title: Mechanical roles of apical constriction, cell elongation, and cell migration during neural tube formation in Xenopus.
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.
authors.affiliation: Institute for Frontier Medical Sciences, Kyoto University, Kyoto, Japan. inoue@frontier.kyoto-u.ac.jp.
authors.forename: Yasuhiro
authors.initials: Y
authors.lastname: Inoue
authors.affiliation: National Institute for Basic Biology, Okazaki, Aichi, Japan.
authors.forename: Makoto
authors.initials: M
authors.lastname: Suzuki
authors.affiliation: Institute for Frontier Medical Sciences, Kyoto University, Kyoto, Japan.
authors.forename: Tadashi
authors.initials: T
authors.lastname: Watanabe
authors.affiliation: National Institute for Basic Biology, Okazaki, Aichi, Japan.
authors.forename: Naoko
authors.initials: N
authors.lastname: Yasue
authors.affiliation: Institute for Frontier Medical Sciences, Kyoto University, Kyoto, Japan.
authors.forename: Itsuki
authors.initials: I
authors.lastname: Tateo
authors.affiliation: Institute for Frontier Medical Sciences, Kyoto University, Kyoto, Japan.
authors.forename: Taiji
authors.initials: T
authors.lastname: Adachi
authors.affiliation: National Institute for Basic Biology, Okazaki, Aichi, Japan.
authors.forename: Naoto
authors.initials: N
authors.lastname: Ueno
mesh_terms: D000818:Animals; D001696:Biomechanical Phenomena; D002465:Cell Movement; D048430:Cell Shape; D003198:Computer Simulation; D004625:Embryo, Nonmammalian / Q000166:cytology; D008954:Models, Biological; D009024:Morphogenesis; D054259:Neural Tube / Q000166:cytology*; D029867:Xenopus Proteins / Q000378:metabolism; D014982:Xenopus laevis / Q000196:embryology*
chemical_list: D029867:Xenopus Proteins
keywords: 3D vertex simulation; Apical constriction; Cell elongation; Cell migration; Neural tube closure