Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells
The mammalian germline is characterized by extensive epigenetic reprogramming during its development into functional eggs and sperm. Specifically, the epigenome requires resetting before parental marks can be established and transmitted to the next generation. In the female germline, X-chromosome in...
| Autores: | , , , , , , , , , , , , , , |
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| Formato: | artículo |
| Estado: | Versión publicada |
| Fecha de publicación: | 2022 |
| País: | España |
| Recursos: | Universitat Pompeu Fabra |
| Repositorio: | Repositorio Digital de la UPF |
| OAI Identifier: | oai:repositori.upf.edu:10230/53522 |
| Acesso em linha: | http://hdl.handle.net/10230/53522 http://dx.doi.org/10.15252/embj.2021109457 |
| Access Level: | acceso abierto |
| Palavra-chave: | Cromosoma X Epigenètica Cèl·lules germinals |
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Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cellsSeverino, Jacqueline, 1990-Bauer, Moritz, 1987-Mattimoe, TomArecco, NiccolòCozzuto, LucaLorden, PatriciaHamada, NorioNosaka, YoshiakiNagaoka, So I.Audergon, PaulineTarruell Pellegrin, Antonio,1990-Heyn, HolgerHayashi, KatsuhikoSaitou, MitinoriPayer, BernhardCromosoma XEpigenèticaCèl·lules germinalsThe mammalian germline is characterized by extensive epigenetic reprogramming during its development into functional eggs and sperm. Specifically, the epigenome requires resetting before parental marks can be established and transmitted to the next generation. In the female germline, X-chromosome inactivation and reactivation are among the most prominent epigenetic reprogramming events, yet very little is known about their kinetics and biological function. Here, we investigate X-inactivation and reactivation dynamics using a tailor-made in vitro system of primordial germ cell-like cell (PGCLC) differentiation from mouse embryonic stem cells. We find that X-inactivation in PGCLCs in vitro and in germ cell-competent epiblast cells in vivo is moderate compared to somatic cells, and frequently characterized by escaping genes. X-inactivation is followed by step-wise X-reactivation, which is mostly completed during meiotic prophase I. Furthermore, we find that PGCLCs which fail to undergo X-inactivation or reactivate too rapidly display impaired meiotic potential. Thus, our data reveal fine-tuned X-chromosome remodelling as a critical feature of female germ cell development towards meiosis and oogenesis.This work was supported by the Spanish Ministry of Science, Innovation and Universities (BFU2014-55275-P, BFU2017-88407-P to B.P.), the Agencia Estatal de Investigación (AEI) (EUR2019-103817 to B.P.), the AXA Research Fund (to B.P.) and the Agencia de Gestio d’Ajuts Universitaris i de Recerca (AGAUR, 2017 SGR 346 to B.P.). We would like to thank the Spanish Ministry of Economy, Industry and Competitiveness (MEIC) to the EMBL partnership and to the “Centro de Excelencia Severo Ochoa.” We also acknowledge support of the CERCA Programme of the Generalitat de Catalunya. N.A. is supported by an EMBO postdoctoral fellowship (LTF 695-2019). J.S. and M.B. were supported by La Caixa International PhD Fellowships and J.S. by a travel grant from the Company of Biologists (Development Journal). P.A. has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 751651EMBO Press202220222022info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/53522http://dx.doi.org/10.15252/embj.2021109457reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésinfo:eu-repo/grantAgreement/EC/H2020/751651info:eu-repo/grantAgreement/ES/1PE/BFU2014-55275-Pinfo:eu-repo/grantAgreement/ES/2PE/BFU2017-88407-P© 2022 Jacqueline Severino et al. Published under the terms of the CC BY 4.0 licensehttps://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/535222026-06-12T07:21:37Z |
| dc.title.none.fl_str_mv |
Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells |
| title |
Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells |
| spellingShingle |
Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells Severino, Jacqueline, 1990- Cromosoma X Epigenètica Cèl·lules germinals |
| title_short |
Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells |
| title_full |
Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells |
