A dual-function SNF2 protein drives chromatid resolution and nascent transcripts removal in mitosis
Mitotic chromatin is largely assumed incompatible with transcription due to changes in the transcription machinery and chromosome architecture. However, the mechanisms of mitotic transcriptional inactivation and their interplay with chromosome assembly remain largely unknown. By monitoring ongoing t...
Gespeichert in:
| Veröffentlicht in: | EMBO reports 2023-09, Vol.24 (9), p.e56463-e56463 |
|---|---|
| Hauptverfasser: | , , , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | e56463 |
|---|---|
| container_issue | 9 |
| container_start_page | e56463 |
| container_title | EMBO reports |
| container_volume | 24 |
| creator | Carmo, Catarina Coelho, João Silva, Rui D Tavares, Alexandra Boavida, Ana Gaetani, Paola Guilgur, Leonardo G Martinho, Rui Gonçalo Oliveira, Raquel A |
| description | Mitotic chromatin is largely assumed incompatible with transcription due to changes in the transcription machinery and chromosome architecture. However, the mechanisms of mitotic transcriptional inactivation and their interplay with chromosome assembly remain largely unknown. By monitoring ongoing transcription in Drosophila early embryos, we reveal that eviction of nascent mRNAs from mitotic chromatin occurs after substantial chromosome compaction and is not promoted by condensin I. Instead, we show that the timely removal of transcripts from mitotic chromatin is driven by the SNF2 helicase-like protein Lodestar (Lds), identified here as a modulator of sister chromatid cohesion defects. In addition to the eviction of nascent transcripts, we uncover that Lds cooperates with Topoisomerase 2 to ensure efficient sister chromatid resolution and mitotic fidelity. We conclude that the removal of nascent transcripts upon mitotic entry is not a passive consequence of cell cycle progression and/or chromosome compaction but occurs via dedicated mechanisms with functional parallelisms to sister chromatid resolution. |
| doi_str_mv | 10.15252/embr.202256463 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10481674</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2861166001</sourcerecordid><originalsourceid>FETCH-LOGICAL-p323t-5e51278db9e966a0076baae6648e7d28acb29427e0726433ab625a2cf9c3d9993</originalsourceid><addsrcrecordid>eNpdkUtr3TAQhUVJyKtZd1cE2XTjRBrJkrUq4ZJHISSLtJCdGdu6jYItuZJ8If--anJbmqxmmPnmcA5DyCfOTnkNNZzZqYunwABqJZX4QA64VKYSXDc72x6AP-yTw5SeGGO10c0e2RdaqjIXB6Q_p8OCY7VefJ9d8PT-9hLoHEO2ztMhuo1NtH-MYcLsBhptCuPyAqIfqMfUW59pjuhTH92cU0GmsMGRlvPJ5ZBc-kh21zgme7ytR-TH5cX31XV1c3f1bXV-U80CRK5qW3PQzdAZa5RCxrTqEK1SsrF6gAb7DowEbZkGJYXATkGN0K9NLwZjjDgiX19156Wb7PDHWcSxnaObMD63AV37duPdY_szbFrOZMOVlkXhy1Yhhl-LTbmdXEk4juhtWFILjTAgG62goCfv0KewRF_yFUpxrhRjvFCf_7f0z8vfB4jfhamJvw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2861166001</pqid></control><display><type>article</type><title>A dual-function SNF2 protein drives chromatid resolution and nascent transcripts removal in mitosis</title><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Access via Wiley Online Library</source><source>Wiley Online Library (Open Access Collection)</source><source>PubMed Central</source><source>Springer Nature OA/Free Journals</source><creator>Carmo, Catarina ; Coelho, João ; Silva, Rui D ; Tavares, Alexandra ; Boavida, Ana ; Gaetani, Paola ; Guilgur, Leonardo G ; Martinho, Rui Gonçalo ; Oliveira, Raquel A</creator><creatorcontrib>Carmo, Catarina ; Coelho, João ; Silva, Rui D ; Tavares, Alexandra ; Boavida, Ana ; Gaetani, Paola ; Guilgur, Leonardo G ; Martinho, Rui Gonçalo ; Oliveira, Raquel A</creatorcontrib><description>Mitotic chromatin is largely assumed incompatible with transcription due to changes