Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
Biomech Model Mechanobiol
2016 Dec 01;156:1733-1746. doi: 10.1007/s10237-016-0794-1.
Show Gene links
Show Anatomy links
Mechanical roles of apical constriction, cell elongation, and cell migration during neural tube formation in Xenopus.
Inoue Y
,
Suzuki M
,
Watanabe T
,
Yasue N
,
Tateo I
,
Adachi T
,
Ueno N
.
???displayArticle.abstract??? Neural tube closure is an important and necessary process during the development of the central nervous system. The formation of the neural tube structure from a flat sheet of neural epithelium requires several cell morphogenetic events and tissue dynamics to account for the mechanics of tissue deformation. Cell elongation changes cuboidal cells into columnar cells, and apical constriction then causes them to adopt apically narrow, wedge-like shapes. In addition, the neural plate in Xenopus is stratified, and the non-neural cells in the deep layer (deep cells) pull the overlying superficial cells, eventually bringing the two layers of cells to the midline. Thus, neural tube closure appears to be a complex event in which these three physical events are considered to play key mechanical roles. To test whether these three physical events are mechanically sufficient to drive neural tube formation, we employed a three-dimensional vertex model and used it to simulate the process of neural tube closure. The results suggest that apical constriction cued the bending of the neural plate by pursing the circumference of the apical surface of the neural cells. Neural cell elongation in concert with apical constriction further narrowed the apical surface of the cells and drove the rapid folding of the neural plate, but was insufficient for complete neural tube closure. Migration of the deep cells provided the additional tissue deformation necessary for closure. To validate the model, apical constriction and cell elongation were inhibited in Xenopus laevis embryos. The resulting cell and tissue shapes resembled the corresponding simulation results.
Fig. 1.
a Initial shape of the double-layered ectoderm for simulations. The neural and non-neural cells are hexagonally packed in superficial and deep layers, with the superficial neural cells displayed in white. The basic energy function Λhw=H/W
Fig. 2. Different combinations of the physical events during neural tube closure examined using a model I, b model II, and c model III are shown as snapshots over time. The migrating cells are outside of the visualized area except Λhw, as a function of time t
Fig. 3. Shapes of control, and MID1/2 and Shroom3 inhibited (AC/EL inhibition) embryos observed in silico and in vivo. Mediolateral cross-sectional views of the neural tissue shape at time t=0.58, which are compared with the experimental values. m, n The experimental values of those ratios at stage 16
Fig. 4. Shapes of control, and MID1/2 inhibited (EL inhibition) embryos observed in silico and in vivo. The neural tube closure in the simulations using a model III with Λhw, and i the lumen size in experiments
Fig. 5. Effect of the elastic sheet underneath the deep layer on neural tube shapes were examined with and without cell elongation. Simulation results using model III (control) for a
ke/ks
Fig. 6. Effect of permutation of onset time of the apical constriction (AC), cell elongation (EL), and cell migration (CM) on the neural tube shape. The order of three events is a AC t= 0.00, 0.25, and 0.49, respectively
Clarke,
Role of polarized cell divisions in zebrafish neural tube formation.
2009, Pubmed
Clarke,
Role of polarized cell divisions in zebrafish neural tube formation.
2009,
Pubmed
Colas,
Towards a cellular and molecular understanding of neurulation.
2001,
Pubmed
Davidson,
Neural tube closure in Xenopus laevis involves medial migration, directed protrusive activity, cell intercalation and convergent extension.
1999,
Pubmed
,
Xenbase
Eiraku,
Self-organizing optic-cup morphogenesis in three-dimensional culture.
2011,
Pubmed
,
Xenbase
Haigo,
Shroom induces apical constriction and is required for hingepoint formation during neural tube closure.
2003,
Pubmed
,
Xenbase
Harrington,
Comparative analysis of neurulation: first impressions do not count.
2009,
Pubmed
Hirashima,
Pattern formation of an epithelial tubule by mechanical instability during epididymal development.
2014,
Pubmed
Honda,
A three-dimensional vertex dynamics cell model of space-filling polyhedra simulating cell behavior in a cell aggregate.
2004,
Pubmed
Honda,
Computer simulation of emerging asymmetry in the mouse blastocyst.
2008,
Pubmed
Honda,
Two different mechanisms of planar cell intercalation leading to tissue elongation.
2008,
Pubmed
Lee,
Shroom family proteins regulate gamma-tubulin distribution and microtubule architecture during epithelial cell shape change.
2007,
Pubmed
,
Xenbase
Lowery,
Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation.
2004,
Pubmed
Morita,
Cell movements of the deep layer of non-neural ectoderm underlie complete neural tube closure in Xenopus.
2012,
Pubmed
,
Xenbase
Nishimura,
Planar cell polarity links axes of spatial dynamics in neural-tube closure.
2012,
Pubmed
Okamoto,
TAG-1-assisted progenitor elongation streamlines nuclear migration to optimize subapical crowding.
2013,
Pubmed
Okuda,
Vertex dynamics simulations of viscosity-dependent deformation during tissue morphogenesis.
2015,
Pubmed
Okuda,
Apical contractility in growing epithelium supports robust maintenance of smooth curvatures against cell-division-induced mechanical disturbance.
2013,
Pubmed
Okuda,
Reversible network reconnection model for simulating large deformation in dynamic tissue morphogenesis.
2013,
Pubmed
Ossipova,
Planar polarization of Vangl2 in the vertebrate neural plate is controlled by Wnt and Myosin II signaling.
2015,
Pubmed
,
Xenbase
Sawyer,
Apical constriction: a cell shape change that can drive morphogenesis.
2010,
Pubmed
,
Xenbase
Schneider,
NIH Image to ImageJ: 25 years of image analysis.
2012,
Pubmed
Schoenwolf,
Mechanisms of neurulation: traditional viewpoint and recent advances.
1990,
Pubmed
Schroeder,
Neurulation in Xenopus laevis. An analysis and model based upon light and electron microscopy.
1970,
Pubmed
,
Xenbase
Suzuki,
MID1 and MID2 are required for Xenopus neural tube closure through the regulation of microtubule organization.
2010,
Pubmed
,
Xenbase
Suzuki,
Molecular mechanisms of cell shape changes that contribute to vertebrate neural tube closure.
2012,
Pubmed
Ueno,
Planar cell polarity genes and neural tube closure.
2003,
Pubmed
,
Xenbase
Wallingford,
Neural tube closure requires Dishevelled-dependent convergent extension of the midline.
2002,
Pubmed
,
Xenbase