Granule neuron precursor cell proliferation is regulated by NFIX and intersectin 1 during postnatal cerebellar development

Brain Struct Funct. 2019 Mar;224(2):811-827. doi: 10.1007/s00429-018-1801-3. Epub 2018 Dec 3.

Abstract

Cerebellar granule neurons are the most numerous neuronal subtype in the central nervous system. Within the developing cerebellum, these neurons are derived from a population of progenitor cells found within the external granule layer of the cerebellar anlage, namely the cerebellar granule neuron precursors (GNPs). The timely proliferation and differentiation of these precursor cells, which, in rodents occurs predominantly in the postnatal period, is tightly controlled to ensure the normal morphogenesis of the cerebellum. Despite this, our understanding of the factors mediating how GNP differentiation is controlled remains limited. Here, we reveal that the transcription factor nuclear factor I X (NFIX) plays an important role in this process. Mice lacking Nfix exhibit reduced numbers of GNPs during early postnatal development, but elevated numbers of these cells at postnatal day 15. Moreover, Nfix-/- GNPs exhibit increased proliferation when cultured in vitro, suggestive of a role for NFIX in promoting GNP differentiation. At a mechanistic level, profiling analyses using both ChIP-seq and RNA-seq identified the actin-associated factor intersectin 1 as a downstream target of NFIX during cerebellar development. In support of this, mice lacking intersectin 1 also displayed delayed GNP differentiation. Collectively, these findings highlight a key role for NFIX and intersectin 1 in the regulation of cerebellar development.

Keywords: Cerebellum; External granular layer; Granule neuron; NFIX.

MeSH terms

  • Adaptor Proteins, Vesicular Transport / genetics
  • Adaptor Proteins, Vesicular Transport / metabolism*
  • Animals
  • Cell Proliferation / physiology*
  • Cerebellum / cytology*
  • Cerebellum / growth & development
  • Cerebellum / metabolism
  • Gene Expression Regulation, Developmental
  • Mice, Knockout
  • NFI Transcription Factors / genetics
  • NFI Transcription Factors / metabolism*
  • Neural Stem Cells / cytology*
  • Neural Stem Cells / metabolism
  • Neurogenesis / physiology
  • Neurons / cytology*
  • Neurons / metabolism

Substances

  • Adaptor Proteins, Vesicular Transport
  • NFI Transcription Factors
  • Nfix protein, mouse
  • intersectin 1