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Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis

Cooperative morphogenesis of cell lineages underlies the development of functional units and organs. To study mechanisms driving the coordination of lineages, we investigated soma-germline interactions during oogenesis. From invertebrates to vertebrates, oocytes develop as part of a germline cyst th...

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Autores principales: Weichselberger, Vanessa, Dondl, Patrick, Classen, Anne-Kathrin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9605976/
https://www.ncbi.nlm.nih.gov/pubmed/36289235
http://dx.doi.org/10.1038/s41467-022-33845-1
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author Weichselberger, Vanessa
Dondl, Patrick
Classen, Anne-Kathrin
author_facet Weichselberger, Vanessa
Dondl, Patrick
Classen, Anne-Kathrin
author_sort Weichselberger, Vanessa
collection PubMed
description Cooperative morphogenesis of cell lineages underlies the development of functional units and organs. To study mechanisms driving the coordination of lineages, we investigated soma-germline interactions during oogenesis. From invertebrates to vertebrates, oocytes develop as part of a germline cyst that consists of the oocyte itself and so-called nurse cells, which feed the oocyte and are eventually removed. The enveloping somatic cells specialize to facilitate either oocyte maturation or nurse cell removal, which makes it essential to establish the right match between germline and somatic cells. We uncover that the transcriptional regulator Eya, expressed in the somatic lineage, controls bilateral cell–cell affinity between germline and somatic cells in Drosophila oogenesis. Employing functional studies and mathematical modelling, we show that differential affinity and the resulting forces drive somatic cell redistribution over the germline surface and control oocyte growth to match oocyte and nurse cells with their respective somatic cells. Thus, our data demonstrate that differential affinity between cell lineages is sufficient to drive the complex assembly of inter-lineage functional units and underlies tissue self-organization during Drosophila oogenesis.
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spelling pubmed-96059762022-10-28 Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis Weichselberger, Vanessa Dondl, Patrick Classen, Anne-Kathrin Nat Commun Article Cooperative morphogenesis of cell lineages underlies the development of functional units and organs. To study mechanisms driving the coordination of lineages, we investigated soma-germline interactions during oogenesis. From invertebrates to vertebrates, oocytes develop as part of a germline cyst that consists of the oocyte itself and so-called nurse cells, which feed the oocyte and are eventually removed. The enveloping somatic cells specialize to facilitate either oocyte maturation or nurse cell removal, which makes it essential to establish the right match between germline and somatic cells. We uncover that the transcriptional regulator Eya, expressed in the somatic lineage, controls bilateral cell–cell affinity between germline and somatic cells in Drosophila oogenesis. Employing functional studies and mathematical modelling, we show that differential affinity and the resulting forces drive somatic cell redistribution over the germline surface and control oocyte growth to match oocyte and nurse cells with their respective somatic cells. Thus, our data demonstrate that differential affinity between cell lineages is sufficient to drive the complex assembly of inter-lineage functional units and underlies tissue self-organization during Drosophila oogenesis. Nature Publishing Group UK 2022-10-26 /pmc/articles/PMC9605976/ /pubmed/36289235 http://dx.doi.org/10.1038/s41467-022-33845-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Weichselberger, Vanessa
Dondl, Patrick
Classen, Anne-Kathrin
Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis
title Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis
title_full Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis
title_fullStr Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis
title_full_unstemmed Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis
title_short Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis
title_sort eya-controlled affinity between cell lineages drives tissue self-organization during drosophila oogenesis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9605976/
https://www.ncbi.nlm.nih.gov/pubmed/36289235
http://dx.doi.org/10.1038/s41467-022-33845-1
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