2 in G3 MBs by gene editing nucleases accelerated tumorigenesis, whereas Ezh2 re-expression reversed attendant histone modifications and slowed tumor progression. Candidate oncogenic drivers suppressed by Ezh2 included Gfi1, a proto-oncogene frequently activated in human G3 MBs. Gfi1 disruption antagonized the tumor-promoting effects of Ezh2 loss; conversely, Gfi1 overexpression collaborated with Myc to bypass effects of Trp53 inactivation in driving MB progression in primary cerebellar neuronal progenitors. Although negative regulation of Gfi1 by Ezh2 may restrain MB development, Gfi1 activation can bypass these effects.

Keywords: EZH2; GFI1; Hox genes; MYC; PRC2; SUZ12; enhancer of zeste homology 2; epigenetic repression; group 3 medulloblastoma; growth factor independent 1; histone H3 modification; polycomb-repressive complex 2; suppressor of zeste 12 homolog.

MeSH terms

  • Animals
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Cerebellar Neoplasms / genetics
  • Cerebellar Neoplasms / pathology*
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Disease Progression
  • Enhancer of Zeste Homolog 2 Protein / metabolism*
  • Gene Deletion
  • Gene Expression Regulation, Neoplastic
  • Medulloblastoma / genetics*
  • Medulloblastoma / pathology*
  • Mice, Nude
  • Mutation / genetics
  • Neoplasm Invasiveness
  • Neoplasm Proteins / metabolism
  • Oncogenes
  • Polycomb Repressive Complex 2 / metabolism
  • Protein Binding
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins c-myc / metabolism*
  • Spheroids, Cellular / metabolism
  • Spheroids, Cellular / pathology
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Up-Regulation / genetics*

Substances

  • DNA-Binding Proteins
  • Gfi1 protein, mouse
  • MAS1 protein, human
  • Neoplasm Proteins
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins c-myc
  • SUZ12 protein, human
  • Transcription Factors
  • Enhancer of Zeste Homolog 2 Protein
  • Polycomb Repressive Complex 2