PUBLICATION

Absence of an external germinal layer in zebrafish and shark reveals a distinct, anamniote ground plan of cerebellum development

Authors
Chaplin, N., Tendeng, C., and Wingate, R.J.
ID
ZDB-PUB-100302-10
Date
2010
Source
The Journal of neuroscience : the official journal of the Society for Neuroscience   30(8): 3048-3057 (Journal)
Registered Authors
Tendeng, Christian
Keywords
none
MeSH Terms
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors/genetics
  • Basic Helix-Loop-Helix Transcription Factors/metabolism
  • Biological Evolution
  • Brain Mapping
  • Cell Differentiation/genetics
  • Cell Lineage/genetics
  • Cell Movement/genetics
  • Cell Proliferation
  • Cerebellum/cytology
  • Cerebellum/embryology*
  • Dogfish/embryology
  • Evolution, Molecular
  • Gene Expression Regulation, Developmental/genetics
  • Neurogenesis/genetics*
  • Neurons/cytology
  • Neurons/metabolism
  • Organogenesis/genetics*
  • Phylogeny
  • Rhombencephalon/cytology
  • Rhombencephalon/embryology
  • Sharks/embryology*
  • Species Specificity
  • Stem Cells/cytology
  • Stem Cells/metabolism*
  • Zebrafish/embryology*
  • Zebrafish Proteins/genetics
  • Zebrafish Proteins/metabolism
PubMed
20181601 Full text @ J. Neurosci.
Abstract
The granule cell layer of the cerebellum comprises the largest population of neurons in the vertebrate CNS. In amniotes, its precursors undergo a unique phase of transit amplification, regulated by Sonic hedgehog. They do so within a prominent but transient secondary proliferative epithelium, the external germinal layer, which is formed by tangential migration of precursor cells from the rhombic lip. This behavior is a hallmark of bird and mammal cerebellum development. Despite its significance for both development and disease, it is unclear whether an external germinal layer is a requirement for granule cell production or an expedient of transit amplification. Evidence for its existence in more basal vertebrates is contradictory. We therefore examined cerebellum development in the zebrafish, specifically in relation to the expression of the basic helix-loop-helix gene Atonal 1, which definitively characterizes granule cell precursors. The expression of Atoh1a-Atoh1c, in combination with patterns of proliferation and fate maps, define precursor pools at the rhombic lip and cerebellar midline but demonstrate that an external germinal layer is absent. Sonic hedgehog signaling is correspondingly absent in the zebrafish cerebellum. Sustained roof-plate-derived signals suggest that, in the absence of transit amplification, primary granule cell precursor pools are maintained throughout development. To determine whether this pattern is specific to zebrafish or reflects a more general anamniote organization, we examined the expression of similar genes in the dogfish, Scylliorhinus canicula. We show that these anamniotes share a common ground plan of granule cell production that does not include an external germinal layer.
Genes / Markers
Figures
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Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping