Cyclin B1 is essential for mitosis in mouse embryos, and its nuclear export sets the time for mitosis

There is remarkable redundancy between the Cyclin-Cdk complexes that comprise the cell cycle machinery. None of the mammalian A-, D-, or E-type cyclins are required in development until implantation, and only Cdk1 is essential for early cell divisions. Cyclin B1 is essential for development, but whe...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:The Journal of cell biology 2018-01, Vol.217 (1), p.179-193
Hauptverfasser: Strauss, Bernhard, Harrison, Andrew, Coelho, Paula Almeida, Yata, Keiko, Zernicka-Goetz, Magdalena, Pines, Jonathon
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 193
container_issue 1
container_start_page 179
container_title The Journal of cell biology
container_volume 217
creator Strauss, Bernhard
Harrison, Andrew
Coelho, Paula Almeida
Yata, Keiko
Zernicka-Goetz, Magdalena
Pines, Jonathon
description There is remarkable redundancy between the Cyclin-Cdk complexes that comprise the cell cycle machinery. None of the mammalian A-, D-, or E-type cyclins are required in development until implantation, and only Cdk1 is essential for early cell divisions. Cyclin B1 is essential for development, but whether it is required for cell division is contentious. Here, we used a novel imaging approach to analyze Cyclin B1-null embryos from fertilization onward. We show that Cyclin B1 embryos arrest in G2 phase after just two divisions. This is the earliest arrest of any Cyclin known and places Cyclin B1 with cdk1 as the essential regulators of the cell cycle. We reintroduced mutant proteins into this genetically null background to determine why Cyclin B1 is constantly exported from the nucleus. We found that Cyclin B1 must be exported from the nucleus for the cell to prevent premature entry to mitosis, and retaining Cyclin B1-Cdk1 at the plasma membrane precludes entry to mitosis.
doi_str_mv 10.1083/jcb.201612147
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5748970</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1990815796</sourcerecordid><originalsourceid>FETCH-LOGICAL-c481t-94cb87071cf4e72923c3acffc0155e69fd5319b221f63cc60737d5e5a8391c703</originalsourceid><addsrcrecordid>eNpdkc2LFDEQxYMo7uzq0asEvHiw16p8dDoXQQe_YMGLnkM6U-1m6O6MSffi_PdGdx1WTwWvfjzq1WPsGcIlQidf70N_KQBbFKjMA7ZBraDpUMFDtgEQ2Fgt9Bk7L2UPAMoo-ZidCQtGGTAbRttjGOPM3yGPhVMpNC_Rj3xImU9xSaWqdT2ltRCnqc_HVF5xP-94XAqf1zCSz5x-HlJeeKGqLdfElzjRfYsn7NHgx0JP7-YF-_bh_dftp-bqy8fP27dXTVAdLo1Voe_qWRgGRUZYIYP0YRgCoNbU2mGnJdpeCBxaGUILRpqdJu07aTEYkBfsza3vYe0n2oUaJvvRHXKcfD665KP7dzPHa_c93ThtVGf_GLy8M8jpx0plcVMsgcbRz1Rf4NBW0kgUqqIv_kP3ac1zjVcpCx1qY9tKNbdUyKmUTMPpGAT3u0BXC3SnAiv__H6CE_23MfkLb0WW2w</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1990815796</pqid></control><display><type>article</type><title>Cyclin B1 is essential for mitosis in mouse embryos, and its nuclear export sets the time for mitosis</title><source>MEDLINE</source><source>Alma/SFX Local Collection</source><source>EZB Electronic Journals Library</source><creator>Strauss, Bernhard ; Harrison, Andrew ; Coelho, Paula Almeida ; Yata, Keiko ; Zernicka-Goetz, Magdalena ; Pines, Jonathon</creator><creatorcontrib>Strauss, Bernhard ; Harrison, Andrew ; Coelho, Paula Almeida ; Yata, Keiko ; Zernicka-Goetz, Magdalena ; Pines, Jonathon</creatorcontrib><description>There is remarkable redundancy between the Cyclin-Cdk complexes that comprise the cell cycle machinery. None of the mammalian A-, D-, or E-type cyclins are required in development until implantation, and only Cdk1 is essential for early cell divisions. Cyclin B1 is essential for development, but whether it is required for cell division is contentious. Here, we used a novel imaging approach to analyze Cyclin B1-null embryos from fertilization onward. We show that Cyclin B1 embryos arrest in G2 phase after just two divisions. This is the earliest arrest of any Cyclin known and places Cyclin B1 with cdk1 as the essential regulators of the cell cycle. We reintroduced mutant proteins into this genetically null background to determine why Cyclin B1 is constantly exported from the nucleus. We found that Cyclin B1 must be exported from the nucleus for the cell to prevent premature entry to mitosis, and retaining Cyclin B1-Cdk1 at the plasma membrane precludes entry to mitosis.