Functional midbody assembly in the absence of a central spindle
Contractile ring constriction during cytokinesis is thought to compact central spindle microtubules to form the midbody, an antiparallel microtubule bundle at the intercellular bridge. In Caenorhabditis elegans, central spindle microtubule assembly requires targeting of the CLASP family protein CLS-...
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Veröffentlicht in: | The Journal of cell biology 2022-03, Vol.221 (3), p.1 |
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creator | Hirsch, Sophia M Edwards, Frances Shirasu-Hiza, Mimi Dumont, Julien Canman, Julie C |
description | Contractile ring constriction during cytokinesis is thought to compact central spindle microtubules to form the midbody, an antiparallel microtubule bundle at the intercellular bridge. In Caenorhabditis elegans, central spindle microtubule assembly requires targeting of the CLASP family protein CLS-2 to the kinetochores in metaphase and spindle midzone in anaphase. CLS-2 targeting is mediated by the CENP-F-like HCP-1/2, but their roles in cytokinesis and midbody assembly are not known. We found that although HCP-1 and HCP-2 mostly function cooperatively, HCP-1 plays a more primary role in promoting CLS-2-dependent central spindle microtubule assembly. HCP-1/2 codisrupted embryos did not form central spindles but completed cytokinesis and formed functional midbodies capable of supporting abscission. These central spindle-independent midbodies appeared to form via contractile ring constriction-driven bundling of astral microtubules at the furrow tip. This work suggests that, in the absence of a central spindle, astral microtubules can support midbody assembly and that midbody assembly is more predictive of successful cytokinesis than central spindle assembly. |
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In Caenorhabditis elegans, central spindle microtubule assembly requires targeting of the CLASP family protein CLS-2 to the kinetochores in metaphase and spindle midzone in anaphase. CLS-2 targeting is mediated by the CENP-F-like HCP-1/2, but their roles in cytokinesis and midbody assembly are not known. We found that although HCP-1 and HCP-2 mostly function cooperatively, HCP-1 plays a more primary role in promoting CLS-2-dependent central spindle microtubule assembly. HCP-1/2 codisrupted embryos did not form central spindles but completed cytokinesis and formed functional midbodies capable of supporting abscission. These central spindle-independent midbodies appeared to form via contractile ring constriction-driven bundling of astral microtubules at the furrow tip. This work suggests that, in the absence of a central spindle, astral microtubules can support midbody assembly and that midbody assembly is more predictive of successful cytokinesis than central spindle assembly.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.202011085</identifier><identifier>PMID: 34994802</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Abscission ; Anaphase ; Animals ; Assembly ; Caenorhabditis elegans - embryology ; Caenorhabditis elegans Proteins - metabolism ; Cell Cycle and Division ; Constrictions ; Contractility ; Cytokinesis ; Cytoskeleton ; Embryo, Nonmammalian - metabolism ; Embryos ; Genetics ; Green Fluorescent Proteins - metabolism ; Kinetochores ; Life Sciences ; Metaphase ; Microtubules ; Microtubules - metabolism ; Spindle Apparatus - metabolism ; Spindles</subject><ispartof>The Journal of cell biology, 2022-03, Vol.221 (3), p.1</ispartof><rights>2021 Hirsch et al.</rights><rights>Copyright Rockefeller University Press Mar 2022</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2021 Hirsch et al. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c449t-a11dee127ae39233f26c7b1cbee91a1a940b7a866e9daac7cde06a812c0c065a3</citedby><cites>FETCH-LOGICAL-c449t-a11dee127ae39233f26c7b1cbee91a1a940b7a866e9daac7cde06a812c0c065a3</cites><orcidid>0000-0001-5312-9770 ; 0000-0002-2730-1765 ; 0000-0001-8135-2072 ; 0000-0003-0888-6689 ; 0000-0002-4351-7136</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34994802$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://cnrs.hal.science/hal-03864927$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Hirsch, Sophia M</creatorcontrib><creatorcontrib>Edwards, Frances</creatorcontrib><creatorcontrib>Shirasu-Hiza, Mimi</creatorcontrib><creatorcontrib>Dumont, Julien</creatorcontrib><creatorcontrib>Canman, Julie C</creatorcontrib><title>Functional midbody assembly in the absence of a central spindle</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Contractile ring constriction during cytokinesis is thought to compact central spindle microtubules to form the midbody, an antiparallel microtubule bundle at the intercellular bridge. In Caenorhabditis elegans, central spindle microtubule assembly requires targeting of the CLASP family protein CLS-2 to the kinetochores in metaphase and spindle midzone in anaphase. CLS-2 targeting is mediated by the CENP-F-like HCP-1/2, but their roles in cytokinesis and midbody assembly are not known. We found that although HCP-1 and HCP-2 mostly function cooperatively, HCP-1 plays a more primary role in promoting CLS-2-dependent central spindle microtubule assembly. HCP-1/2 codisrupted embryos did not form central spindles but completed cytokinesis and formed functional midbodies capable of supporting abscission. These central spindle-independent midbodies appeared to form via contractile ring constriction-driven bundling of astral microtubules at the furrow tip. This work suggests that, in the absence of a central spindle, astral microtubules can support midbody assembly and that midbody assembly is more predictive of successful cytokinesis than central spindle assembly.