in the transcription machinery and chromosome architecture. However, the mechanisms of mitotic transcriptional inactivation and their interplay with chromosome assembly remain largely unknown. By monitoring ongoing transcription in Drosophila early embryos, we reveal that eviction of nascent mRNAs from mitotic chromatin occurs after substantial chromosome compaction and is not promoted by condensin I. Instead, we show that the timely removal of transcripts from mitotic chromatin is driven by the SNF2 helicase-like protein Lodestar (Lds), identified here as a modulator of sister chromatid cohesion defects. In addition to the eviction of nascent transcripts, we uncover that Lds cooperates with Topoisomerase 2 to ensure efficient sister chromatid resolution and mitotic fidelity. We conclude that the removal of nascent transcripts upon mitotic entry is not a passive consequence of cell cycle progression and/or chromosome compaction but occurs via dedicated mechanisms with functional parallelisms to sister chromatid resolution.</description><identifier>ISSN: 1469-221X</identifier><identifier>EISSN: 1469-3178</identifier><identifier>DOI: 10.15252/embr.202256463</identifier><identifier>PMID: 37462213</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Accuracy ; Cell cycle ; Chromatin ; Chromosomes ; Cohesion ; Compaction ; Condensin ; Defects ; DNA helicase ; DNA topoisomerase ; Embryos ; Fidelity ; Gene expression ; Inactivation ; Mitosis ; Proteins ; Snf2 protein ; Transcription ; Transcription factors ; Yeast</subject><ispartof>EMBO reports, 2023-09, Vol.24 (9), p.e56463-e56463</ispartof><rights>2023 The Authors. Published under the terms of the CC BY NC ND 4.0 license.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0002-1641-3403 ; 0000-0002-8293-8603 ; 0000-0003-3668-4291 ; 0000-0003-4786-6189 ; 0000-0002-5332-3386 ; 0000-0003-0083-0146 ; 0000-0002-8197-5920</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10481674/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10481674/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,887,27933,27934,53800,53802</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37462213$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Carmo, Catarina</creatorcontrib><creatorcontrib>Coelho, João</creatorcontrib><creatorcontrib>Silva, Rui D</creatorcontrib><creatorcontrib>Tavares, Alexandra</creatorcontrib><creatorcontrib>Boavida, Ana</creatorcontrib><creatorcontrib>Gaetani, Paola</creatorcontrib><creatorcontrib>Guilgur, Leonardo G</creatorcontrib><creatorcontrib>Martinho, Rui Gonçalo</creatorcontrib><creatorcontrib>Oliveira, Raquel A</creatorcontrib><title>A dual-function SNF2 protein drives chromatid resolution and nascent transcripts removal in mitosis</title><title>EMBO reports</title><addtitle>EMBO Rep</addtitle><description>Mitotic chromatin is largely assumed incompatible with transcription due to changes in the transcription machinery and chromosome architecture. However, the mechanisms of mitotic transcriptional inactivation and their interplay with chromosome assembly remain largely unknown. By monitoring ongoing transcription in Drosophila early embryos, we reveal that eviction of nascent mRNAs from mitotic chromatin occurs after substantial chromosome compaction and is not promoted by condensin I. Instead, we show that the timely removal of transcripts from mitotic chromatin is driven by the SNF2 helicase-like protein Lodestar (Lds), identified here as a modulator of sister chromatid cohesion defects. In addition to the eviction of nascent transcripts, we uncover that Lds cooperates with Topoisomerase 2 to ensure efficient sister chromatid resolution and mitotic fidelity. We conclude that the removal of nascent transcripts upon mitotic entry is not a passive consequence of cell cycle progression and/or chromosome compaction but occurs via dedicated mechanisms with functional parallelisms to sister chromatid resolution.