Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis

Bibliographic Details
Main Author: Feijão, Tália
Publication Date: 2022
Other Authors: Marques, Bruno, Silva, Rui D., Carvalho, Célia, Sobral, Daniel, Matos, Ricardo, Tan, Tian, Pereira, António, Morais de Sá, Eurico, Maiato, Hélder, DeLuca, Steven Z., Martinho, Rui Goncalo
Format: Article
Language: eng
Source: Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
Download full: http://hdl.handle.net/10451/54839
Summary: Copyright © 2022 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
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spelling Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosisPolycomb group proteinsMeiosisPolycomplexesSynaptonemal complexTranscriptionCopyright © 2022 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).The synaptonemal complex (SC) is a proteinaceous scaffold that is assembled between paired homologous chromosomes during the onset of meiosis. Timely expression of SC coding genes is essential for SC assembly and successful meiosis. However, SC components have an intrinsic tendency to self-organize into abnormal repetitive structures, which are not assembled between the paired homologs and whose formation is potentially deleterious for meiosis and gametogenesis. This creates an interesting conundrum, where SC genes need to be robustly expressed during meiosis, but their expression must be carefully regulated to prevent the formation of anomalous SC structures. In this manuscript, we show that the Polycomb group protein Sfmbt, the Drosophila ortholog of human MBTD1 and L3MBTL2, is required to avoid excessive expression of SC genes during prophase I. Although SC assembly is normal after Sfmbt depletion, SC disassembly is abnormal with the formation of multiple synaptonemal complexes (polycomplexes) within the oocyte. Overexpression of the SC gene corona and depletion of other Polycomb group proteins are similarly associated with polycomplex formation during SC disassembly. These polycomplexes are highly dynamic and have a well-defined periodic structure. Further confirming the importance of Sfmbt, germ line depletion of this protein is associated with significant metaphase I defects and a reduction in female fertility. Since transcription of SC genes mostly occurs during early prophase I, our results suggest a role of Sfmbt and other Polycomb group proteins in downregulating the expression of these and other early prophase I genes during later stages of meiosis.R.G.M. is supported by Portuguese national funding through Fundação para a Ciência e a Tecnologia (FCT grant refs. PTDC/BIA-BID/28441/2017 and PTDC/BIA-BID/1606/2020). B.M. and R.D.S. are both supported by Portuguese national funding through Fundação para a Ciência e a Tecnologia, respectively, PD/BD/128342/2017 (within the scope of the ProRegeM PhD program; PD/00117/2012, CRM:0027030) and DL 57/2016/CP1361/CT0019. The Light Microscopy Unit of ABC-RI was partially supported by Portuguese national funding (FCT: PPBI-POCI-01-0145-FEDER-022122). This work was developed with the support of the research infrastructure Congento (project LISBOA-01-0145-FEDER-022170). The Transgenic RNAi Project (TRiP) collection at Harvard Medical School was supported by NIH/NIGMS R01-GM084947.National Academy of ScienceRepositório da Universidade de LisboaFeijão, TáliaMarques, BrunoSilva, Rui D.Carvalho, CéliaSobral, DanielMatos, RicardoTan, TianPereira, AntónioMorais de Sá, EuricoMaiato, HélderDeLuca, Steven Z.Martinho, Rui Goncalo2022-10-20T14:42:05Z20222022-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10451/54839engProc Natl Acad Sci USA . 2022 Oct 18;119(42):e22047011190027-842410.1073/pnas.22047011191091-6490info:eu-repo/semantics/openAccessreponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiainstacron:RCAAP2025-03-17T14:50:28Zoai:repositorio.ulisboa.pt:10451/54839Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireinfo@rcaap.ptopendoar:https://opendoar.ac.uk/repository/71602025-05-29T03:26:29.248869Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiafalse
dc.title.none.fl_str_mv Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis
title Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis
spellingShingle Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis
Feijão, Tália
Polycomb group proteins
Meiosis
Polycomplexes
Synaptonemal complex
Transcription
title_short Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis
title_full Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis
title_fullStr Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis
title_full_unstemmed Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis
title_sort Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis
author Feijão, Tália
author_facet Feijão, Tália
Marques, Bruno
Silva, Rui D.
Carvalho, Célia
Sobral, Daniel
Matos, Ricardo
Tan, Tian
Pereira, António
Morais de Sá, Eurico
Maiato, Hélder
DeLuca, Steven Z.
Martinho, Rui Goncalo
author_role author
author2 Marques, Bruno
Silva, Rui D.
Carvalho, Célia
Sobral, Daniel
Matos, Ricardo
Tan, Tian
Pereira, António
Morais de Sá, Eurico
Maiato, Hélder
DeLuca, Steven Z.
Martinho, Rui Goncalo
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Repositório da Universidade de Lisboa
dc.contributor.author.fl_str_mv Feijão, Tália
Marques, Bruno
Silva, Rui D.
Carvalho, Célia
Sobral, Daniel
Matos, Ricardo
Tan, Tian
Pereira, António
Morais de Sá, Eurico
Maiato, Hélder
DeLuca, Steven Z.
Martinho, Rui Goncalo
dc.subject.por.fl_str_mv Polycomb group proteins
Meiosis
Polycomplexes
Synaptonemal complex
Transcription
topic Polycomb group proteins
Meiosis
Polycomplexes
Synaptonemal complex
Transcription
description Copyright © 2022 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
publishDate 2022
dc.date.none.fl_str_mv 2022-10-20T14:42:05Z
2022
2022-01-01T00:00:00Z
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dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Proc Natl Acad Sci USA . 2022 Oct 18;119(42):e2204701119
0027-8424
10.1073/pnas.2204701119
1091-6490
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dc.publisher.none.fl_str_mv National Academy of Science
publisher.none.fl_str_mv National Academy of Science
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instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologia
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reponame_str Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
collection Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
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