Stepwise Maturation of Apicobasal Polarity of the Neuroepithelium Is Essential for Vertebrate Neurulation

Abstract

During vertebrate neurulation, extensive cell movements transform the flat neural plate into the neural tube. This dynamic morphogenesis requires the tissue to bear a certain amount of plasticity to accommodate shape and position changes of individual cells as well as intercellular cohesiveness to maintain tissue integrity and architecture. For most of the neural plate-neural tube transition, cells are polarized along the apicobasal axis. The establishment and maintenance of this polarity requires many polarity proteins that mediate cell-cell adhesion either directly or indirectly. Intercellular adhesion reduces tissue plasticity and enhances tissue integrity. However, it remains unclear how apicobasal polarity is regulated to meet the opposing needs for tissue plasticity and tissue integrity during neurulation. Here, we show that N-Cad/ZO-1 complex-initiated apicobasal polarity is stabilized by the late-onsetting Lin7c/Nok complex after the extensive morphogenetic cell movements in neurulation. Loss of either N-Cad or Lin7c disrupts neural tube formation. Furthermore, precocious overexpression of Lin7c induces multiaxial mirror symmetry in zebrafish neurulation. Our data suggest that stepwise maturation of apicobasal polarity plays an essential role in vertebrate neurulation.

Bone morphogenetic proteins regulate neural tube closure by interacting with the apicobasal polarity pathway

“…This dynamic modulation of polarity in turn provides the neural plate with the flexibility to bend and shape into a neural tube while maintaining overall epithelial integrity (Bryant and Mostov, 2008). Such partially polarized cells have also been noted in other morphogenetically active epithelia undergoing organogenesis (Ewald et al, 2008;Suzuki et al, 2009;Yang et al, 2009). …”

“…apical constriction, cell cycle progression, apicobasal span) regulated and coordinated during neural tube closure (Copp et al, 2003;Haigo et al, 2003;Nishimura and Takeichi, 2008;Yang et al, 2009)? Recently, the coordinated bending of epithelial sheets into complex organs has been attributed to the dynamic regulation of apicobasal epithelial polarity (Andrew and Ewald, 2010;Bryant and Mostov, 2008).…”

“…According to these studies, simple epithelial sheets can progressively transform themselves into complex branched tubules by polarized cell divisions and the dynamic shunting of cells through unpolarized, semi-polarized and polarized states (Bryant and Mostov, 2008). In such 'morphogenetically active' epithelia, altering the polarity of a few cells at a time while retaining it in others allows the epithelial sheet to retain its overall integrity while possessing the flexibility to be bent and shaped (Ewald et al, 2008;Yang et al, 2009).…”

Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements

“…Asymmetric centrosome and cilia position in the somitic mesoderm has been observed as early as 14 hpf (10 somite stage) (Barrios et al, 2003;Borovina et al, 2010). Pard3 becomes apically localized by early segmentation stages (six or seven somites, 12 hpf) in cells of the neural tube (Tawk et al, 2007;Hong et al, 2010), accompanied by the tight junction marker ZO-1 (fiveand 10-somite stage, 11.4 and 14 hpf) (Hong and Brewster, 2006;Yang et al, 2009) and polarity component aPKC (12 somites, 15 hpf) (Hong and Brewster, 2006). Furthermore, orientation of the MT cytoskeleton after 12 hpf (Hong et al, 2010) reveals the maturing apicobasal polarity in the neural epithelium.…”

Claudin‐5a in developing zebrafish brain barriers: another brick in the wall

“…The mechanisms of neurulation are similar among all vertebrates and the anterior portion of the neural tube will eventually give rise to the brain, whereas the posterior portion will form the spinal cord. Already prior to neurulation, neuroepithelial cells strongly polarize along their apical-basal axes and establish apically localized adherens and tight junctions along their ventricular surfaces [37,38]. Coherence of neuroepithelial cells via these apical junctional structures is required for the expansion of brain ventricles and for correct morphogenesis of the brain (Fig.…”