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Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula

The origin of extracellular digestion in metazoans was accompanied by structural and physiological alterations of the gut. These adaptations culminated in the differentiation of a novel digestive structure in jawed vertebrates, the stomach. Specific endoderm/mesenchyme signalling is required for sto...

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Autores principales: Gonçalves, Odete, Freitas, Renata, Ferreira, Patrícia, Araújo, Mafalda, Zhang, GuangJun, Mazan, Sylvie, Cohn, Martin J., Castro, L. Filipe C., Wilson, Jonathan M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6346038/
https://www.ncbi.nlm.nih.gov/pubmed/30679499
http://dx.doi.org/10.1038/s41598-018-36413-0
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author Gonçalves, Odete
Freitas, Renata
Ferreira, Patrícia
Araújo, Mafalda
Zhang, GuangJun
Mazan, Sylvie
Cohn, Martin J.
Castro, L. Filipe C.
Wilson, Jonathan M.
author_facet Gonçalves, Odete
Freitas, Renata
Ferreira, Patrícia
Araújo, Mafalda
Zhang, GuangJun
Mazan, Sylvie
Cohn, Martin J.
Castro, L. Filipe C.
Wilson, Jonathan M.
author_sort Gonçalves, Odete
collection PubMed
description The origin of extracellular digestion in metazoans was accompanied by structural and physiological alterations of the gut. These adaptations culminated in the differentiation of a novel digestive structure in jawed vertebrates, the stomach. Specific endoderm/mesenchyme signalling is required for stomach differentiation, involving the growth and transcription factors: 1) Shh and Bmp4, required for stomach outgrowth; 2) Barx1, Sfrps and Sox2, required for gastric epithelium development and 3) Cdx1 and Cdx2, involved in intestinal versus gastric identity. Thus, modulation of endoderm/mesenchyme signalling emerges as a plausible mechanism linked to the origin of the stomach. In order to gain insight into the ancient mechanisms capable of generating this structure in jawed vertebrates, we characterised the development of the gut in the catshark Scyliorhinus canicula. As chondrichthyans, these animals retained plesiomorphic features of jawed vertebrates, including a well-differentiated stomach. We identified a clear molecular regionalization of their embryonic gut, characterised by the expression of barx1 and sox2 in the prospective stomach region and expression of cdx1 and cdx2 in the prospective intestine. Furthermore, we show that gastric gland development occurs close to hatching, accompanied by the onset of gastric proton pump activity. Our findings favour a scenario in which the developmental mechanisms involved in the origin of the stomach were present in the common ancestor of chondrichthyans and osteichthyans.
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spelling pubmed-63460382019-01-29 Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula Gonçalves, Odete Freitas, Renata Ferreira, Patrícia Araújo, Mafalda Zhang, GuangJun Mazan, Sylvie Cohn, Martin J. Castro, L. Filipe C. Wilson, Jonathan M. Sci Rep Article The origin of extracellular digestion in metazoans was accompanied by structural and physiological alterations of the gut. These adaptations culminated in the differentiation of a novel digestive structure in jawed vertebrates, the stomach. Specific endoderm/mesenchyme signalling is required for stomach differentiation, involving the growth and transcription factors: 1) Shh and Bmp4, required for stomach outgrowth; 2) Barx1, Sfrps and Sox2, required for gastric epithelium development and 3) Cdx1 and Cdx2, involved in intestinal versus gastric identity. Thus, modulation of endoderm/mesenchyme signalling emerges as a plausible mechanism linked to the origin of the stomach. In order to gain insight into the ancient mechanisms capable of generating this structure in jawed vertebrates, we characterised the development of the gut in the catshark Scyliorhinus canicula. As chondrichthyans, these animals retained plesiomorphic features of jawed vertebrates, including a well-differentiated stomach. We identified a clear molecular regionalization of their embryonic gut, characterised by the expression of barx1 and sox2 in the prospective stomach region and expression of cdx1 and cdx2 in the prospective intestine. Furthermore, we show that gastric gland development occurs close to hatching, accompanied by the onset of gastric proton pump activity. Our findings favour a scenario in which the developmental mechanisms involved in the origin of the stomach were present in the common ancestor of chondrichthyans and osteichthyans. Nature Publishing Group UK 2019-01-24 /pmc/articles/PMC6346038/ /pubmed/30679499 http://dx.doi.org/10.1038/s41598-018-36413-0 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Gonçalves, Odete
Freitas, Renata
Ferreira, Patrícia
Araújo, Mafalda
Zhang, GuangJun
Mazan, Sylvie
Cohn, Martin J.
Castro, L. Filipe C.
Wilson, Jonathan M.
Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula
title Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula
title_full Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula
title_fullStr Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula
title_full_unstemmed Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula
title_short Molecular ontogeny of the stomach in the catshark Scyliorhinus canicula
title_sort molecular ontogeny of the stomach in the catshark scyliorhinus canicula
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6346038/
https://www.ncbi.nlm.nih.gov/pubmed/30679499
http://dx.doi.org/10.1038/s41598-018-36413-0
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