Mesoderm is required for coordinated cell movements within zebrafish neural plate in vivo

Araya, Claudio; Tawk, Marcel; Girdler, Gemma; Costa, Marta; Carmona‐Fontaine, Carlos; Clarke, Jon

doi:10.1186/1749-8104-9-9

Cited by 29 publications

(70 citation statements)

References 54 publications

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“…For instance, N-cadherin protein was decreased at the membrane of Nodal signaling-deficient embryos at tailbud and early somite stages, but mRNA levels were normal (Aquilina-Beck et al, 2007). Similarly, ZO1 (TJP1a), which is associated with both adherens and tight junctions, was expressed at normal levels in embryos treated with SB505124 at similar stages to our study (Araya et al, 2014). …”

Section: Discussionsupporting

confidence: 83%

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Identification of transcripts potentially involved in neural tube closure using RNA sequencing

Kindt

Perosino

Ersfeld

et al. 2018

Genesis

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Anencephaly is a fatal human neural tube defect (NTD) in which the anterior neural tube remains open. Zebrafish embryos with reduced Nodal signaling display an open anterior neural tube phenotype that is analogous to anencephaly. Previous work from our laboratory suggests that Nodal signaling acts through induction of the head mesendoderm and mesoderm. Head mesendoderm/mesoderm then, through an unknown mechanism, promotes formation of the polarized neuroepithelium that is capable of undergoing the movements required for closure. We compared the transcriptome of embryos treated with a Nodal signaling inhibitor at sphere stage, which causes NTDs, to embryos treated at 30% epiboly, which does not cause NTDs. This screen identified over 3,000 transcripts with potential roles in anterior neurulation. Expression of several genes encoding components of tight and adherens junctions was significantly reduced, supporting the model that Nodal signaling regulates formation of the neuroepithelium. mRNAs involved in Wnt, FGF, and BMP signaling were also differentially expressed, suggesting these pathways might regulate anterior neurulation. In support of this, we found that pharmacological inhibition of FGF-receptor function causes an open anterior NTD as well as loss of mesodermal derivatives. This suggests that Nodal and FGF signaling both promote anterior neurulation through induction of head mesoderm.

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Section: Discussionsupporting

confidence: 83%

“…Previous studies indicate the developing neural tube is disorganized in Nodal signaling deficient embryos with an open neural tube (Aquilina-Beck et al, 2007; Araya et al, 2014). The organization of the neural tube is mediated by adherens and tight junctions, which form in a step wise fashion.…”

Section: Discussionmentioning

confidence: 99%

Identification of transcripts potentially involved in neural tube closure using RNA sequencing

Kindt

Perosino

Ersfeld

et al. 2018

Genesis

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“…In wild‐type embryos, neural plate and mesoderm lie very close to each other throughout neurulation (Fig. A–C) (Araya et al, ). In fn1+lamC1 MO embryos, however, we found that small gaps between neural and mesoderm layers were already present at the onset of neurulation (arrowheads in Fig.…”

Section: Resultsmentioning

confidence: 82%

Section: Introductionmentioning

confidence: 99%

“…Additionally, we have shown that interactions with adjacent tissues like the underlying mesoderm are necessary for coordinated movements of the neural plate cells (Araya et al, ). In fact, our previous analysis indicates that the movements between the neuroectoderm and the underlying mesoderm are highly coupled during initial stages of zebrafish neurulation (Araya et al, ). Furthermore, in vivo time‐lapse analysis also demonstrates that in the absence of mesoderm progenitors, neural plate cells undergo disrupted dorsal converging movements and embryos develop aberrant neural tube organization (Araya et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Extracellular matrix couples the convergence movements of mesoderm and neural plate during the early stages of neurulation

Araya

Carmona‐Fontaine

Clarke

2016

Developmental Dynamics

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Background: During the initial stages zebrafish neurulation, neural plate cells undergo highly coordinated movements before they assemble into a multicellular solid neural rod. We have previously identified that the underlying mesoderm is critical to ensure such coordination and generate correct neural tube organization. However, how intertissue coordination is achieved in vivo during zebrafish neural tube morphogenesis is unknown. Results: In this work, we use quantitative live imaging to study the coordinated movements of neural ectoderm and mesoderm during dorsal tissue convergence. We show the extracellular matrix components laminin and fibronectin that lie between mesoderm and neural plate act to couple the movements of neural plate and mesoderm during early stages of neurulation and to maintain the close apposition of these two tissues. Conclusions: Our study highlights the importance of the extracellular matrix proteins laminin and libronectin in coupling the movements and spatial proximity of mesoderm and neuroectoderm during the morphogenetic movements of neurulation. Developmental Dynamics 245:580-589,

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Coordinating cell and tissue behavior during zebrafish neural tube morphogenesis

Araya

Ward

Girdler

et al. 2015

Developmental Dynamics

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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.

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Mesoderm is required for coordinated cell movements within zebrafish neural plate in vivo

Cited by 29 publications

References 54 publications

Identification of transcripts potentially involved in neural tube closure using RNA sequencing

Identification of transcripts potentially involved in neural tube closure using RNA sequencing

Extracellular matrix couples the convergence movements of mesoderm and neural plate during the early stages of neurulation

Coordinating cell and tissue behavior during zebrafish neural tube morphogenesis

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