Cargando…

Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development

Neural tube closure is a fundamental process during vertebrate embryogenesis, which leads to the formation of the central nervous system. Defective neural tube closure leads to neural tube defects which are some of the most common human birth defects. While the intrinsic morphogenetic events shaping...

Descripción completa

Detalles Bibliográficos
Autores principales: Christodoulou, Neophytos, Skourides, Paris A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9868421/
https://www.ncbi.nlm.nih.gov/pubmed/36699010
http://dx.doi.org/10.3389/fcell.2022.1091629
_version_ 1784876533434810368
author Christodoulou, Neophytos
Skourides, Paris A.
author_facet Christodoulou, Neophytos
Skourides, Paris A.
author_sort Christodoulou, Neophytos
collection PubMed
description Neural tube closure is a fundamental process during vertebrate embryogenesis, which leads to the formation of the central nervous system. Defective neural tube closure leads to neural tube defects which are some of the most common human birth defects. While the intrinsic morphogenetic events shaping the neuroepithelium have been studied extensively, how tissues mechanically coupled with the neural plate influence neural tube closure remains poorly understood. Here, using Xenopus laevis embryos, live imaging in combination with loss of function experiments and morphometric analysis of fixed samples we explore the reciprocal mechanical communication between the neural plate and the somitic mesoderm and its impact on tissue morphogenesis. We show that although somitic mesoderm convergent extension occurs independently from neural plate morphogenesis neural tube closure depends on somitic mesoderm morphogenesis. Specifically, impaired somitic mesoderm remodelling results in defective apical constriction within the neuroepithelium and failure of neural tube closure. Last, our data reveal that mild abnormalities in somitic mesoderm and neural plate morphogenesis have a synergistic effect during neurulation, leading to severe neural tube closure defects. Overall, our data reveal that defective morphogenesis of tissues mechanically coupled with the neural plate can not only drastically exacerbate mild neural tube defects that may arise from abnormalities within the neural tissue but can also elicit neural tube defects even when the neural plate is itself free of inherent defects.
format Online
Article
Text
id pubmed-9868421
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-98684212023-01-24 Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development Christodoulou, Neophytos Skourides, Paris A. Front Cell Dev Biol Cell and Developmental Biology Neural tube closure is a fundamental process during vertebrate embryogenesis, which leads to the formation of the central nervous system. Defective neural tube closure leads to neural tube defects which are some of the most common human birth defects. While the intrinsic morphogenetic events shaping the neuroepithelium have been studied extensively, how tissues mechanically coupled with the neural plate influence neural tube closure remains poorly understood. Here, using Xenopus laevis embryos, live imaging in combination with loss of function experiments and morphometric analysis of fixed samples we explore the reciprocal mechanical communication between the neural plate and the somitic mesoderm and its impact on tissue morphogenesis. We show that although somitic mesoderm convergent extension occurs independently from neural plate morphogenesis neural tube closure depends on somitic mesoderm morphogenesis. Specifically, impaired somitic mesoderm remodelling results in defective apical constriction within the neuroepithelium and failure of neural tube closure. Last, our data reveal that mild abnormalities in somitic mesoderm and neural plate morphogenesis have a synergistic effect during neurulation, leading to severe neural tube closure defects. Overall, our data reveal that defective morphogenesis of tissues mechanically coupled with the neural plate can not only drastically exacerbate mild neural tube defects that may arise from abnormalities within the neural tissue but can also elicit neural tube defects even when the neural plate is itself free of inherent defects. Frontiers Media S.A. 2023-01-09 /pmc/articles/PMC9868421/ /pubmed/36699010 http://dx.doi.org/10.3389/fcell.2022.1091629 Text en Copyright © 2023 Christodoulou and Skourides. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Christodoulou, Neophytos
Skourides, Paris A.
Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development
title Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development
title_full Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development
title_fullStr Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development
title_full_unstemmed Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development
title_short Somitic mesoderm morphogenesis is necessary for neural tube closure during Xenopus development
title_sort somitic mesoderm morphogenesis is necessary for neural tube closure during xenopus development
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9868421/
https://www.ncbi.nlm.nih.gov/pubmed/36699010
http://dx.doi.org/10.3389/fcell.2022.1091629
work_keys_str_mv AT christodoulouneophytos somiticmesodermmorphogenesisisnecessaryforneuraltubeclosureduringxenopusdevelopment
AT skouridesparisa somiticmesodermmorphogenesisisnecessaryforneuraltubeclosureduringxenopusdevelopment