</description><subject>Abscission</subject><subject>Anaphase</subject><subject>Animals</subject><subject>Assembly</subject><subject>Caenorhabditis elegans - embryology</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Cell Cycle and Division</subject><subject>Constrictions</subject><subject>Contractility</subject><subject>Cytokinesis</subject><subject>Cytoskeleton</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryos</subject><subject>Genetics</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Kinetochores</subject><subject>Life Sciences</subject><subject>Metaphase</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Spindle Apparatus - metabolism</subject><subject>Spindles</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU1P4zAQhq0Vq6Wwe-SKInGBQ9gZ2_nwBYQQHytV2gucrYkzpamSuMQJUv89iVoq4GTZfvzMeF4hThAuEXL1d-WKSwkScNwlP8QMEw1xjhoOxAxAYmwSmRyKoxBWAKAzrX6JQ6WN0TnImbi-H1rXV76lOmqqsvDlJqIQuCnqTVS1Ub_kiIrArePILyKKHLd9N8JhXbVlzb_FzwXVgf_s1mPxfH_3dPsYz_8__Lu9mcdOa9PHhFgyo8yIlZFKLWTqsgJdwWyQkIyGIqM8TdmURC5zJUNKOUoHDtKE1LG42nrXQ9FwuevCrruqoW5jPVX2601bLe2Lf7N5lmCWpKPgYitYfnv2eDO30xmoPNVGZm84sue7Yp1_HTj0tqmC47qmlv0QrEwxlypROGnPvqErP3TjNCdKacBx0JMw3lKu8yF0vNh3gGCnGO0Yo93HOPKnn3-7pz9yU-9aV5e6</recordid><startdate>20220307</startdate><enddate>20220307</enddate><creator>Hirsch, Sophia M</creator><creator>Edwards, Frances</creator><creator>Shirasu-Hiza, Mimi</creator><creator>Dumont, Julien</creator><creator>Canman, Julie C</creator><general>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>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5312-9770</orcidid><orcidid>https://orcid.org/0000-0002-2730-1765</orcidid><orcidid>https://orcid.org/0000-0001-8135-2072</orcidid><orcidid>https://orcid.org/0000-0003-0888-6689</orcidid><orcidid>https://orcid.org/0000-0002-4351-7136</orcidid></search><sort><creationdate>20220307</creationdate><title>Functional midbody assembly in the absence of a central spindle</title><author>Hirsch, Sophia M ; Edwards, Frances ; Shirasu-Hiza, Mimi ; Dumont, Julien ; Canman, Julie C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c449t-a11dee127ae39233f26c7b1cbee91a1a940b7a866e9daac7cde06a812c0c065a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Abscission</topic><topic>Anaphase</topic><topic>Animals</topic><topic>Assembly</topic><topic>Caenorhabditis elegans - embryology</topic><topic>Caenorhabditis elegans Proteins - metabolism</topic><topic>Cell Cycle and Division</topic><topic>Constrictions</topic><topic>Contractility</topic><topic>Cytokinesis</topic><topic>Cytoskeleton</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Embryos</topic><topic>Genetics</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Kinetochores</topic><topic>Life Sciences</topic><topic>Metaphase</topic><topic>Microtubules</topic><topic>Microtubules - metabolism</topic><topic>Spindle Apparatus - metabolism</topic><topic>Spindles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hirsch, Sophia M</creatorcontrib><creatorcontrib>Edwards, Frances</creatorcontrib><creatorcontrib>Shirasu-Hiza, Mimi</creatorcontrib><creatorcontrib>Dumont, Julien</creatorcontrib><creatorcontrib>Canman, Julie C</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 & 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>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</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>Hirsch, Sophia M</au><au>Edwards, Frances</au><au>Shirasu-Hiza, Mimi</au><au>Dumont, Julien</au><au>Canman, Julie C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional midbody assembly in the absence of a central spindle</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2022-03-07</date><risdate>2022</risdate><volume>221</volume><issue>3</issue><spage>1</spage><pages>1-</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><abstract>Contractile ring constriction during cytokinesis is thought to compact central spindle microtubules to form the midbody, an antiparallel microtubule bundle at the intercellular bridge. In Caenorhabditis elegans, central spindle microtubule assembly requires targeting of the CLASP family protein CLS-2 to the kinetochores in metaphase and spindle midzone in anaphase. CLS-2 targeting is mediated by the CENP-F-like HCP-1/2, but their roles in cytokinesis and midbody assembly are not known. We found that although HCP-1 and HCP-2 mostly function cooperatively, HCP-1 plays a more primary role in promoting CLS-2-dependent central spindle microtubule assembly. HCP-1/2 codisrupted embryos did not form central spindles but completed cytokinesis and formed functional midbodies capable of supporting abscission. These central spindle-independent midbodies appeared to form via contractile ring constriction-driven bundling of astral microtubules at the furrow tip. 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subjects | Abscission Anaphase Animals Assembly Caenorhabditis elegans - embryology Caenorhabditis elegans Proteins - metabolism Cell Cycle and Division Constrictions Contractility Cytokinesis Cytoskeleton Embryo, Nonmammalian - metabolism Embryos Genetics Green Fluorescent Proteins - metabolism Kinetochores Life Sciences Metaphase Microtubules Microtubules - metabolism Spindle Apparatus - metabolism Spindles |
title | Functional midbody assembly in the absence of a central spindle |
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