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The beetle amnion and serosa functionally interact as apposed epithelia

Unlike passive rupture of the human chorioamnion at birth, the insect extraembryonic (EE) tissues – the amnion and serosa – actively rupture and withdraw in late embryogenesis. Withdrawal is essential for development and has been a morphogenetic puzzle. Here, we use new fluorescent transgenic lines...

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Autores principales: Hilbrant, Maarten, Horn, Thorsten, Koelzer, Stefan, Panfilio, Kristen A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4786423/
https://www.ncbi.nlm.nih.gov/pubmed/26824390
http://dx.doi.org/10.7554/eLife.13834
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author Hilbrant, Maarten
Horn, Thorsten
Koelzer, Stefan
Panfilio, Kristen A
author_facet Hilbrant, Maarten
Horn, Thorsten
Koelzer, Stefan
Panfilio, Kristen A
author_sort Hilbrant, Maarten
collection PubMed
description Unlike passive rupture of the human chorioamnion at birth, the insect extraembryonic (EE) tissues – the amnion and serosa – actively rupture and withdraw in late embryogenesis. Withdrawal is essential for development and has been a morphogenetic puzzle. Here, we use new fluorescent transgenic lines in the beetle Tribolium castaneum to show that the EE tissues dynamically form a basal-basal epithelial bilayer, contradicting the previous hypothesis of EE intercalation. We find that the EE tissues repeatedly detach and reattach throughout development and have distinct roles. Quantitative live imaging analyses show that the amnion initiates EE rupture in a specialized anterior-ventral cap. RNAi phenotypes demonstrate that the serosa contracts autonomously. Thus, apposition in a bilayer enables the amnion as 'initiator' to coordinate with the serosa as 'driver' to achieve withdrawal. This EE strategy may reflect evolutionary changes within the holometabolous insects and serves as a model to study interactions between developing epithelia. DOI: http://dx.doi.org/10.7554/eLife.13834.001
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spelling pubmed-47864232016-03-17 The beetle amnion and serosa functionally interact as apposed epithelia Hilbrant, Maarten Horn, Thorsten Koelzer, Stefan Panfilio, Kristen A eLife Cell Biology Unlike passive rupture of the human chorioamnion at birth, the insect extraembryonic (EE) tissues – the amnion and serosa – actively rupture and withdraw in late embryogenesis. Withdrawal is essential for development and has been a morphogenetic puzzle. Here, we use new fluorescent transgenic lines in the beetle Tribolium castaneum to show that the EE tissues dynamically form a basal-basal epithelial bilayer, contradicting the previous hypothesis of EE intercalation. We find that the EE tissues repeatedly detach and reattach throughout development and have distinct roles. Quantitative live imaging analyses show that the amnion initiates EE rupture in a specialized anterior-ventral cap. RNAi phenotypes demonstrate that the serosa contracts autonomously. Thus, apposition in a bilayer enables the amnion as 'initiator' to coordinate with the serosa as 'driver' to achieve withdrawal. This EE strategy may reflect evolutionary changes within the holometabolous insects and serves as a model to study interactions between developing epithelia. DOI: http://dx.doi.org/10.7554/eLife.13834.001 eLife Sciences Publications, Ltd 2016-01-29 /pmc/articles/PMC4786423/ /pubmed/26824390 http://dx.doi.org/10.7554/eLife.13834 Text en © 2016, Hilbrant et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Hilbrant, Maarten
Horn, Thorsten
Koelzer, Stefan
Panfilio, Kristen A
The beetle amnion and serosa functionally interact as apposed epithelia
title The beetle amnion and serosa functionally interact as apposed epithelia
title_full The beetle amnion and serosa functionally interact as apposed epithelia
title_fullStr The beetle amnion and serosa functionally interact as apposed epithelia
title_full_unstemmed The beetle amnion and serosa functionally interact as apposed epithelia
title_short The beetle amnion and serosa functionally interact as apposed epithelia
title_sort beetle amnion and serosa functionally interact as apposed epithelia
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4786423/
https://www.ncbi.nlm.nih.gov/pubmed/26824390
http://dx.doi.org/10.7554/eLife.13834
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