| title_fullStr |
Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells |
| title_full_unstemmed |
Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells |
| title_sort |
Controlled X-chromosome dynamics defines meiotic potential of female mouse in vitro germ cells |
| dc.creator.none.fl_str_mv |
Severino, Jacqueline, 1990- Bauer, Moritz, 1987- Mattimoe, Tom Arecco, Niccolò Cozzuto, Luca Lorden, Patricia Hamada, Norio Nosaka, Yoshiaki Nagaoka, So I. Audergon, Pauline Tarruell Pellegrin, Antonio,1990- Heyn, Holger Hayashi, Katsuhiko Saitou, Mitinori Payer, Bernhard |
| author |
Severino, Jacqueline, 1990- |
| author_facet |
Severino, Jacqueline, 1990- Bauer, Moritz, 1987- Mattimoe, Tom Arecco, Niccolò Cozzuto, Luca Lorden, Patricia Hamada, Norio Nosaka, Yoshiaki Nagaoka, So I. Audergon, Pauline Tarruell Pellegrin, Antonio,1990- Heyn, Holger Hayashi, Katsuhiko Saitou, Mitinori Payer, Bernhard |
| author_role |
author |
| author2 |
Bauer, Moritz, 1987- Mattimoe, Tom Arecco, Niccolò Cozzuto, Luca Lorden, Patricia Hamada, Norio Nosaka, Yoshiaki Nagaoka, So I. Audergon, Pauline Tarruell Pellegrin, Antonio,1990- Heyn, Holger Hayashi, Katsuhiko Saitou, Mitinori Payer, Bernhard |
| author2_role |
author author author author author author author author author author author author author author |
| dc.subject.none.fl_str_mv |
Cromosoma X Epigenètica Cèl·lules germinals |
| topic |
Cromosoma X Epigenètica Cèl·lules germinals |
| description |
The mammalian germline is characterized by extensive epigenetic reprogramming during its development into functional eggs and sperm. Specifically, the epigenome requires resetting before parental marks can be established and transmitted to the next generation. In the female germline, X-chromosome inactivation and reactivation are among the most prominent epigenetic reprogramming events, yet very little is known about their kinetics and biological function. Here, we investigate X-inactivation and reactivation dynamics using a tailor-made in vitro system of primordial germ cell-like cell (PGCLC) differentiation from mouse embryonic stem cells. We find that X-inactivation in PGCLCs in vitro and in germ cell-competent epiblast cells in vivo is moderate compared to somatic cells, and frequently characterized by escaping genes. X-inactivation is followed by step-wise X-reactivation, which is mostly completed during meiotic prophase I. Furthermore, we find that PGCLCs which fail to undergo X-inactivation or reactivate too rapidly display impaired meiotic potential. Thus, our data reveal fine-tuned X-chromosome remodelling as a critical feature of female germ cell development towards meiosis and oogenesis. |
| publishDate |
2022 |
| dc.date.none.fl_str_mv |
2022 2022 2022 |
| dc.type.none.fl_str_mv |
info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion |
| format |
article |
| status_str |
publishedVersion |
| dc.identifier.none.fl_str_mv |
http://hdl.handle.net/10230/53522 http://dx.doi.org/10.15252/embj.2021109457 |
| url |
http://hdl.handle.net/10230/53522 http://dx.doi.org/10.15252/embj.2021109457 |
| dc.language.none.fl_str_mv |
Inglés |
| language_invalid_str_mv |
Inglés |
| dc.relation.none.fl_str_mv |
info:eu-repo/grantAgreement/EC/H2020/751651 info:eu-repo/grantAgreement/ES/1PE/BFU2014-55275-P info:eu-repo/grantAgreement/ES/2PE/BFU2017-88407-P |
| dc.rights.none.fl_str_mv |
© 2022 Jacqueline Severino et al. Published under the terms of the CC BY 4.0 license https://creativecommons.org/licenses/by/4.0/ info:eu-repo/semantics/openAccess |
| rights_invalid_str_mv |
© 2022 Jacqueline Severino et al. Published under the terms of the CC BY 4.0 license https://creativecommons.org/licenses/by/4.0/ |
| eu_rights_str_mv |
openAccess |
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application/pdf application/pdf |
| dc.publisher.none.fl_str_mv |
EMBO Press |
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EMBO Press |
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reponame:Repositorio Digital de la UPF instname:Universitat Pompeu Fabra |
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Universitat Pompeu Fabra |
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Repositorio Digital de la UPF |
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Repositorio Digital de la UPF |
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