Loss of Smarc proteins impairs cerebellar development

J Neurosci. 2014 Oct 1;34(40):13486-91. doi: 10.1523/JNEUROSCI.2560-14.2014.

Abstract

SMARCA4 (BRG1) and SMARCB1 (INI1) are tumor suppressor genes that are crucially involved in the formation of malignant rhabdoid tumors, such as atypical teratoid/rhabdoid tumor (AT/RT). AT/RTs typically affect infants and occur at various sites of the CNS with a particular frequency in the cerebellum. Here, granule neurons and their progenitors represent the most abundant cell type and are known to give rise to a subset of medulloblastoma, a histologically similar embryonal brain tumor. To test how Smarc proteins influence the development of granule neurons and whether this population may serve as cellular origin for AT/RTs, we specifically deleted Smarca4 and Smarcb1 in cerebellar granule cell precursors. Respective mutant mice displayed severe ataxia and motor coordination deficits, but did not develop any tumors. In fact, they suffered from a severely hypoplastic cerebellum due to a significant inhibition of granule neuron precursor proliferation. Molecularly, this was accompanied by an enhanced activity of Wnt/β-catenin signaling that, by itself, is known to cause a nearly identical phenotype. We further used an hGFAP-cre allele, which deleted Smarcb1 much earlier and in a wider neural precursor population, but we still did not detect any tumor formation in the CNS. In summary, our results emphasize cell-type-dependent roles of Smarc proteins and argue against cerebellar granule cells and other progeny of hGFAP-positive neural precursors as the cellular origin for AT/RTs.

Keywords: AT/RT; Smarc; brain; cerebellum; development; tumor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Age Factors
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cell Proliferation / genetics
  • Cells, Cultured
  • Cerebellum / cytology
  • Cerebellum / growth & development*
  • Chromosomal Proteins, Non-Histone / deficiency*
  • Chromosomal Proteins, Non-Histone / genetics
  • DNA Helicases / deficiency*
  • DNA Helicases / genetics
  • Flow Cytometry
  • Gene Expression Regulation, Developmental / genetics*
  • Glial Fibrillary Acidic Protein / metabolism
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Mice
  • Mice, Transgenic
  • Mutation / genetics
  • Neural Stem Cells / physiology
  • Neurons / metabolism
  • Nuclear Proteins / deficiency*
  • Nuclear Proteins / genetics
  • Phosphopyruvate Hydratase / metabolism
  • SMARCB1 Protein
  • Signal Transduction / genetics
  • Transcription Factors / deficiency*
  • Transcription Factors / genetics
  • Wnt Proteins / metabolism

Substances

  • Atoh1 protein, mouse
  • Basic Helix-Loop-Helix Transcription Factors
  • Chromosomal Proteins, Non-Histone
  • Glial Fibrillary Acidic Protein
  • Nuclear Proteins
  • SMARCB1 Protein
  • Smarcb1 protein, mouse
  • Transcription Factors
  • Wnt Proteins
  • Green Fluorescent Proteins
  • Smarca4 protein, mouse
  • DNA Helicases
  • Phosphopyruvate Hydratase