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E-cadherin acts as a positive regulator of the JAK-STAT signaling pathway during Drosophila oogenesis

The JAK-STAT pathway is evolutionary conserved. The simplicity of this signaling in Drosophila, due to the limited redundancy between pathway components, makes it an ideal model for investigation. In the Drosophila follicular epithelium, highly stereotyped functions of JAK-STAT signaling have been w...

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Autores principales: Mallart, Charlotte, Chalvet, Fabienne, Netter, Sophie, Torres, Alba Yurani, Poidevin, Mickael, Montagne, Jacques, Pret, Anne-Marie, Malartre, Marianne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9473917/
https://www.ncbi.nlm.nih.gov/pubmed/36120588
http://dx.doi.org/10.3389/fcell.2022.886312
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author Mallart, Charlotte
Chalvet, Fabienne
Netter, Sophie
Torres, Alba Yurani
Poidevin, Mickael
Montagne, Jacques
Pret, Anne-Marie
Malartre, Marianne
author_facet Mallart, Charlotte
Chalvet, Fabienne
Netter, Sophie
Torres, Alba Yurani
Poidevin, Mickael
Montagne, Jacques
Pret, Anne-Marie
Malartre, Marianne
author_sort Mallart, Charlotte
collection PubMed
description The JAK-STAT pathway is evolutionary conserved. The simplicity of this signaling in Drosophila, due to the limited redundancy between pathway components, makes it an ideal model for investigation. In the Drosophila follicular epithelium, highly stereotyped functions of JAK-STAT signaling have been well characterized, but how signaling activity is regulated precisely to allow the different outcomes is not well understood. In this tissue, the ligand is secreted by the polar cells positioned at each follicle extremity, thus generating a gradient of JAK-STAT activity in adjacent cells. One way to control the delivered quantity of ligand is by regulating the number of polar cells, which is reduced by apoptosis to exactly two at each pole by mid-oogenesis. Hence, JAK-STAT activity is described as symmetrical between follicle anterior and posterior regions. Here, we show that JAK-STAT signaling activity is actually highly dynamic, resulting in asymmetry between poles by mid-oogenesis. Interestingly, we found similar temporal dynamics at follicle poles in the accumulation of the adherens junction E-cadherin protein. Remarkably, E-cadherin and JAK-STAT signaling not only display patterning overlaps but also share functions during oogenesis. In particular, we show that E-cadherin, like JAK-STAT signaling, regulates polar cell apoptosis non-cell-autonomously from follicle cells. Finally, our work reveals that E-cadherin is required for optimal JAK-STAT activity throughout oogenesis and that E-cadherin and Stat92E, the transcription factor of the pathway, form part of a physical complex in follicle cells. Taken together, our study establishes E-cadherin as a new positive regulator of JAK-STAT signaling during oogenesis.
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spelling pubmed-94739172022-09-15 E-cadherin acts as a positive regulator of the JAK-STAT signaling pathway during Drosophila oogenesis Mallart, Charlotte Chalvet, Fabienne Netter, Sophie Torres, Alba Yurani Poidevin, Mickael Montagne, Jacques Pret, Anne-Marie Malartre, Marianne Front Cell Dev Biol Cell and Developmental Biology The JAK-STAT pathway is evolutionary conserved. The simplicity of this signaling in Drosophila, due to the limited redundancy between pathway components, makes it an ideal model for investigation. In the Drosophila follicular epithelium, highly stereotyped functions of JAK-STAT signaling have been well characterized, but how signaling activity is regulated precisely to allow the different outcomes is not well understood. In this tissue, the ligand is secreted by the polar cells positioned at each follicle extremity, thus generating a gradient of JAK-STAT activity in adjacent cells. One way to control the delivered quantity of ligand is by regulating the number of polar cells, which is reduced by apoptosis to exactly two at each pole by mid-oogenesis. Hence, JAK-STAT activity is described as symmetrical between follicle anterior and posterior regions. Here, we show that JAK-STAT signaling activity is actually highly dynamic, resulting in asymmetry between poles by mid-oogenesis. Interestingly, we found similar temporal dynamics at follicle poles in the accumulation of the adherens junction E-cadherin protein. Remarkably, E-cadherin and JAK-STAT signaling not only display patterning overlaps but also share functions during oogenesis. In particular, we show that E-cadherin, like JAK-STAT signaling, regulates polar cell apoptosis non-cell-autonomously from follicle cells. Finally, our work reveals that E-cadherin is required for optimal JAK-STAT activity throughout oogenesis and that E-cadherin and Stat92E, the transcription factor of the pathway, form part of a physical complex in follicle cells. Taken together, our study establishes E-cadherin as a new positive regulator of JAK-STAT signaling during oogenesis. Frontiers Media S.A. 2022-08-23 /pmc/articles/PMC9473917/ /pubmed/36120588 http://dx.doi.org/10.3389/fcell.2022.886312 Text en Copyright © 2022 Mallart, Chalvet, Netter, Torres, Poidevin, Montagne, Pret and Malartre. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Mallart, Charlotte
Chalvet, Fabienne
Netter, Sophie
Torres, Alba Yurani
Poidevin, Mickael
Montagne, Jacques
Pret, Anne-Marie
Malartre, Marianne
E-cadherin acts as a positive regulator of the JAK-STAT signaling pathway during Drosophila oogenesis
title E-cadherin acts as a positive regulator of the JAK-STAT signaling pathway during Drosophila oogenesis
title_full E-cadherin acts as a positive regulator of the JAK-STAT signaling pathway during Drosophila oogenesis
title_fullStr E-cadherin acts as a positive regulator of the JAK-STAT signaling pathway during Drosophila oogenesis
title_full_unstemmed E-cadherin acts as a positive regulator of the JAK-STAT signaling pathway during Drosophila oogenesis
title_short E-cadherin acts as a positive regulator of the JAK-STAT signaling pathway during Drosophila oogenesis
title_sort e-cadherin acts as a positive regulator of the jak-stat signaling pathway during drosophila oogenesis
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9473917/
https://www.ncbi.nlm.nih.gov/pubmed/36120588
http://dx.doi.org/10.3389/fcell.2022.886312
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