Microtubule Release from the Centrosome in Migrating Cells
In migrating cells, force production relies essentially on a polarized actomyosin system, whereas the spatial regulation of actomyosin contraction and substrate contact turnover involves a complex cooperation between the microtubule (MT) and the actin filament networks. Targeting and capture of MT p...
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Veröffentlicht in: | The Journal of cell biology 2002-12, Vol.159 (5), p.731-737 |
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creator | Abal, Miguel Piel, Matthieu Bouckson-Castaing, Veronique Mogensen, Mette Sibarita, Jean-Baptiste Bornens, Michel |
description | In migrating cells, force production relies essentially on a polarized actomyosin system, whereas the spatial regulation of actomyosin contraction and substrate contact turnover involves a complex cooperation between the microtubule (MT) and the actin filament networks. Targeting and capture of MT plus ends at the cell periphery has been described, but whether or not the minus ends of these MTs are anchored at the centrosome is not known. Here, we show that release of short MTs from the centrosome is frequent in migrating cells and that their transport toward the cell periphery is blocked when dynein activity is impaired. We further show that MT release, but not MT nucleation or polymerization dynamics, is abolished by overexpression of the centrosomal MT-anchoring protein ninein. In addition, a dramatic inhibition of cell migration was observed; but, contrary to cells treated by drugs inhibiting MT dynamics, polarized membrane ruffling activity was not affected in ninein overexpressing cells. We thus propose that the balance between MT minus-end capture and release from the centrosome is critical for efficient cell migration. |
doi_str_mv | 10.1083/jcb.200207076 |
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Targeting and capture of MT plus ends at the cell periphery has been described, but whether or not the minus ends of these MTs are anchored at the centrosome is not known. Here, we show that release of short MTs from the centrosome is frequent in migrating cells and that their transport toward the cell periphery is blocked when dynein activity is impaired. We further show that MT release, but not MT nucleation or polymerization dynamics, is abolished by overexpression of the centrosomal MT-anchoring protein ninein. In addition, a dramatic inhibition of cell migration was observed; but, contrary to cells treated by drugs inhibiting MT dynamics, polarized membrane ruffling activity was not affected in ninein overexpressing cells. We thus propose that the balance between MT minus-end capture and release from the centrosome is critical for efficient cell migration.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.200207076</identifier><identifier>PMID: 12473683</identifier><identifier>CODEN: JCLBA3</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animal cells ; Animals ; Cell Line ; Cell Movement ; Cells ; Cellular biology ; Centrosome - metabolism ; Centrosome - physiology ; Centrosomes ; Cytoskeletal Proteins ; Dynactin Complex ; Dyneins - antagonists & inhibitors ; Dyneins - metabolism ; Epithelial cells ; Fibroblasts - cytology ; Fibroblasts - physiology ; Green Fluorescent Proteins ; GTP-Binding Proteins - drug effects ; GTP-Binding Proteins - metabolism ; GTP-Binding Proteins - physiology ; HeLa Cells ; Humans ; Indicators and Reagents ; Kinetics ; Locomotion ; Luminescent Proteins - metabolism ; Mice ; Microfilaments ; Microscopy, Video - methods ; Microtubule-Associated Proteins - antagonists & inhibitors ; Microtubule-Associated Proteins - metabolism ; Microtubules ; Microtubules - metabolism ; Microtubules - physiology ; Nocodazole - pharmacology ; Nuclear Proteins ; Polymerization ; Regrowth ; Skin - cytology ; Time Factors ; Trajectories ; Tumor Cells, Cultured</subject><ispartof>The Journal of cell biology, 2002-12, Vol.159 (5), p.731-737</ispartof><rights>Copyright 2002 The Rockefeller University Press</rights><rights>Copyright Rockefeller University Press Dec 9, 2002</rights><rights>Copyright © 2002, The Rockefeller