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Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis

It is unknown how growth in one tissue impacts morphogenesis in a neighboring tissue. To address this, we used the Drosophila ovarian follicle, in which a cluster of 15 nurse cells and a posteriorly located oocyte are surrounded by a layer of epithelial cells. It is known that as the nurse cells gro...

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Autores principales: Lamiré, Laurie-Anne, Milani, Pascale, Runel, Gaël, Kiss, Annamaria, Arias, Leticia, Vergier, Blandine, de Bossoreille, Stève, Das, Pradeep, Cluet, David, Boudaoud, Arezki, Grammont, Muriel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7703951/
https://www.ncbi.nlm.nih.gov/pubmed/33253165
http://dx.doi.org/10.1371/journal.pbio.3000940
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author Lamiré, Laurie-Anne
Milani, Pascale
Runel, Gaël
Kiss, Annamaria
Arias, Leticia
Vergier, Blandine
de Bossoreille, Stève
Das, Pradeep
Cluet, David
Boudaoud, Arezki
Grammont, Muriel
author_facet Lamiré, Laurie-Anne
Milani, Pascale
Runel, Gaël
Kiss, Annamaria
Arias, Leticia
Vergier, Blandine
de Bossoreille, Stève
Das, Pradeep
Cluet, David
Boudaoud, Arezki
Grammont, Muriel
author_sort Lamiré, Laurie-Anne
collection PubMed
description It is unknown how growth in one tissue impacts morphogenesis in a neighboring tissue. To address this, we used the Drosophila ovarian follicle, in which a cluster of 15 nurse cells and a posteriorly located oocyte are surrounded by a layer of epithelial cells. It is known that as the nurse cells grow, the overlying epithelial cells flatten in a wave that begins in the anterior. Here, we demonstrate that an anterior to posterior gradient of decreasing cytoplasmic pressure is present across the nurse cells and that this gradient acts through TGFβ to control both the triggering and the progression of the wave of epithelial cell flattening. Our data indicate that intrinsic nurse cell growth is important to control proper nurse cell pressure. Finally, we reveal that nurse cell pressure and subsequent TGFβ activity in the stretched cells combine to increase follicle elongation in the anterior, which is crucial for allowing nurse cell growth and pressure control. More generally, our results reveal that during development, inner cytoplasmic pressure in individual cells has an important role in shaping their neighbors.
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spelling pubmed-77039512020-12-03 Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis Lamiré, Laurie-Anne Milani, Pascale Runel, Gaël Kiss, Annamaria Arias, Leticia Vergier, Blandine de Bossoreille, Stève Das, Pradeep Cluet, David Boudaoud, Arezki Grammont, Muriel PLoS Biol Research Article It is unknown how growth in one tissue impacts morphogenesis in a neighboring tissue. To address this, we used the Drosophila ovarian follicle, in which a cluster of 15 nurse cells and a posteriorly located oocyte are surrounded by a layer of epithelial cells. It is known that as the nurse cells grow, the overlying epithelial cells flatten in a wave that begins in the anterior. Here, we demonstrate that an anterior to posterior gradient of decreasing cytoplasmic pressure is present across the nurse cells and that this gradient acts through TGFβ to control both the triggering and the progression of the wave of epithelial cell flattening. Our data indicate that intrinsic nurse cell growth is important to control proper nurse cell pressure. Finally, we reveal that nurse cell pressure and subsequent TGFβ activity in the stretched cells combine to increase follicle elongation in the anterior, which is crucial for allowing nurse cell growth and pressure control. More generally, our results reveal that during development, inner cytoplasmic pressure in individual cells has an important role in shaping their neighbors. Public Library of Science 2020-11-30 /pmc/articles/PMC7703951/ /pubmed/33253165 http://dx.doi.org/10.1371/journal.pbio.3000940 Text en © 2020 Lamiré et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Lamiré, Laurie-Anne
Milani, Pascale
Runel, Gaël
Kiss, Annamaria
Arias, Leticia
Vergier, Blandine
de Bossoreille, Stève
Das, Pradeep
Cluet, David
Boudaoud, Arezki
Grammont, Muriel
Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis
title Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis
title_full Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis
title_fullStr Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis
title_full_unstemmed Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis
title_short Gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis
title_sort gradient in cytoplasmic pressure in germline cells controls overlying epithelial cell morphogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7703951/
https://www.ncbi.nlm.nih.gov/pubmed/33253165
http://dx.doi.org/10.1371/journal.pbio.3000940
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