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.201612147</identifier><identifier>PMID: 29074707</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Active Transport, Cell Nucleus - physiology ; Animals ; CDC2 Protein Kinase - genetics ; cdc25 Phosphatases - metabolism ; Cell cycle ; Cell Cycle Proteins - metabolism ; Cell division ; Cyclin B1 ; Cyclin B1 - genetics ; Cyclins ; DNA-Binding Proteins - metabolism ; Embryonic Development - genetics ; Embryos ; Fertilization ; G2 phase ; Implantation ; Machinery and equipment ; Mice ; Mice, Knockout ; Mitosis ; Mitosis - genetics ; Mutation ; Nuclear Proteins - metabolism ; Nuclear transport ; Nuclei (cytology) ; Phosphorylation ; Protein-Tyrosine Kinases - metabolism ; Proteins ; Redundancy ; Regulators ; Transcription Factors - metabolism ; Transplants &amp; implants</subject><ispartof>The Journal of cell biology, 2018-01, Vol.217 (1), p.179-193</ispartof><rights>2018 Strauss et al.</rights><rights>Copyright Rockefeller University Press Jan 2018</rights><rights>2018 Strauss et al. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c481t-94cb87071cf4e72923c3acffc0155e69fd5319b221f63cc60737d5e5a8391c703</citedby><cites>FETCH-LOGICAL-c481t-94cb87071cf4e72923c3acffc0155e69fd5319b221f63cc60737d5e5a8391c703</cites><orcidid>0000-0002-5227-6004 ; 0000-0001-7648-4898 ; 0000-0003-0614-7575 ; 0000-0002-3778-8415</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29074707$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Strauss, Bernhard</creatorcontrib><creatorcontrib>Harrison, Andrew</creatorcontrib><creatorcontrib>Coelho, Paula Almeida</creatorcontrib><creatorcontrib>Yata, Keiko</creatorcontrib><creatorcontrib>Zernicka-Goetz, Magdalena</creatorcontrib><creatorcontrib>Pines, Jonathon</creatorcontrib><title>Cyclin B1 is essential for mitosis in mouse embryos, and its nuclear export sets the time for mitosis</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>There is remarkable redundancy between the Cyclin-Cdk complexes that comprise the cell cycle machinery. None of the mammalian A-, D-, or E-type cyclins are required in development until implantation, and only Cdk1 is essential for early cell divisions. Cyclin B1 is essential for development, but whether it is required for cell division is contentious. Here, we used a novel imaging approach to analyze Cyclin B1-null embryos from fertilization onward. We show that Cyclin B1 embryos arrest in G2 phase after just two divisions. This is the earliest arrest of any Cyclin known and places Cyclin B1 with cdk1 as the essential regulators of the cell cycle. We reintroduced mutant proteins into this genetically null background to determine why Cyclin B1 is constantly exported from the nucleus. We found that Cyclin B1 must be exported from the nucleus for the cell to prevent premature entry to mitosis, and retaining Cyclin B1-Cdk1 at the plasma membrane precludes entry to mitosis.