Coordinating cell and tissue behavior during zebrafish neural tube morphogenesis

Abstract

The development of a vertebrate neural epithelium with well-organized apico-basal polarity and a central lumen is essential for its proper function. However, how this polarity is established during embryonic development and the potential influence of surrounding signals and tissues on such organization has remained less understood. In recent years the combined superior transparency and genetics of the zebrafish embryo has allowed for in vivo visualization and quantification of the cellular and molecular dynamics that govern neural tube structure. Here, we discuss recent studies revealing how co-ordinated cell-cell interactions coupled with adjacent tissue dynamics are critical to regulate final neural tissue architecture. Furthermore, new findings show how the spatial regulation and timing of orientated cell division is key in defining precise lumen formation at the tissue midline. In addition, we compare zebrafish neurulation with that of amniotes and amphibians in an attempt to understand the conserved cellular mechanisms driving neurulation and resolve the apparent differences among animals. Zebrafish neurulation not only offers fundamental insights into early vertebrate brain development but also the opportunity to explore in vivo cell and tissue dynamics during complex three-dimensional animal morphogenesis. Developmental Dynamics 245:197-208, 2016. V C 2015 Wiley Periodicals, Inc.

Planar cell polarity in moving cells: think globally, act locally

“…Pk and Vangl localize together at the level of AJs on anterior membranes in the frog neural plate (Ossipova et al, 2015b). In the fish, in which maturation of the apical surface of neuroepithelial progenitors is delayed (Araya et al, 2016), Pk and Vangl2 localize asymmetrically to the anterior side of immature progenitors (Ciruna et al, 2006;Roszko et al, 2015) and are subsequently recruited to anterior AJs (Davey et al, 2016). The Flamingo homolog Celsr1 localizes to both anterior and posterior AJs, a localization that is particularly apparent when cells become aligned along the mediolateral axis of the chick neural plate (Nishimura et al, 2012) (Fig.…”

Contributions of the chick embryo and experimental embryology to understanding the cellular mechanisms of neurulation

“…However, cooling embryos to 4 0 C after the neural plate cells have elongated (or treating embryos with chemicals that disrupt microtubules, such as colchicine or nocodazole), a process that depolymerizes microtubules, decreases cell heights by about 25% (Schoenwolf and Powers, 1987), suggesting that microtubules are the main driver of cell elongation during shaping of the neural plate. Similarly, cell elongation during neural keel formation in the zebrafish depends heavily on microtubules (Araya et al, 2016;Minc et al, 2009). Thus, the second premise of the classical model for neural plate shaping (that apicobasal cell elongation during neural plate formation is driven at least in large part by microtubules) is also valid for both chick and zebrafish embryos.…”

Delta/Notch signaling controls neuroepithelial morphogenesis in the zebrafish spinal cord

“…In contrast to tetrapods, the initial stages of zebrafish spinal cord morphogenesis take place in a neural primordium that lacks a polarized epithelial architecture [17][18][19][20][21] . While the cellular organization of the zebrafish neural plate displays similarities to the pseudostratified epithelium of higher vertebrates 14,18,21,22 , major signs of apico-basal polarity such as apical Par protein localization, adherens junctions and tight junctions appear only by mid-segmentation stages, when neurogenesis is well under way [17][18][19][20][21]23 . This raises the question whether and how Notch signaling and neuroepithelial morphogenesis are linked during zebrafish neural development?…”

“…A second particularity of the development of the zebrafish is the occurrence of a particular type of morphogenetic cell division 17,18,20,24 . In C-divisions, a cell originating from one side of the neural primordium divides at the embryonic midline so that one of its daughters integrates the contralateral half 17,20,24 .…”

“…Neural primordia in which cell divisions have been blocked establish apico-basal polarity, but fail to form a straight, regular tube apical neural tube midline 25 . It has therefore been suggested that C-divisions, while not being absolutely required for the establishment of neural tube apico-basal polarity, confer a morphogenetic advantage to the embryo by relocating cells that would otherwise span the neural tube midline 18,21,25 . Despite the fact that Cdivisions confer robustness to neural tube development, their regulation remains poorly understood.…”