Sequential Contraction and Exchange of Apical Junctions Drives Zippering and Neural Tube Closure in a Simple Chordate

• Published in: Developmental cell 2015-01, Vol.32 (2), p.241-255
• Main Authors: Hashimoto, Hidehiko, Robin, Francois B., Sherrard, Kristin M., Munro, Edwin M.
• Format: Article
• Language: English
• Subjects: Animals; Cell Differentiation - physiology; Cell Polarity - physiology; Chordata; Ciona intestinalis - metabolism; Intercellular Junctions - metabolism; Intercellular Junctions - pathology; Life Sciences; Neural Crest - cytology; Neural Tube - cytology
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2014.12.017

Unidirectional zippering is a key step in neural tube closure that remains poorly understood. Here, we combine experimental and computational approaches to identify the mechanism for zippering in a basal chordate, Ciona intestinalis. We show that myosin II is activated sequentially from posterior to anterior along the neural/epidermal (Ne/Epi) boundary just ahead of the advancing zipper. This promotes rapid shortening of Ne/Epi junctions, driving the zipper forward and drawing the neural folds together. Cell contact rearrangements (Ne/Epi + Ne/Epi → Ne/Ne + Epi/Epi) just behind the zipper lower tissue resistance to zipper progression by allowing transiently stretched cells to detach and relax toward isodiametric shapes. Computer simulations show that measured differences in junction tension, timing of primary contractions, and delay before cell detachment are sufficient to explain the speed and direction of zipper progression and highlight key advantages of a sequential contraction mechanism for robust efficient zippering. •Unidirectional zippering is required for neural tube closure•Sequential activation of junctional myosin drives posterior-to-anterior zippering•Local coupling of junction shortening and rearrangement makes zippering directional•Computer simulations support the sufficiency of a sequential contraction mechanism Neural tube closure is a critical morphogenetic process in chordate embryonic development. Combining experimental analysis and computer simulation, Hashimoto, Robin, et al. show how local myosin activation and junctional rearrangements together produce directional zippering to drive neural tube closure in a basal chordate. Similar mechanisms may operate in vertebrate neurulation.