</description><subject>Accuracy</subject><subject>Cell cycle</subject><subject>Chromatin</subject><subject>Chromosomes</subject><subject>Cohesion</subject><subject>Compaction</subject><subject>Condensin</subject><subject>Defects</subject><subject>DNA helicase</subject><subject>DNA topoisomerase</subject><subject>Embryos</subject><subject>Fidelity</subject><subject>Gene expression</subject><subject>Inactivation</subject><subject>Mitosis</subject><subject>Proteins</subject><subject>Snf2 protein</subject><subject>Transcription</subject><subject>Transcription factors</subject><subject>Yeast</subject><issn>1469-221X</issn><issn>1469-3178</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNpdkUtr3TAQhUVJyKtZd1cE2XTjRBrJkrUq4ZJHISSLtJCdGdu6jYItuZJ8If--anJbmqxmmPnmcA5DyCfOTnkNNZzZqYunwABqJZX4QA64VKYSXDc72x6AP-yTw5SeGGO10c0e2RdaqjIXB6Q_p8OCY7VefJ9d8PT-9hLoHEO2ztMhuo1NtH-MYcLsBhptCuPyAqIfqMfUW59pjuhTH92cU0GmsMGRlvPJ5ZBc-kh21zgme7ytR-TH5cX31XV1c3f1bXV-U80CRK5qW3PQzdAZa5RCxrTqEK1SsrF6gAb7DowEbZkGJYXATkGN0K9NLwZjjDgiX19156Wb7PDHWcSxnaObMD63AV37duPdY_szbFrOZMOVlkXhy1Yhhl-LTbmdXEk4juhtWFILjTAgG62goCfv0KewRF_yFUpxrhRjvFCf_7f0z8vfB4jfhamJvw</recordid><startdate>20230906</startdate><enddate>20230906</enddate><creator>Carmo, Catarina</creator><creator>Coelho, João</creator><creator>Silva, Rui D</creator><creator>Tavares, Alexandra</creator><creator>Boavida, Ana</creator><creator>Gaetani, Paola</creator><creator>Guilgur, Leonardo G</creator><creator>Martinho, Rui Gonçalo</creator><creator>Oliveira, Raquel A</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>NPM</scope><scope>7QL</scope><scope>7T5</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1641-3403</orcidid><orcidid>https://orcid.org/0000-0002-8293-8603</orcidid><orcidid>https://orcid.org/0000-0003-3668-4291</orcidid><orcidid>https://orcid.org/0000-0003-4786-6189</orcidid><orcidid>https://orcid.org/0000-0002-5332-3386</orcidid><orcidid>https://orcid.org/0000-0003-0083-0146</orcidid><orcidid>https://orcid.org/0000-0002-8197-5920</orcidid></search><sort><creationdate>20230906</creationdate><title>A dual-function SNF2 protein drives chromatid resolution and nascent transcripts removal in mitosis</title><author>Carmo, Catarina ; Coelho, João ; Silva, Rui D ; Tavares, Alexandra ; Boavida, Ana ; Gaetani, Paola ; Guilgur, Leonardo G ; Martinho, Rui Gonçalo ; Oliveira, Raquel A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p323t-5e51278db9e966a0076baae6648e7d28acb29427e0726433ab625a2cf9c3d9993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Accuracy</topic><topic>Cell cycle</topic><topic>Chromatin</topic><topic>Chromosomes</topic><topic>Cohesion</topic><topic>Compaction</topic><topic>Condensin</topic><topic>Defects</topic><topic>DNA helicase</topic><topic>DNA topoisomerase</topic><topic>Embryos</topic><topic>Fidelity</topic><topic>Gene expression</topic><topic>Inactivation</topic><topic>Mitosis</topic><topic>Proteins</topic><topic>Snf2 protein</topic><topic>Transcription</topic><topic>Transcription factors</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Carmo, Catarina</creatorcontrib><creatorcontrib>Coelho, João</creatorcontrib><creatorcontrib>Silva, Rui D</creatorcontrib><creatorcontrib>Tavares, Alexandra</creatorcontrib><creatorcontrib>Boavida, Ana</creatorcontrib><creatorcontrib>Gaetani, Paola</creatorcontrib><creatorcontrib>Guilgur, Leonardo G</creatorcontrib><creatorcontrib>Martinho, Rui Gonçalo</creatorcontrib><creatorcontrib>Oliveira, Raquel A</creatorcontrib><collection>PubMed</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>EMBO reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Carmo, Catarina</au><au>Coelho, João</au><au>Silva, Rui D</au><au>Tavares, Alexandra</au><au>Boavida, Ana</au><au>Gaetani, Paola</au><au>Guilgur, Leonardo G</au><au>Martinho, Rui Gonçalo</au><au>Oliveira, Raquel A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A dual-function SNF2 protein drives chromatid resolution and nascent transcripts removal in mitosis</atitle><jtitle>EMBO reports</jtitle><addtitle>EMBO Rep</addtitle><date>2023-09-06</date><risdate>2023</risdate><volume>24</volume><issue>9</issue><spage>e56463</spage><epage>e56463</epage><pages>e56463-e56463</pages><issn>1469-221X</issn><eissn>1469-3178</eissn><abstract>Mitotic chromatin is largely assumed incompatible with transcription due to changes in the transcription machinery and chromosome architecture. However, the mechanisms of mitotic transcriptional inactivation and their interplay with chromosome assembly remain largely unknown. By monitoring ongoing transcription in Drosophila early embryos, we reveal that eviction of nascent mRNAs from mitotic chromatin occurs after substantial chromosome compaction and is not promoted by condensin I. Instead, we show that the timely removal of transcripts from mitotic chromatin is driven by the SNF2 helicase-like protein Lodestar (Lds), identified here as a modulator of sister chromatid cohesion defects. In addition to the eviction of nascent transcripts, we uncover that Lds cooperates with Topoisomerase 2 to ensure efficient sister chromatid resolution and mitotic fidelity. We conclude that the removal of nascent transcripts upon mitotic entry is not a passive consequence of cell cycle progression and/or chromosome compaction but occurs via dedicated mechanisms with functional parallelisms to sister chromatid resolution.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>37462213</pmid><doi>10.15252/embr.202256463</doi><orcidid>https://orcid.org/0000-0002-1641-3403</orcidid><orcidid>https://orcid.org/0000-0002-8293-8603</orcidid><orcidid>https://orcid.org/0000-0003-3668-4291</orcidid><orcidid>https://orcid.org/0000-0003-4786-6189</orcidid><orcidid>https://orcid.org/0000-0002-5332-3386</orcidid><orcidid>https://orcid.org/0000-0003-0083-0146</orcidid><orcidid>https://orcid.org/0000-0002-8197-5920</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1469-221X |
| ispartof | EMBO reports, 2023-09, Vol.24 (9), p.e56463-e56463 |
| issn | 1469-221X 1469-3178 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10481674 |
| source | Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Access via Wiley Online Library; Wiley Online Library (Open Access Collection); PubMed Central; Springer Nature OA/Free Journals |
| subjects | Accuracy Cell cycle Chromatin Chromosomes Cohesion Compaction Condensin Defects DNA helicase DNA topoisomerase Embryos Fidelity Gene expression Inactivation Mitosis Proteins Snf2 protein Transcription Transcription factors Yeast |
| title | A dual-function SNF2 protein drives chromatid resolution and nascent transcripts removal in mitosis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-03T01%3A26%3A57IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20dual-function%20SNF2%20protein%20drives%20chromatid%20resolution%20and%20nascent%20transcripts%20removal%20in%20mitosis&rft.jtitle=EMBO%20reports&rft.au=Carmo,%20Catarina&rft.date=2023-09-06&rft.volume=24&rft.issue=9&rft.spage=e56463&rft.epage=e56463&rft.pages=e56463-e56463&rft.issn=1469-221X&rft.eissn=1469-3178&rft_id=info:doi/10.15252/embr.202256463&rft_dat=%3Cproquest_pubme%3E2861166001%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2861166001&rft_id=info:pmid/37462213&rfr_iscdi=true |