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On the origin of vertebrate somites

INTRODUCTION: Somites, blocks of mesoderm tissue located on either side of the neural tube in the developing vertebrate embryo, are derived from mesenchymal cells in the presomitic mesoderm (PSM) and are a defining characteristic of vertebrates. In vertebrates, the somite segmental boundary is deter...

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Autores principales: Onai, Takayuki, Aramaki, Toshihiro, Inomata, Hidehiko, Hirai, Tamami, Kuratani, Shigeru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4660845/
https://www.ncbi.nlm.nih.gov/pubmed/26613046
http://dx.doi.org/10.1186/s40851-015-0033-0
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author Onai, Takayuki
Aramaki, Toshihiro
Inomata, Hidehiko
Hirai, Tamami
Kuratani, Shigeru
author_facet Onai, Takayuki
Aramaki, Toshihiro
Inomata, Hidehiko
Hirai, Tamami
Kuratani, Shigeru
author_sort Onai, Takayuki
collection PubMed
description INTRODUCTION: Somites, blocks of mesoderm tissue located on either side of the neural tube in the developing vertebrate embryo, are derived from mesenchymal cells in the presomitic mesoderm (PSM) and are a defining characteristic of vertebrates. In vertebrates, the somite segmental boundary is determined by Notch signalling and the antagonistic relationship of the downstream targets of Notch, Lfng, and Delta1 in the anterior PSM. The presence of somites in the basal chordate amphioxus (Branchiostoma floridae) indicates that the last common ancestor of chordates also had somites. However, it remains unclear how the genetic mechanisms underlying somitogenesis in vertebrates evolved from those in ancestral chordates. RESULTS: We demonstrate that during the gastrula stages of amphioxus embryos, BfFringe expression in the endoderm of the archenteron is detected ventrally to the ventral limit of BfDelta expression in the presumptive rostral somites along the dorsal/ventral (D/V) body axis. Suppression of Notch signalling by DAPT (a γ-secretase inhibitor that indirectly inhibits Notch) treatment from the late blastula stage reduced late gastrula stage expression of BfFringe in the endodermal archenteron and somite markers BfDelta and BfHairy-b in the mesodermal archenteron. Later in development, somites in the DAPT-treated embryo did not separate completely from the dorsal roof of the archenteron. In addition, clear segmental boundaries between somites were not detected in DAPT-treated amphioxus embryos at the larva stage. Similarly, in vertebrates, DAPT treatment from the late blastula stage in Xenopus (Xenopus laevis) embryos resulted in disruption of somite XlDelta-2 expression at the late gastrula stage. At the tail bud stage, the segmental expression of XlMyoD in myotomes was diminished. CONCLUSIONS: We propose that Notch signalling and the Fringe/Delta cassette for dorso-ventral boundary formation in the archenteron that separates somites from the gut in an amphioxus-like ancestral chordate were co-opted for anteroposterior segmental boundary formation in the vertebrate anterior PSM during evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40851-015-0033-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-46608452015-11-27 On the origin of vertebrate somites Onai, Takayuki Aramaki, Toshihiro Inomata, Hidehiko Hirai, Tamami Kuratani, Shigeru Zoological Lett Research Article INTRODUCTION: Somites, blocks of mesoderm tissue located on either side of the neural tube in the developing vertebrate embryo, are derived from mesenchymal cells in the presomitic mesoderm (PSM) and are a defining characteristic of vertebrates. In vertebrates, the somite segmental boundary is determined by Notch signalling and the antagonistic relationship of the downstream targets of Notch, Lfng, and Delta1 in the anterior PSM. The presence of somites in the basal chordate amphioxus (Branchiostoma floridae) indicates that the last common ancestor of chordates also had somites. However, it remains unclear how the genetic mechanisms underlying somitogenesis in vertebrates evolved from those in ancestral chordates. RESULTS: We demonstrate that during the gastrula stages of amphioxus embryos, BfFringe expression in the endoderm of the archenteron is detected ventrally to the ventral limit of BfDelta expression in the presumptive rostral somites along the dorsal/ventral (D/V) body axis. Suppression of Notch signalling by DAPT (a γ-secretase inhibitor that indirectly inhibits Notch) treatment from the late blastula stage reduced late gastrula stage expression of BfFringe in the endodermal archenteron and somite markers BfDelta and BfHairy-b in the mesodermal archenteron. Later in development, somites in the DAPT-treated embryo did not separate completely from the dorsal roof of the archenteron. In addition, clear segmental boundaries between somites were not detected in DAPT-treated amphioxus embryos at the larva stage. Similarly, in vertebrates, DAPT treatment from the late blastula stage in Xenopus (Xenopus laevis) embryos resulted in disruption of somite XlDelta-2 expression at the late gastrula stage. At the tail bud stage, the segmental expression of XlMyoD in myotomes was diminished. CONCLUSIONS: We propose that Notch signalling and the Fringe/Delta cassette for dorso-ventral boundary formation in the archenteron that separates somites from the gut in an amphioxus-like ancestral chordate were co-opted for anteroposterior segmental boundary formation in the vertebrate anterior PSM during evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40851-015-0033-0) contains supplementary material, which is available to authorized users. BioMed Central 2015-11-26 /pmc/articles/PMC4660845/ /pubmed/26613046 http://dx.doi.org/10.1186/s40851-015-0033-0 Text en © Onai et al. 2015 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
Onai, Takayuki
Aramaki, Toshihiro
Inomata, Hidehiko
Hirai, Tamami
Kuratani, Shigeru
On the origin of vertebrate somites
title On the origin of vertebrate somites
title_full On the origin of vertebrate somites
title_fullStr On the origin of vertebrate somites
title_full_unstemmed On the origin of vertebrate somites
title_short On the origin of vertebrate somites
title_sort on the origin of vertebrate somites
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4660845/
https://www.ncbi.nlm.nih.gov/pubmed/26613046
http://dx.doi.org/10.1186/s40851-015-0033-0
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