Clathrin promotes centrosome integrity in early mitosis through stabilization of centrosomal ch-TOG
Clathrin depletion by ribonucleic acid interference (RNAi) impairs mitotic spindle stability and cytokinesis. Depletion of several clathrin-associated proteins affects centrosome integrity, suggesting a further cell cycle function for clathrin. In this paper, we report that RNAi depletion of CHC17 (...
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Veröffentlicht in: | The Journal of cell biology 2012-08, Vol.198 (4), p.591-605 |
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creator | Foraker, Amy B Camus, Stéphane M Evans, Timothy M Majeed, Sophia R Chen, Chih-Ying Taner, Sabrina B Corrêa, Jr, Ivan R Doxsey, Stephen J Brodsky, Frances M |
description | Clathrin depletion by ribonucleic acid interference (RNAi) impairs mitotic spindle stability and cytokinesis. Depletion of several clathrin-associated proteins affects centrosome integrity, suggesting a further cell cycle function for clathrin. In this paper, we report that RNAi depletion of CHC17 (clathrin heavy chain 17) clathrin, but not the CHC22 clathrin isoform, induced centrosome amplification and multipolar spindles. To stage clathrin function within the cell cycle, a cell line expressing SNAP-tagged clathrin light chains was generated. Acute clathrin inactivation by chemical dimerization of the SNAP-tag during S phase caused reduction of both clathrin and ch-TOG (colonic, hepatic tumor overexpressed gene) at metaphase centrosomes, which became fragmented. This was phenocopied by treatment with Aurora A kinase inhibitor, suggesting a centrosomal role for the Aurora A-dependent complex of clathrin, ch-TOG, and TACC3 (transforming acidic coiled-coil protein 3). Clathrin inactivation in S phase also reduced total cellular levels of ch-TOG by metaphase. Live-cell imaging showed dynamic clathrin recruitment during centrosome maturation. Therefore, we propose that clathrin promotes centrosome maturation by stabilizing the microtubule-binding protein ch-TOG, defining a novel role for the clathrin-ch-TOG-TACC3 complex. |
doi_str_mv | 10.1083/jcb.201205116 |
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Depletion of several clathrin-associated proteins affects centrosome integrity, suggesting a further cell cycle function for clathrin. In this paper, we report that RNAi depletion of CHC17 (clathrin heavy chain 17) clathrin, but not the CHC22 clathrin isoform, induced centrosome amplification and multipolar spindles. To stage clathrin function within the cell cycle, a cell line expressing SNAP-tagged clathrin light chains was generated. Acute clathrin inactivation by chemical dimerization of the SNAP-tag during S phase caused reduction of both clathrin and ch-TOG (colonic, hepatic tumor overexpressed gene) at metaphase centrosomes, which became fragmented. This was phenocopied by treatment with Aurora A kinase inhibitor, suggesting a centrosomal role for the Aurora A-dependent complex of clathrin, ch-TOG, and TACC3 (transforming acidic coiled-coil protein 3). Clathrin inactivation in S phase also reduced total cellular levels of ch-TOG by metaphase. Live-cell imaging showed dynamic clathrin recruitment during centrosome maturation. Therefore, we propose that clathrin promotes centrosome maturation by stabilizing the microtubule-binding protein ch-TOG, defining a novel role for the clathrin-ch-TOG-TACC3 complex.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.201205116</identifier><identifier>PMID: 22891263</identifier><identifier>CODEN: JCLBA3</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Cell cycle ; Cell division ; Centrosome - metabolism ; Clathrin - genetics ; Clathrin - physiology ; Clathrin Heavy Chains - antagonists & inhibitors ; Clathrin Heavy Chains - genetics ; Clathrin Heavy Chains - metabolism ; Cytokines ; Gene expression ; HeLa Cells ; Humans ; Microtubule-Associated Proteins - metabolism ; Mitosis - physiology ; Proteins ; Ribonucleic acid ; RNA ; RNA Interference ; RNA Stability - genetics ; RNA, Small Interfering - genetics</subject><ispartof>The Journal of cell biology, 2012-08, Vol.198 (4), p.591-605</ispartof><rights>Copyright Rockefeller University Press Aug 20, 