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Cilia are required for asymmetric nodal induction in the sea urchin embryo

BACKGROUND: Left-right (LR) organ asymmetries are a common feature of metazoan animals. In many cases, laterality is established by a conserved asymmetric Nodal signaling cascade during embryogenesis. In most vertebrates, asymmetric nodal induction results from a cilia-driven leftward fluid flow at...

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Autores principales: Tisler, Matthias, Wetzel, Franziska, Mantino, Sabrina, Kremnyov, Stanislav, Thumberger, Thomas, Schweickert, Axel, Blum, Martin, Vick, Philipp
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4994401/
https://www.ncbi.nlm.nih.gov/pubmed/27553781
http://dx.doi.org/10.1186/s12861-016-0128-7
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author Tisler, Matthias
Wetzel, Franziska
Mantino, Sabrina
Kremnyov, Stanislav
Thumberger, Thomas
Schweickert, Axel
Blum, Martin
Vick, Philipp
author_facet Tisler, Matthias
Wetzel, Franziska
Mantino, Sabrina
Kremnyov, Stanislav
Thumberger, Thomas
Schweickert, Axel
Blum, Martin
Vick, Philipp
author_sort Tisler, Matthias
collection PubMed
description BACKGROUND: Left-right (LR) organ asymmetries are a common feature of metazoan animals. In many cases, laterality is established by a conserved asymmetric Nodal signaling cascade during embryogenesis. In most vertebrates, asymmetric nodal induction results from a cilia-driven leftward fluid flow at the left-right organizer (LRO), a ciliated epithelium present during gastrula/neurula stages. Conservation of LRO and flow beyond the vertebrates has not been reported yet. RESULTS: Here we study sea urchin embryos, which use nodal to establish larval LR asymmetry as well. Cilia were found in the archenteron of embryos undergoing gastrulation. Expression of foxj1 and dnah9 suggested that archenteron cilia were motile. Cilia were polarized to the posterior pole of cells, a prerequisite of directed flow. High-speed videography revealed rotating cilia in the archenteron slightly before asymmetric nodal induction. Removal of cilia through brief high salt treatments resulted in aberrant patterns of nodal expression. Our data demonstrate that cilia - like in vertebrates - are required for asymmetric nodal induction in sea urchin embryos. CONCLUSIONS: Based on these results we argue that the anterior archenteron represents a bona fide LRO and propose that cilia-based symmetry breakage is a synapomorphy of the deuterostomes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12861-016-0128-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-49944012016-08-24 Cilia are required for asymmetric nodal induction in the sea urchin embryo Tisler, Matthias Wetzel, Franziska Mantino, Sabrina Kremnyov, Stanislav Thumberger, Thomas Schweickert, Axel Blum, Martin Vick, Philipp BMC Dev Biol Research Article BACKGROUND: Left-right (LR) organ asymmetries are a common feature of metazoan animals. In many cases, laterality is established by a conserved asymmetric Nodal signaling cascade during embryogenesis. In most vertebrates, asymmetric nodal induction results from a cilia-driven leftward fluid flow at the left-right organizer (LRO), a ciliated epithelium present during gastrula/neurula stages. Conservation of LRO and flow beyond the vertebrates has not been reported yet. RESULTS: Here we study sea urchin embryos, which use nodal to establish larval LR asymmetry as well. Cilia were found in the archenteron of embryos undergoing gastrulation. Expression of foxj1 and dnah9 suggested that archenteron cilia were motile. Cilia were polarized to the posterior pole of cells, a prerequisite of directed flow. High-speed videography revealed rotating cilia in the archenteron slightly before asymmetric nodal induction. Removal of cilia through brief high salt treatments resulted in aberrant patterns of nodal expression. Our data demonstrate that cilia - like in vertebrates - are required for asymmetric nodal induction in sea urchin embryos. CONCLUSIONS: Based on these results we argue that the anterior archenteron represents a bona fide LRO and propose that cilia-based symmetry breakage is a synapomorphy of the deuterostomes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12861-016-0128-7) contains supplementary material, which is available to authorized users. BioMed Central 2016-08-23 /pmc/articles/PMC4994401/ /pubmed/27553781 http://dx.doi.org/10.1186/s12861-016-0128-7 Text en © The Author(s). 2016 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 Article
Tisler, Matthias
Wetzel, Franziska
Mantino, Sabrina
Kremnyov, Stanislav
Thumberger, Thomas
Schweickert, Axel
Blum, Martin
Vick, Philipp
Cilia are required for asymmetric nodal induction in the sea urchin embryo
title Cilia are required for asymmetric nodal induction in the sea urchin embryo
title_full Cilia are required for asymmetric nodal induction in the sea urchin embryo
title_fullStr Cilia are required for asymmetric nodal induction in the sea urchin embryo
title_full_unstemmed Cilia are required for asymmetric nodal induction in the sea urchin embryo
title_short Cilia are required for asymmetric nodal induction in the sea urchin embryo
title_sort cilia are required for asymmetric nodal induction in the sea urchin embryo
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4994401/
https://www.ncbi.nlm.nih.gov/pubmed/27553781
http://dx.doi.org/10.1186/s12861-016-0128-7
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