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Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate

BACKGROUND: The notochord has organizer properties and is required for floor plate induction and dorsoventral patterning of the neural tube. This activity has been attributed to sonic hedgehog (shh) signaling, which originates in the notochord, forms a gradient, and autoinduces shh expression in the...

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Autores principales: Kremnyov, Stanislav, Henningfeld, Kristine, Viebahn, Christoph, Tsikolia, Nikoloz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5791209/
https://www.ncbi.nlm.nih.gov/pubmed/29423139
http://dx.doi.org/10.1186/s13227-017-0090-x
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author Kremnyov, Stanislav
Henningfeld, Kristine
Viebahn, Christoph
Tsikolia, Nikoloz
author_facet Kremnyov, Stanislav
Henningfeld, Kristine
Viebahn, Christoph
Tsikolia, Nikoloz
author_sort Kremnyov, Stanislav
collection PubMed
description BACKGROUND: The notochord has organizer properties and is required for floor plate induction and dorsoventral patterning of the neural tube. This activity has been attributed to sonic hedgehog (shh) signaling, which originates in the notochord, forms a gradient, and autoinduces shh expression in the floor plate. However, reported data are inconsistent and the spatiotemporal development of the relevant shh expression domains has not been studied in detail. We therefore studied the expression dynamics of shh in rabbit, chicken and Xenopus laevis embryos (as well as indian hedgehog and desert hedgehog as possible alternative functional candidates in the chicken). RESULTS: Our analysis reveals a markedly divergent pattern within these vertebrates: whereas in the rabbit shh is first expressed in the notochord and its floor plate domain is then induced during subsequent somitogenesis stages, in the chick embryo shh is expressed in the prospective neuroectoderm prior to the notochord formation and, interestingly, prior to mesoderm immigration. Neither indian hedgehog nor desert hedgehog are expressed in these midline structures although mRNA of both genes was detected in other structures of the early chick embryo. In X. laevis, shh is expressed at the beginning of gastrulation in a distinct area dorsal to the dorsal blastopore lip and adjacent to the prospective neuroectoderm, whereas the floor plate expresses shh at the end of gastrulation. CONCLUSIONS: While shh expression patterns in rabbit and X. laevis embryos are roughly compatible with the classical view of “ventral to dorsal induction” of the floor plate, the early shh expression in the chick floor plate challenges this model. Intriguingly, this alternative sequence of domain induction is related to the asymmetrical morphogenesis of the primitive node and other axial organs in the chick. Our results indicate that the floor plate in X. laevis and chick embryos may be initially induced by planar interaction within the ectoderm or epiblast. Furthermore, we propose that the mode of the floor plate induction adapts to the variant topography of interacting tissues during gastrulation and notochord formation and thereby reveals evolutionary plasticity of early embryonic induction. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-017-0090-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-57912092018-02-08 Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate Kremnyov, Stanislav Henningfeld, Kristine Viebahn, Christoph Tsikolia, Nikoloz EvoDevo Research BACKGROUND: The notochord has organizer properties and is required for floor plate induction and dorsoventral patterning of the neural tube. This activity has been attributed to sonic hedgehog (shh) signaling, which originates in the notochord, forms a gradient, and autoinduces shh expression in the floor plate. However, reported data are inconsistent and the spatiotemporal development of the relevant shh expression domains has not been studied in detail. We therefore studied the expression dynamics of shh in rabbit, chicken and Xenopus laevis embryos (as well as indian hedgehog and desert hedgehog as possible alternative functional candidates in the chicken). RESULTS: Our analysis reveals a markedly divergent pattern within these vertebrates: whereas in the rabbit shh is first expressed in the notochord and its floor plate domain is then induced during subsequent somitogenesis stages, in the chick embryo shh is expressed in the prospective neuroectoderm prior to the notochord formation and, interestingly, prior to mesoderm immigration. Neither indian hedgehog nor desert hedgehog are expressed in these midline structures although mRNA of both genes was detected in other structures of the early chick embryo. In X. laevis, shh is expressed at the beginning of gastrulation in a distinct area dorsal to the dorsal blastopore lip and adjacent to the prospective neuroectoderm, whereas the floor plate expresses shh at the end of gastrulation. CONCLUSIONS: While shh expression patterns in rabbit and X. laevis embryos are roughly compatible with the classical view of “ventral to dorsal induction” of the floor plate, the early shh expression in the chick floor plate challenges this model. Intriguingly, this alternative sequence of domain induction is related to the asymmetrical morphogenesis of the primitive node and other axial organs in the chick. Our results indicate that the floor plate in X. laevis and chick embryos may be initially induced by planar interaction within the ectoderm or epiblast. Furthermore, we propose that the mode of the floor plate induction adapts to the variant topography of interacting tissues during gastrulation and notochord formation and thereby reveals evolutionary plasticity of early embryonic induction. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13227-017-0090-x) contains supplementary material, which is available to authorized users. BioMed Central 2018-01-31 /pmc/articles/PMC5791209/ /pubmed/29423139 http://dx.doi.org/10.1186/s13227-017-0090-x Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Kremnyov, Stanislav
Henningfeld, Kristine
Viebahn, Christoph
Tsikolia, Nikoloz
Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate
title Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate
title_full Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate
title_fullStr Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate
title_full_unstemmed Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate
title_short Divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate
title_sort divergent axial morphogenesis and early shh expression in vertebrate prospective floor plate
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5791209/
https://www.ncbi.nlm.nih.gov/pubmed/29423139
http://dx.doi.org/10.1186/s13227-017-0090-x
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