Mirror-symmetric microtubule assembly and cell interactions drive lumen formation in the zebrafish neural rod

EMBO J. 2013 Jan 9;32(1):30-44. doi: 10.1038/emboj.2012.305. Epub 2012 Nov 30.

Abstract

By analysing the cellular and subcellular events that occur in the centre of the developing zebrafish neural rod, we have uncovered a novel mechanism of cell polarisation during lumen formation. Cells from each side of the neural rod interdigitate across the tissue midline. This is necessary for localisation of apical junctional proteins to the region where cells intersect the tissue midline. Cells assemble a mirror-symmetric microtubule cytoskeleton around the tissue midline, which is necessary for the trafficking of proteins required for normal lumen formation, such as partitioning defective 3 and Rab11a to this point. This occurs in advance and is independent of the midline cell division that has been shown to have a powerful role in lumen organisation. To our knowledge, this is the first example of the initiation of apical polarisation part way along the length of a cell, rather than at a cell extremity. Although the midline division is not necessary for apical polarisation, it confers a morphogenetic advantage by efficiently eliminating cellular processes that would otherwise bridge the developing lumen.

Publication types

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

MeSH terms

  • Animals
  • Body Patterning
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Communication*
  • Cell Division
  • Cell Movement
  • Cell Polarity
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / embryology
  • Green Fluorescent Proteins / chemistry
  • Luminescent Agents / chemistry
  • Microtubules / genetics
  • Microtubules / metabolism*
  • Mutation
  • Neural Tube / cytology
  • Neural Tube / embryology*
  • Neurulation*
  • Nocodazole / pharmacology
  • Protein Transport / drug effects
  • Recombinant Fusion Proteins
  • Tubulin Modulators / pharmacology
  • Zebrafish / anatomy & histology
  • Zebrafish / embryology*
  • Zebrafish / genetics
  • Zebrafish / metabolism
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism*
  • rab GTP-Binding Proteins / genetics
  • rab GTP-Binding Proteins / metabolism

Substances

  • Carrier Proteins
  • Luminescent Agents
  • Recombinant Fusion Proteins
  • Tubulin Modulators
  • Zebrafish Proteins
  • pard3ab protein, zebrafish
  • Green Fluorescent Proteins
  • rab11 protein
  • rab GTP-Binding Proteins
  • Nocodazole