2012</rights><rights>2012 Foraker et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c415t-ae72398b050a16e5c5c85b0097473292c9588b4c6ae8e93b678b4ffe8d64d5523</citedby><cites>FETCH-LOGICAL-c415t-ae72398b050a16e5c5c85b0097473292c9588b4c6ae8e93b678b4ffe8d64d5523</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22891263$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Foraker, Amy B</creatorcontrib><creatorcontrib>Camus, Stéphane M</creatorcontrib><creatorcontrib>Evans, Timothy M</creatorcontrib><creatorcontrib>Majeed, Sophia R</creatorcontrib><creatorcontrib>Chen, Chih-Ying</creatorcontrib><creatorcontrib>Taner, Sabrina B</creatorcontrib><creatorcontrib>Corrêa, Jr, Ivan R</creatorcontrib><creatorcontrib>Doxsey, Stephen J</creatorcontrib><creatorcontrib>Brodsky, Frances M</creatorcontrib><title>Clathrin promotes centrosome integrity in early mitosis through stabilization of centrosomal ch-TOG</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Clathrin depletion by ribonucleic acid interference (RNAi) impairs mitotic spindle stability and cytokinesis. Depletion of several clathrin-associated proteins affects centrosome integrity, suggesting a further cell cycle function for clathrin. In this paper, we report that RNAi depletion of CHC17 (clathrin heavy chain 17) clathrin, but not the CHC22 clathrin isoform, induced centrosome amplification and multipolar spindles. To stage clathrin function within the cell cycle, a cell line expressing SNAP-tagged clathrin light chains was generated. Acute clathrin inactivation by chemical dimerization of the SNAP-tag during S phase caused reduction of both clathrin and ch-TOG (colonic, hepatic tumor overexpressed gene) at metaphase centrosomes, which became fragmented. This was phenocopied by treatment with Aurora A kinase inhibitor, suggesting a centrosomal role for the Aurora A-dependent complex of clathrin, ch-TOG, and TACC3 (transforming acidic coiled-coil protein 3). Clathrin inactivation in S phase also reduced total cellular levels of ch-TOG by metaphase. Live-cell imaging showed dynamic clathrin recruitment during centrosome maturation. Therefore, we propose that clathrin promotes centrosome maturation by stabilizing the microtubule-binding protein ch-TOG, defining a novel role for the clathrin-ch-TOG-TACC3 complex.</description><subject>Cell cycle</subject><subject>Cell division</subject><subject>Centrosome - metabolism</subject><subject>Clathrin - genetics</subject><subject>Clathrin - physiology</subject><subject>Clathrin Heavy Chains - antagonists & inhibitors</subject><subject>Clathrin Heavy Chains - genetics</subject><subject>Clathrin Heavy Chains - metabolism</subject><subject>Cytokines</subject><subject>Gene expression</subject><subject>HeLa Cells</subject><subject>Humans</subject><subject>Microtubule-Associated Proteins - metabolism</subject><subject>Mitosis - physiology</subject><subject>Proteins</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA Interference</subject><subject>RNA Stability - genetics</subject><subject>RNA, Small Interfering - genetics</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1rGzEQxUVpaJyPY69F0Esum4y-dqVLIZjGLQRycc5CK2ttmd2VK2kDzl9fOUndNqfRoN88Zt5D6DOBawKS3Wxte02BUBCE1B_QjAgOlSQcPqIZACWVElScorOUtgDAG84-oVNKpSK0ZjNk573Jm-hHvIthCNklbN2YY0hhcNiP2a2jz_vyws7Efo8Hn0PyCZehMK03OGXT-t4_m-zDiEP3d9z02G6q5cPiAp10pk_u8q2eo8e778v5j-r-YfFzfntfWU5EroxrKFOyBQGG1E5YYaVoAVTDG0YVtUpI2XJbGyedYm3dlK7rnFzVfCUEZefo26vubmoHt3pZxPR6F_1g4l4H4_X_P6Pf6HV40kwUvzgUgas3gRh-TS5lPfhkXd-b0YUpaQKM10IqaAr69R26DVMcy3kHqliuGmCFql4pWxxJ0XXHZQjoQ3y6xKeP8RX-y78XHOk_ebHfYaOXYw</recordid><startdate>20120820</startdate><enddate>20120820</enddate><creator>Foraker, Amy B</creator><creator>Camus, Stéphane M</creator><creator>Evans, Timothy M</creator><creator>Majeed, Sophia R</creator><creator>Chen, Chih-Ying</creator><creator>Taner, Sabrina B</creator><creator>Corrêa, Jr, Ivan R</creator><creator>Doxsey, Stephen J</creator><creator>Brodsky, Frances M</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></search><sort><creationdate>20120820</creationdate><title>Clathrin promotes centrosome integrity in early mitosis through stabilization of centrosomal ch-TOG</title><author>Foraker, Amy B ; Camus, Stéphane M ; Evans, Timothy M ; Majeed, Sophia R ; Chen, Chih-Ying ; Taner, Sabrina B ; Corrêa, Jr, Ivan R ; Doxsey, Stephen J ; Brodsky, Frances M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c415t-ae72398b050a16e5c5c85b0097473292c9588b4c6ae8e93b678b4ffe8d64d5523</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Cell cycle</topic><topic>Cell division</topic><topic>Centrosome - metabolism</topic><topic>Clathrin - genetics</topic><topic>Clathrin - physiology</topic><topic>Clathrin Heavy Chains - antagonists & inhibitors</topic><topic>Clathrin Heavy Chains - genetics</topic><topic>Clathrin Heavy Chains - metabolism</topic><topic>Cytokines</topic><topic>Gene expression</topic><topic>HeLa Cells</topic><topic>Humans</topic><topic>Microtubule-Associated Proteins - metabolism</topic><topic>Mitosis - physiology</topic><topic>Proteins</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA Interference</topic><topic>RNA Stability - genetics</topic><topic>RNA, Small Interfering - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Foraker, Amy B</creatorcontrib><creatorcontrib>Camus, Stéphane M</creatorcontrib><creatorcontrib>Evans, Timothy M</creatorcontrib><creatorcontrib>Majeed, Sophia R</creatorcontrib><creatorcontrib>Chen, Chih-Ying</creatorcontrib><creatorcontrib>Taner, Sabrina B</creatorcontrib><creatorcontrib>Corrêa, Jr, Ivan R</creatorcontrib><creatorcontrib>Doxsey, Stephen J</creatorcontrib><creatorcontrib>Brodsky, Frances M</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>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>Foraker, Amy B</au><au>Camus, Stéphane M</au><au>Evans, Timothy M</au><au>Majeed, Sophia R</au><au>Chen, Chih-Ying</au><au>Taner, Sabrina B</au><au>Corrêa, Jr, Ivan R</au><au>Doxsey, Stephen J</au><au>Brodsky, Frances M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Clathrin promotes centrosome integrity in early mitosis through stabilization of centrosomal ch-TOG</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2012-08-20</date><risdate>2012</risdate><volume>198</volume><issue>4</issue><spage>591</spage><epage>605</epage><pages>591-605</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><coden>JCLBA3</coden><abstract>Clathrin depletion by ribonucleic acid interference (RNAi) impairs mitotic spindle stability and cytokinesis. Depletion of several clathrin-associated proteins affects centrosome integrity, suggesting a further cell cycle function for clathrin. In this paper, we report that RNAi depletion of CHC17 (clathrin heavy chain 17) clathrin, but not the CHC22 clathrin isoform, induced centrosome amplification and multipolar spindles. To stage clathrin function within the cell cycle, a cell line expressing SNAP-tagged clathrin light chains was generated. Acute clathrin inactivation by chemical dimerization of the SNAP-tag during S phase caused reduction of both clathrin and ch-TOG (colonic, hepatic tumor overexpressed gene) at metaphase centrosomes, which became fragmented. This was phenocopied by treatment with Aurora A kinase inhibitor, suggesting a centrosomal role for the Aurora A-dependent complex of clathrin, ch-TOG, and TACC3 (transforming acidic coiled-coil protein 3). Clathrin inactivation in S phase also reduced total cellular levels of ch-TOG by metaphase. Live-cell imaging showed dynamic clathrin recruitment during centrosome maturation. Therefore, we propose that clathrin promotes centrosome maturation by stabilizing the microtubule-binding protein ch-TOG, defining a novel role for the clathrin-ch-TOG-TACC3 complex.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>22891263</pmid><doi>10.1083/jcb.201205116</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Cell cycle Cell division Centrosome - metabolism Clathrin - genetics Clathrin - physiology Clathrin Heavy Chains - antagonists & inhibitors Clathrin Heavy Chains - genetics Clathrin Heavy Chains - metabolism Cytokines Gene expression HeLa Cells Humans Microtubule-Associated Proteins - metabolism Mitosis - physiology Proteins Ribonucleic acid RNA RNA Interference RNA Stability - genetics RNA, Small Interfering - genetics |
title | Clathrin promotes centrosome integrity in early mitosis through stabilization of centrosomal ch-TOG |
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