A transitory signaling center controls timing of primordial germ cell differentiation

Organogenesis requires exquisite spatiotemporal coordination of cell morphogenesis, migration, proliferation, and differentiation of multiple cell types. For gonads, this involves complex interactions between somatic and germline tissues. During Drosophila ovary morphogenesis, primordial germ cells...

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Main Authors: Banisch, Torsten U, Slaidina, Maija, Gupta, Selena, Ho, Megan, Gilboa, Lilach, Lehmann, Ruth
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:English
Published: Elsevier BV 2022
Online Access:https://hdl.handle.net/1721.1/146883
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author Banisch, Torsten U
Slaidina, Maija
Gupta, Selena
Ho, Megan
Gilboa, Lilach
Lehmann, Ruth
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Banisch, Torsten U
Slaidina, Maija
Gupta, Selena
Ho, Megan
Gilboa, Lilach
Lehmann, Ruth
author_sort Banisch, Torsten U
collection MIT
description Organogenesis requires exquisite spatiotemporal coordination of cell morphogenesis, migration, proliferation, and differentiation of multiple cell types. For gonads, this involves complex interactions between somatic and germline tissues. During Drosophila ovary morphogenesis, primordial germ cells (PGCs) either are sequestered in stem cell niches and are maintained in an undifferentiated germline stem cell state or transition directly toward differentiation. Here, we identify a mechanism that links hormonal triggers of somatic tissue morphogenesis with PGC differentiation. An early ecdysone pulse initiates somatic swarm cell (SwC) migration, positioning these cells close to PGCs. A second hormone peak activates Torso-like signal in SwCs, which stimulates the Torso receptor tyrosine kinase (RTK) signaling pathway in PGCs promoting their differentiation by de-repression of the differentiation gene, bag of marbles. Thus, systemic temporal cues generate a transitory signaling center that coordinates ovarian morphogenesis with stem cell self-renewal and differentiation programs, highlighting a more general role for such centers in reproductive and developmental biology.
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spelling mit-1721.1/1468832022-12-15T03:50:18Z A transitory signaling center controls timing of primordial germ cell differentiation Banisch, Torsten U Slaidina, Maija Gupta, Selena Ho, Megan Gilboa, Lilach Lehmann, Ruth Massachusetts Institute of Technology. Department of Biology Organogenesis requires exquisite spatiotemporal coordination of cell morphogenesis, migration, proliferation, and differentiation of multiple cell types. For gonads, this involves complex interactions between somatic and germline tissues. During Drosophila ovary morphogenesis, primordial germ cells (PGCs) either are sequestered in stem cell niches and are maintained in an undifferentiated germline stem cell state or transition directly toward differentiation. Here, we identify a mechanism that links hormonal triggers of somatic tissue morphogenesis with PGC differentiation. An early ecdysone pulse initiates somatic swarm cell (SwC) migration, positioning these cells close to PGCs. A second hormone peak activates Torso-like signal in SwCs, which stimulates the Torso receptor tyrosine kinase (RTK) signaling pathway in PGCs promoting their differentiation by de-repression of the differentiation gene, bag of marbles. Thus, systemic temporal cues generate a transitory signaling center that coordinates ovarian morphogenesis with stem cell self-renewal and differentiation programs, highlighting a more general role for such centers in reproductive and developmental biology. 2022-12-14T18:20:12Z 2022-12-14T18:20:12Z 2021 2022-12-14T18:16:12Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/146883 Banisch, Torsten U, Slaidina, Maija, Gupta, Selena, Ho, Megan, Gilboa, Lilach et al. 2021. "A transitory signaling center controls timing of primordial germ cell differentiation." Developmental Cell, 56 (12). en 10.1016/J.DEVCEL.2021.05.008 Developmental Cell Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier BV PMC
spellingShingle Banisch, Torsten U
Slaidina, Maija
Gupta, Selena
Ho, Megan
Gilboa, Lilach
Lehmann, Ruth
A transitory signaling center controls timing of primordial germ cell differentiation
title A transitory signaling center controls timing of primordial germ cell differentiation
title_full A transitory signaling center controls timing of primordial germ cell differentiation
title_fullStr A transitory signaling center controls timing of primordial germ cell differentiation
title_full_unstemmed A transitory signaling center controls timing of primordial germ cell differentiation
title_short A transitory signaling center controls timing of primordial germ cell differentiation
title_sort transitory signaling center controls timing of primordial germ cell differentiation
url https://hdl.handle.net/1721.1/146883
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