Stretching morphogenesis of the roof plate and formation of the central canal

PLoS One. 2013;8(2):e56219. doi: 10.1371/journal.pone.0056219. Epub 2013 Feb 7.

Abstract

Background: Neurulation is driven by apical constriction of actomyosin cytoskeleton resulting in conversion of the primitive lumen into the central canal in a mechanism driven by F-actin constriction, cell overcrowding and buildup of axonal tracts. The roof plate of the neural tube acts as the dorsal morphogenetic center and boundary preventing midline crossing by neural cells and axons.

Methodology/principal findings: The roof plate zebrafish transgenics expressing cytosolic GFP were used to study and describe development of this structure in vivo for a first time ever. The conversion of the primitive lumen into the central canal causes significant morphogenetic changes of neuroepithelial cells in the dorsal neural tube. We demonstrated that the roof plate cells stretch along the D-V axis in parallel with conversion of the primitive lumen into central canal and its ventral displacement. Importantly, the stretching of the roof plate is well-coordinated along the whole spinal cord and the roof plate cells extend 3× in length to cover 2/3 of the neural tube diameter. This process involves the visco-elastic extension of the roof place cytoskeleton and depends on activity of Zic6 and the Rho-associated kinase (Rock). In contrast, stretching of the floor plate is much less extensive.

Conclusions/significance: The extension of the roof plate requires its attachment to the apical complex of proteins at the surface of the central canal, which depends on activity of Zic6 and Rock. The D-V extension of the roof plate may change a range and distribution of morphogens it produces. The resistance of the roof plate cytoskeleton attenuates ventral displacement of the central canal in illustration of the novel mechanical role of the roof plate during development of the body axis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / embryology
  • Embryo, Nonmammalian / metabolism
  • Green Fluorescent Proteins / genetics
  • Morphogenesis*
  • Neural Tube / cytology
  • Neural Tube / embryology*
  • Neural Tube / metabolism
  • Repressor Proteins / metabolism
  • Spinal Cord / cytology
  • Spinal Cord / embryology*
  • Spinal Cord / metabolism
  • Zebrafish / embryology

Substances

  • Repressor Proteins
  • Zic6 protein, zebrafish
  • Green Fluorescent Proteins

Grants and funding

This work was supported by the grant of the Agency for Science, Technology and Research (A-STAR) of Singapore. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.