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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Format: | Article |
Language: | English |
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Elsevier BV
2022
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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. |
first_indexed | 2024-09-23T08:21:12Z |
format | Article |
id | mit-1721.1/146883 |
institution | Massachusetts Institute of Technology |
language | English |
last_indexed | 2024-09-23T08:21:12Z |
publishDate | 2022 |
publisher | Elsevier BV |
record_format | dspace |
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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