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![Convergent extension and apical constriction in neural tube morphogenesis. (A) Schematic showing how convergent extension drives the narrowing and lengthening of the neural plate. (B) Stills from time-lapse recordings of Xenopus neurula stage embryos expressing membrane-GFP. Dotted lines delineate the boundaries of the neural plate and show narrowing of the neural plate and neural fold movement towards the midline. (C) Schematic showing how apical actomyosin contraction reduces the apical cell surface area to achieve apical constriction and bend an epithelial tissue. (D) Stills from a time-lapse recording from the posterior region of a neurula-stage Xenopus embryo. Arrowheads indicate the contraction of apical actomyosin and reduced apical cell surface area during AC. B and D adapted with permission from [23].](publication/368573218/figure/fig1/AS:11431281120837743@1676650053967/Convergent-extension-and-apical-constriction-in-neural-tube-morphogenesis-A-Schematic.jpg)
Convergent extension and apical constriction in neural tube morphogenesis. (A) Schematic showing how convergent extension drives the narrowing and lengthening of the neural plate. (B) Stills from time-lapse recordings of Xenopus neurula stage embryos expressing membrane-GFP. Dotted lines delineate the boundaries of the neural plate and show narrowing of the neural plate and neural fold movement towards the midline. (C) Schematic showing how apical actomyosin contraction reduces the apical cell surface area to achieve apical constriction and bend an epithelial tissue. (D) Stills from a time-lapse recording from the posterior region of a neurula-stage Xenopus embryo. Arrowheads indicate the contraction of apical actomyosin and reduced apical cell surface area during AC. B and D adapted with permission from [23].
Source publication
The vertebrate brain and spinal cord arise from a common precursor, the neural tube, which forms very early during embryonic development. To shape the forming neural tube, changes in cellular architecture must be tightly co-ordinated in space and time. Live imaging of different animal models has provided valuable insights into the cellular dynamics...
Contexts in source publication
Context 1
... extension (CE) is a morphogenetic process in which tissue narrows or converges along one axis and elongates or extends in one or both of the orthogonal axes (Figure 1). CE is a fundamental mechanism that shapes many different tissues in both vertebrates and invertebrates and is critical for neural tube formation [13]. ...
Context 2
... constriction (AC) is a common mechanism of tissue remodelling that involves reduction in the apical surface area of a cell [39]. The resulting changes in cell geometry can shape tissues by bending epithelial sheets or causing cell ingression or extrusion (Figure 1). To this end, AC plays a part in neurulation by contributing to the formation of the 'bending points' which facilitate the bending of the neural plate and also assists in force generation which promotes closure of the neural tube [3]. ...
Citations
... Зовні нервова пластинка спочатку схожа на лопатоподібний лист, медіолатеральна частина якого є ширшою за передньо-задню частину, потім вона починає потовщуватися, звужуватися медіолатерально й витягуватися рострокаудально [7]. Цей морфогенетичний процес визначають як конвергентне (клітинні маси конвергують у напрямі дорзальної серединної лінії) розширення (витягування / розширення у передньо-задньому напрямі) [7,21]. ...
... Один із найпоширеніших механізмів, що лежать в основі конвергентного розширення, -інтеркаляція поляризованих клітин, що спрямовуються неканонічним шляхом Wnt/Planar Cell Polarity (PCP). Міжклітинна інтеркаляція -це процес, протягом якого сусідні клітини міняються місцями в одній чи кількох площинах [21,22]. Зазначимо також, що нервова пластинка може формуватися ізольовано від навколишньої епідермальної ектодерми [23]. ...
... Кожний нервовий валик є двошаровим -складається з шару нейроепітелію, що зовні покритий шаром епідермальної ектодерми. Підіймання нервових валиків утворює жолобоподібний простір, що називають нервовою борозною (нервовим жолобком), який пізніше стає просвітом примітивної нервової трубки [21,24]. ...
Neurulation occurs by two different mechanisms, called primary and secondary neurulation. In humans, primary neurulation occurs along most of the rostrocaudal axis of the embryo, while secondary neurulation occurs caudally, only in the lower sacral and coccygeal regions. Primary neurulation is responsible for a change in the neural plate shape, the lateral edges of which rise and then converge at the dorsal midline to merge into a tube. Initially, the neural tube, formed as a result of primary neurulation, is open at both ends through the so-called rostral and caudal neuropores. These neuropores connect the inner part of the neural tube with the environment (amniotic cavity) and later (by the end of primary neurulation) are closed. During primary neurulation, the brain and spinal cord are formed up to the upper sacral region (up to the level of junction between S1 and S2 vertebral bodies), however, the most caudal part of this anatomical region (sacral-coccygeal division of the spinal cord, conus medullaris and filum terminale) is formed at secondary neurulation. In humans, secondary neurulation occurs due to elongation and cavitation of the caudal cell mass into the medulla, which then transforms into a secondary neural tube. Thus, the main differences between primary and secondary neurulation are that the neural plate folds and invaginates into the body of the embryo and separates from the surface ectoderm, forming an underlying hollow tube in primary neurulation. Mesenchymal cell сlusters form a dense cord that undergoes mesenchymal-epithelial transition and forms cavities and an empty tube during secondary neurulation to form the terminal part of the spinal cord. Conclusions. Understanding the detailed molecular and genetic mechanisms of each stage of neurulation is relevant due to widespread congenital neural tube defects, and only perfect knowledge on each aspect of neurulation and all possible factors of potential influence on it will help to develop modern options for influencing some of them, and probably, cause a decrease in neural tube congenital defects.
... In particular, the vertebrate neural plate, a vital precursor of the central nervous system, undergoes extensive rearrangements during neurulation to form the neural tube and nerve cord 20,21,22 . Despite extensive research into the mechanisms underlying neural tube formation during neurulation, little is currently known about neural plate morphogenesis during gastrulation 20,23,24 . Failures of functional neural plate formation in the gastrula result in aberrant tissue shape and position and are associated with severe defects of the brain and nervous system in later stages, as evidenced by many mutants identified in Danio rerio (zebrafish) 25,26,27 . ...
The formation of complex tissues during embryonic development requires an intricate spatiotemporal coordination of local mechanical processes regulating global tissue morphogenesis. Here, we uncover a novel mechanism that mechanically regulates the shape of the anterior neural plate (ANP), a vital forebrain precursor, during zebrafish gastrulation. Combining in vivo and in silico approaches we reveal that the ANP is shaped by global tissue flows regulated by distinct force generating processes. We show that mesendoderm migration and E-cadherin-dependent differential tissue interactions control distinct flow regimes in the neuroectoderm. Initial opposing flows lead to progressive tissue folding and neuroectoderm internalisation which in turn provide forces driving ANP tissue reshaping. We find that convergent extension is dispensable for internalisation but required for ANP tissue extension. Our results highlight how spatiotemporal regulation and coupling of different mechanical processes between tissues in the embryo controls the first folding event in the developing brain.
