Comparative analysis of neurulation: First impressions do not count

Harrington, Michael; Hong, Elim; Brewster, Rachel

doi:10.1002/mrd.21085

Cited by 45 publications

(52 citation statements)

References 99 publications

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“…Such variations among mechanisms of neural tube formation in different animals highlight the diversification of strategies for organ development during animal evolution (Harrington et al. 2009). …”

Section: Introductionmentioning

confidence: 99%

Mechanical roles of apical constriction, cell elongation, and cell migration during neural tube formation in Xenopus

Inoue

Suzuki

Watanabe

et al. 2016

Biomech Model Mechanobiol

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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.Electronic supplementary materialThe online version of this article (doi:10.1007/s10237-016-0794-1) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Mechanical roles of apical constriction, cell elongation, and cell migration during neural tube formation in Xenopus

Inoue

Suzuki

Watanabe

et al. 2016

Biomech Model Mechanobiol

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“…Although the details of neural tube closure (NTC) vary between species (Harrington et al, 2009), broadly conserved cytoskeletal mechanisms bring together the two lateral edges of the neural plate followed by their fusion at the dorsal midline. Disruption of NTC cellular mechanisms, such as those generating apically polarized constrictions in the epithelial neural plate cells, causes severe and sometimes irreparable defects in the spinal cord and brain (Haigo et al, 2003, Ybot-Gonzalez and Copp, 1999).…”

Section: Introductionmentioning

confidence: 99%

T-type Calcium Channel Regulation of Neural Tube Closure and EphrinA/EPHA Expression

et al. 2015

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A major class of human birth defects arise from aberrations during neural tube closure (NTC). We report on a NTC signaling pathway requiring T-type calcium channels (TTCC) that is conserved between primitive chordates (Ciona) and Xenopus. With loss of TTCCs there is a failure to seal the anterior neural folds. Accompanying loss of TTCCs is an upregulation of EphrinA effectors. Ephrin signaling is known to be important in NTC, and ephrins can affect both cell adhesion and repulsion. In Ciona, ephrinA-d expression is down regulated at the end of neurulation, while with loss of TTCC ephrinA-d remains elevated. Accordingly, overexpression of ephrinA-d phenocopied TTCC loss of function, while overexpression of a dominant negative Ephrin receptor was able to rescue NTC in a Ciona TTCC mutant. We hypothesize that signaling through TTCCs is necessary for proper anterior NTC through down regulation of ephrins, and possibly elimination of a repulsive signal.

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“…The brain ventricular system is found in vertebrates, and the ventricles develop after neural tube formation, when the central lumen fills with cerebrospinal fluid (CSF) 1,2 . CSF is a protein rich fluid that is essential for normal brain development and function [3][4][5][6] .…”

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confidence: 99%

An Assay for Permeability of the Zebrafish Embryonic Neuroepithelium

Chang

Sive

2012

JoVE

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The brain ventricular system is conserved among vertebrates and is composed of a series of interconnected cavities called brain ventricles, which form during the earliest stages of brain development and are maintained throughout the animal's life. The brain ventricular system is found in vertebrates, and the ventricles develop after neural tube formation, when the central lumen fills with cerebrospinal fluid (CSF) 1,2 . CSF is a protein rich fluid that is essential for normal brain development and function [3][4][5][6] .In zebrafish, brain ventricle inflation begins at approximately 18 hr post fertilization (hpf), after the neural tube is closed. Multiple processes are associated with brain ventricle formation, including formation of a neuroepithelium, tight junction formation that regulates permeability and CSF production. We showed that the Na,K-ATPase is required for brain ventricle inflation, impacting all these processes 7,8 , while claudin 5a is necessary for tight junction formation 9 . Additionally, we showed that "relaxation" of the embryonic neuroepithelium, via inhibition of myosin, is associated with brain ventricle inflation.To investigate the regulation of permeability during zebrafish brain ventricle inflation, we developed a ventricular dye retention assay. This method uses brain ventricle injection in a living zebrafish embryo, a technique previously developed in our lab 10 , to fluorescently label the cerebrospinal fluid. Embryos are then imaged over time as the fluorescent dye moves through the brain ventricles and neuroepithelium. The distance the dye front moves away from the basal (non-luminal) side of the neuroepithelium over time is quantified and is a measure of neuroepithelial permeability (Figure 1). We observe that dyes 70 kDa and smaller will move through the neuroepithelium and can be detected outside the embryonic zebrafish brain at 24 hpf (Figure 2). This dye retention assay can be used to analyze neuroepithelial permeability in a variety of different genetic backgrounds, at different times during development, and after environmental perturbations. It may also be useful in examining pathological accumulation of CSF. Overall, this technique allows investigators to analyze the role and regulation of permeability during development and disease. Video LinkThe video component of this article can be found at http://www.jove.com/video/4242/ Protocol 1. Preparing for Microinjection 1. Prepare microinjection needles by pulling capillary tubes using Sutter instruments needle puller. 2. Load microinjection needle with fluorescent dye (FITC-Dextran). 3. Mount needle on micromanipulator and microinjection apparatus. 4. Carefully break microinjection needle using forceps to roughly 2 μm in width, however, this will vary depending on your microinjector setup.For our microinjection needles, this corresponds to the first region of the needle from the tip that does not bend. 5. Measure drop size in oil, adjusting injection time and pressure, so that each injection delivers 1 nl. Example ...

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Comparative analysis of neurulation: First impressions do not count

Cited by 45 publications

References 99 publications

Mechanical roles of apical constriction, cell elongation, and cell migration during neural tube formation in Xenopus

Mechanical roles of apical constriction, cell elongation, and cell migration during neural tube formation in Xenopus

T-type Calcium Channel Regulation of Neural Tube Closure and EphrinA/EPHA Expression

An Assay for Permeability of the Zebrafish Embryonic Neuroepithelium

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