ZFIN ID: ZDB-PUB-050328-1
Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products
Lowery, L.A., and Sive, H.
Date: 2005
Source: Development (Cambridge, England)   132(9): 2057-2067 (Journal)
Registered Authors: Lowery, Laura Anne, Sive, Hazel
Keywords: Brain ventricle formation, Brain structure, Circulation, Morphogenesis, Zebrafish, Lumen inflation, snakehead (snk), nagie oko (nok), Neural tube, Epithelial polarity, MAGUK family, Na+K+ ATPase, atp1a1a.1
MeSH Terms:
  • Animals
  • Apoptosis/physiology
  • Blood Circulation/physiology*
  • Cell Proliferation
  • Cerebral Ventricles/embryology*
  • Cerebral Ventricles/physiology
  • Epistasis, Genetic
  • Guanylate Cyclase/genetics*
  • Guanylate Cyclase/metabolism
  • Sodium-Potassium-Exchanging ATPase/genetics*
  • Sodium-Potassium-Exchanging ATPase/metabolism
  • Zebrafish/embryology*
  • Zebrafish Proteins/genetics*
  • Zebrafish Proteins/metabolism
PubMed: 15788456 Full text @ Development
ABSTRACT
The mechanisms by which the vertebrate brain develops its characteristic three-dimensional structure are poorly understood. The brain ventricles are a highly conserved system of cavities that form very early during brain morphogenesis and that are required for normal brain function. We have initiated a study of zebrafish brain ventricle development and show here that the neural tube expands into primary forebrain, midbrain and hindbrain ventricles rapidly, over a 4-hour window during mid-somitogenesis. Circulation is not required for initial ventricle formation, only for later expansion. Cell division rates in the neural tube surrounding the ventricles are higher than between ventricles and, consistently, cell division is required for normal ventricle development. Two zebrafish mutants that do not develop brain ventricles are snakehead and nagie oko. We show that snakehead is allelic to small heart, which has a mutation in the Na(+)K(+) ATPase gene atp1a1a.1. The snakehead neural tube undergoes normal ventricle morphogenesis; however, the ventricles do not inflate, probably owing to impaired ion transport. By contrast, mutants in nagie oko, which was previously shown to encode a MAGUK family protein, fail to undergo ventricle morphogenesis. This correlates with an abnormal brain neuroepithelium, with no clear midline and disrupted junctional protein expression. This study defines three steps that are required for brain ventricle development and that occur independently of circulation: (1) morphogenesis of the neural tube, requiring nok function; (2) lumen inflation requiring atp1a1a.1 function; and (3) localized cell proliferation. We suggest that mechanisms of brain ventricle development are conserved throughout the vertebrates.
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