</description><subject>Active Transport, Cell Nucleus - physiology</subject><subject>Animals</subject><subject>CDC2 Protein Kinase - genetics</subject><subject>cdc25 Phosphatases - metabolism</subject><subject>Cell cycle</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Cell division</subject><subject>Cyclin B1</subject><subject>Cyclin B1 - genetics</subject><subject>Cyclins</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Embryonic Development - genetics</subject><subject>Embryos</subject><subject>Fertilization</subject><subject>G2 phase</subject><subject>Implantation</subject><subject>Machinery and equipment</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Mitosis</subject><subject>Mitosis - genetics</subject><subject>Mutation</subject><subject>Nuclear Proteins - metabolism</subject><subject>Nuclear transport</subject><subject>Nuclei (cytology)</subject><subject>Phosphorylation</subject><subject>Protein-Tyrosine Kinases - metabolism</subject><subject>Proteins</subject><subject>Redundancy</subject><subject>Regulators</subject><subject>Transcription Factors - metabolism</subject><subject>Transplants &amp; implants</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc2LFDEQxYMo7uzq0asEvHiw16p8dDoXQQe_YMGLnkM6U-1m6O6MSffi_PdGdx1WTwWvfjzq1WPsGcIlQidf70N_KQBbFKjMA7ZBraDpUMFDtgEQ2Fgt9Bk7L2UPAMoo-ZidCQtGGTAbRttjGOPM3yGPhVMpNC_Rj3xImU9xSaWqdT2ltRCnqc_HVF5xP-94XAqf1zCSz5x-HlJeeKGqLdfElzjRfYsn7NHgx0JP7-YF-_bh_dftp-bqy8fP27dXTVAdLo1Voe_qWRgGRUZYIYP0YRgCoNbU2mGnJdpeCBxaGUILRpqdJu07aTEYkBfsza3vYe0n2oUaJvvRHXKcfD665KP7dzPHa_c93ThtVGf_GLy8M8jpx0plcVMsgcbRz1Rf4NBW0kgUqqIv_kP3ac1zjVcpCx1qY9tKNbdUyKmUTMPpGAT3u0BXC3SnAiv__H6CE_23MfkLb0WW2w</recordid><startdate>20180102</startdate><enddate>20180102</enddate><creator>Strauss, Bernhard</creator><creator>Harrison, Andrew</creator><creator>Coelho, Paula Almeida</creator><creator>Yata, Keiko</creator><creator>Zernicka-Goetz, Magdalena</creator><creator>Pines, Jonathon</creator><general>Rockefeller University Press</general><general>The Rockefeller University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5227-6004</orcidid><orcidid>https://orcid.org/0000-0001-7648-4898</orcidid><orcidid>https://orcid.org/0000-0003-0614-7575</orcidid><orcidid>https://orcid.org/0000-0002-3778-8415</orcidid></search><sort><creationdate>20180102</creationdate><title>Cyclin B1 is essential for mitosis in mouse embryos, and its nuclear export sets the time for mitosis</title><author>Strauss, Bernhard ; Harrison, Andrew ; Coelho, Paula Almeida ; Yata, Keiko ; Zernicka-Goetz, Magdalena ; Pines, Jonathon</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c481t-94cb87071cf4e72923c3acffc0155e69fd5319b221f63cc60737d5e5a8391c703</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Active Transport, Cell Nucleus - physiology</topic><topic>Animals</topic><topic>CDC2 Protein Kinase - genetics</topic><topic>cdc25 Phosphatases - metabolism</topic><topic>Cell cycle</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Cell division</topic><topic>Cyclin B1</topic><topic>Cyclin B1 - genetics</topic><topic>Cyclins</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Embryonic Development - genetics</topic><topic>Embryos</topic><topic>Fertilization</topic><topic>G2 phase</topic><topic>Implantation</topic><topic>Machinery and equipment</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Mitosis</topic><topic>Mitosis - genetics</topic><topic>Mutation</topic><topic>Nuclear Proteins - metabolism</topic><topic>Nuclear transport</topic><topic>Nuclei (cytology)</topic><topic>Phosphorylation</topic><topic>Protein-Tyrosine Kinases - metabolism</topic><topic>Proteins</topic><topic>Redundancy</topic><topic>Regulators</topic><topic>Transcription Factors - metabolism</topic><topic>Transplants &amp; implants</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Strauss, Bernhard</creatorcontrib><creatorcontrib>Harrison, Andrew</creatorcontrib><creatorcontrib>Coelho, Paula Almeida</creatorcontrib><creatorcontrib>Yata, Keiko</creatorcontrib><creatorcontrib>Zernicka-Goetz, Magdalena</creatorcontrib><creatorcontrib>Pines, Jonathon</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids 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>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>The Journal of cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Strauss, Bernhard</au><au>Harrison, Andrew</au><au>Coelho, Paula Almeida</au><au>Yata, Keiko</au><au>Zernicka-Goetz, Magdalena</au><au>Pines, Jonathon</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cyclin B1 is essential for mitosis in mouse embryos, and its nuclear export sets the time for mitosis</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2018-01-02</date><risdate>2018</risdate><volume>217</volume><issue>1</issue><spage>179</spage><epage>193</epage><pages>179-193</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><abstract>There is remarkable redundancy between the Cyclin-Cdk complexes that comprise the cell cycle machinery. None of the mammalian A-, D-, or E-type cyclins are required in development until implantation, and only Cdk1 is essential for early cell divisions. Cyclin B1 is essential for development, but whether it is required for cell division is contentious. Here, we used a novel imaging approach to analyze Cyclin B1-null embryos from fertilization onward. We show that Cyclin B1 embryos arrest in G2 phase after just two divisions. This is the earliest arrest of any Cyclin known and places Cyclin B1 with cdk1 as the essential regulators of the cell cycle. We reintroduced mutant proteins into this genetically null background to determine why Cyclin B1 is constantly exported from the nucleus. We found that Cyclin B1 must be exported from the nucleus for the cell to prevent premature entry to mitosis, and retaining Cyclin B1-Cdk1 at the plasma membrane precludes entry to mitosis.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>29074707</pmid><doi>10.1083/jcb.201612147</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-5227-6004</orcidid><orcidid>https://orcid.org/0000-0001-7648-4898</orcidid><orcidid>https://orcid.org/0000-0003-0614-7575</orcidid><orcidid>https://orcid.org/0000-0002-3778-8415</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0021-9525
ispartof The Journal of cell biology, 2018-01, Vol.217 (1), p.179-193
issn 0021-9525
1540-8140
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5748970
source MEDLINE; Alma/SFX Local Collection; EZB Electronic Journals Library
subjects Active Transport, Cell Nucleus - physiology
Animals
CDC2 Protein Kinase - genetics
cdc25 Phosphatases - metabolism
Cell cycle
Cell Cycle Proteins - metabolism
Cell division
Cyclin B1
Cyclin B1 - genetics
Cyclins
DNA-Binding Proteins - metabolism
Embryonic Development - genetics
Embryos
Fertilization
G2 phase
Implantation
Machinery and equipment
Mice
Mice, Knockout
Mitosis
Mitosis - genetics
Mutation
Nuclear Proteins - metabolism
Nuclear transport
Nuclei (cytology)
Phosphorylation
Protein-Tyrosine Kinases - metabolism
Proteins
Redundancy
Regulators
Transcription Factors - metabolism
Transplants & implants
title Cyclin B1 is essential for mitosis in mouse embryos, and its nuclear export sets the time for mitosis
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-10T20%3A02%3A03IST&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=Cyclin%20B1%20is%20essential%20for%20mitosis%20in%20mouse%20embryos,%20and%20its%20nuclear%20export%20sets%20the%20time%20for%20mitosis&rft.jtitle=The%20Journal%20of%20cell%20biology&rft.au=Strauss,%20Bernhard&rft.date=2018-01-02&rft.volume=217&rft.issue=1&rft.spage=179&rft.epage=193&rft.pages=179-193&rft.issn=0021-9525&rft.eissn=1540-8140&rft_id=info:doi/10.1083/jcb.201612147&rft_dat=%3Cproquest_pubme%3E1990815796%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=1990815796&rft_id=info:pmid/29074707&rfr_iscdi=true