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Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries

In the Drosophila ovary, somatic escort cells (ECs) form a niche that promotes differentiation of germline stem cell (GSC) progeny. The piRNA (Piwi-interacting RNA) pathway, which represses transposable elements (TEs), is required in ECs to prevent the accumulation of undifferentiated germ cells (ge...

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Autores principales: Sokolova, Olesya A., Mikhaleva, Elena A., Kharitonov, Sergey L., Abramov, Yuri A., Gvozdev, Vladimir A., Klenov, Mikhail S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6978372/
https://www.ncbi.nlm.nih.gov/pubmed/31974416
http://dx.doi.org/10.1038/s41598-020-57901-2
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author Sokolova, Olesya A.
Mikhaleva, Elena A.
Kharitonov, Sergey L.
Abramov, Yuri A.
Gvozdev, Vladimir A.
Klenov, Mikhail S.
author_facet Sokolova, Olesya A.
Mikhaleva, Elena A.
Kharitonov, Sergey L.
Abramov, Yuri A.
Gvozdev, Vladimir A.
Klenov, Mikhail S.
author_sort Sokolova, Olesya A.
collection PubMed
description In the Drosophila ovary, somatic escort cells (ECs) form a niche that promotes differentiation of germline stem cell (GSC) progeny. The piRNA (Piwi-interacting RNA) pathway, which represses transposable elements (TEs), is required in ECs to prevent the accumulation of undifferentiated germ cells (germline tumor phenotype). The soma-specific piRNA cluster flamenco (flam) produces a substantial part of somatic piRNAs. Here, we characterized the biological effects of somatic TE activation on germ cell differentiation in flam mutants. We revealed that the choice between normal and tumorous phenotypes of flam mutant ovaries depends on the number of persisting ECs, which is determined at the larval stage. Accordingly, we found much more frequent DNA breaks in somatic cells of flam larval ovaries than in adult ECs. The absence of Chk2 or ATM checkpoint kinases dramatically enhanced oogenesis defects of flam mutants, in contrast to the germline TE-induced defects that are known to be mostly suppressed by сhk2 mutation. These results demonstrate a crucial role of checkpoint kinases in protecting niche cells against deleterious TE activation and suggest substantial differences between DNA damage responses in ovarian somatic and germ cells.
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spelling pubmed-69783722020-01-30 Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries Sokolova, Olesya A. Mikhaleva, Elena A. Kharitonov, Sergey L. Abramov, Yuri A. Gvozdev, Vladimir A. Klenov, Mikhail S. Sci Rep Article In the Drosophila ovary, somatic escort cells (ECs) form a niche that promotes differentiation of germline stem cell (GSC) progeny. The piRNA (Piwi-interacting RNA) pathway, which represses transposable elements (TEs), is required in ECs to prevent the accumulation of undifferentiated germ cells (germline tumor phenotype). The soma-specific piRNA cluster flamenco (flam) produces a substantial part of somatic piRNAs. Here, we characterized the biological effects of somatic TE activation on germ cell differentiation in flam mutants. We revealed that the choice between normal and tumorous phenotypes of flam mutant ovaries depends on the number of persisting ECs, which is determined at the larval stage. Accordingly, we found much more frequent DNA breaks in somatic cells of flam larval ovaries than in adult ECs. The absence of Chk2 or ATM checkpoint kinases dramatically enhanced oogenesis defects of flam mutants, in contrast to the germline TE-induced defects that are known to be mostly suppressed by сhk2 mutation. These results demonstrate a crucial role of checkpoint kinases in protecting niche cells against deleterious TE activation and suggest substantial differences between DNA damage responses in ovarian somatic and germ cells. Nature Publishing Group UK 2020-01-23 /pmc/articles/PMC6978372/ /pubmed/31974416 http://dx.doi.org/10.1038/s41598-020-57901-2 Text en © The Author(s) 2020, corrected publication 2021 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
Sokolova, Olesya A.
Mikhaleva, Elena A.
Kharitonov, Sergey L.
Abramov, Yuri A.
Gvozdev, Vladimir A.
Klenov, Mikhail S.
Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries
title Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries
title_full Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries
title_fullStr Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries
title_full_unstemmed Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries
title_short Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries
title_sort special vulnerability of somatic niche cells to transposable element activation in drosophila larval ovaries
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6978372/
https://www.ncbi.nlm.nih.gov/pubmed/31974416
http://dx.doi.org/10.1038/s41598-020-57901-2
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