Altered temporal sequence of transcriptional regulators in the generation of human cerebellar granule cells

Elife. 2021 Nov 29:10:e67074. doi: 10.7554/eLife.67074.

Abstract

Brain development is regulated by conserved transcriptional programs across species, but little is known about the divergent mechanisms that create species-specific characteristics. Among brain regions, human cerebellar histogenesis differs in complexity compared with nonhuman primates and rodents, making it important to develop methods to generate human cerebellar neurons that closely resemble those in the developing human cerebellum. We report a rapid protocol for the derivation of the human ATOH1 lineage, the precursor of excitatory cerebellar neurons, from human pluripotent stem cells (hPSCs). Upon transplantation into juvenile mice, hPSC-derived cerebellar granule cells migrated along glial fibers and integrated into the cerebellar cortex. By Translational Ribosome Affinity Purification-seq, we identified an unexpected temporal shift in the expression of RBFOX3 (NeuN) and NEUROD1, which are classically associated with differentiated neurons, in the human outer external granule layer. This molecular divergence may enable the protracted development of the human cerebellum compared to mice.

Keywords: cerebellar granule cells; developmental biology; developmental timing; human; human cerebellum; human pluripotent stem cells; molecular profiling; mouse; quiescent cells; regenerative medicine; stem cells.

Publication types

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

MeSH terms

  • Animals
  • Antigens, Nuclear / genetics*
  • Antigens, Nuclear / metabolism
  • Basic Helix-Loop-Helix Transcription Factors / genetics*
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cell Line
  • Cerebellum / metabolism*
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mutation
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism

Substances

  • Antigens, Nuclear
  • Basic Helix-Loop-Helix Transcription Factors
  • NEUROD1 protein, human
  • Nerve Tissue Proteins
  • neuronal nuclear antigen NeuN, human

Associated data

  • GEO/GSE163710