University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c497t-683d7866214b917c81474b2152ddd1913e05996d95433eb6009f57a684dcdbdf3</citedby><cites>FETCH-LOGICAL-c497t-683d7866214b917c81474b2152ddd1913e05996d95433eb6009f57a684dcdbdf3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12473683$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Abal, Miguel</creatorcontrib><creatorcontrib>Piel, Matthieu</creatorcontrib><creatorcontrib>Bouckson-Castaing, Veronique</creatorcontrib><creatorcontrib>Mogensen, Mette</creatorcontrib><creatorcontrib>Sibarita, Jean-Baptiste</creatorcontrib><creatorcontrib>Bornens, Michel</creatorcontrib><title>Microtubule Release from the Centrosome in Migrating Cells</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>In migrating cells, force production relies essentially on a polarized actomyosin system, whereas the spatial regulation of actomyosin contraction and substrate contact turnover involves a complex cooperation between the microtubule (MT) and the actin filament networks. 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We thus propose that the balance between MT minus-end capture and release from the centrosome is critical for efficient cell migration.</description><subject>Animal cells</subject><subject>Animals</subject><subject>Cell Line</subject><subject>Cell Movement</subject><subject>Cells</subject><subject>Cellular biology</subject><subject>Centrosome - metabolism</subject><subject>Centrosome - physiology</subject><subject>Centrosomes</subject><subject>Cytoskeletal Proteins</subject><subject>Dynactin Complex</subject><subject>Dyneins - antagonists & inhibitors</subject><subject>Dyneins - metabolism</subject><subject>Epithelial cells</subject><subject>Fibroblasts - cytology</subject><subject>Fibroblasts - physiology</subject><subject>Green Fluorescent Proteins</subject><subject>GTP-Binding Proteins - drug effects</subject><subject>GTP-Binding Proteins - metabolism</subject><subject>GTP-Binding Proteins - physiology</subject><subject>HeLa Cells</subject><subject>Humans</subject><subject>Indicators and Reagents</subject><subject>Kinetics</subject><subject>Locomotion</subject><subject>Luminescent Proteins - metabolism</subject><subject>Mice</subject><subject>Microfilaments</subject><subject>Microscopy, Video - methods</subject><subject>Microtubule-Associated Proteins - antagonists & inhibitors</subject><subject>Microtubule-Associated Proteins - metabolism</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Microtubules - physiology</subject><subject>Nocodazole - pharmacology</subject><subject>Nuclear Proteins</subject><subject>Polymerization</subject><subject>Regrowth</subject><subject>Skin - cytology</subject><subject>Time Factors</subject><subject>Trajectories</subject><subject>Tumor Cells, Cultured</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2002</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1Lw0AQxRdRbK0evYkED95SZz-SzXoQpPgFLYLoeUmymzYhydbdRPC_d0NLq54GZn68eTMPoXMMUwwJvanybEoACHDg8QEa44hBmGAGh2js2zgUEYlG6MS5CgAYZ_QYjTBhnMYJHaPbRZlb0_VZX-vgTdc6dToorGmCbqWDmW47a5xpdFC2waJc2rQr26Xv17U7RUdFWjt9tq0T9PH48D57DuevTy-z-3mYM8G70K9RPIljglkmMM-9N84ygiOilMICUw2RELESEaNUZzGAKCKexglTucpUQSfobqO77rNGq3zwlNZybcsmtd_SpKX8O2nLlVyaL0kwp1QkXuB6K2DNZ69dJ5vS5f6EtNWmd5ITHjMCA3j1D6xMb1t_3KAFCQgAD4UbyP_NOauLnRMMcohE-kjkLhLPX_62v6e3GXjgYgNUrjN2P_cfoyyiP9QXj0o</recordid><startdate>20021209</startdate><enddate>20021209</enddate><creator>Abal, Miguel</creator><creator>Piel, Matthieu</creator><creator>Bouckson-Castaing, Veronique</creator><creator>Mogensen, Mette</creator><creator>Sibarita, Jean-Baptiste</creator><creator>Bornens, Michel</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>20021209</creationdate><title>Microtubule Release from the Centrosome in Migrating Cells</title><author>Abal, Miguel ; Piel, Matthieu ; Bouckson-Castaing, Veronique ; Mogensen, Mette ; Sibarita, Jean-Baptiste ; Bornens, Michel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c497t-683d7866214b917c81474b2152ddd1913e05996d95433eb6009f57a684dcdbdf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2002</creationdate><topic>Animal cells</topic><topic>Animals</topic><topic>Cell Line</topic><topic>Cell Movement</topic><topic>Cells</topic><topic>Cellular biology</topic><topic>Centrosome - metabolism</topic><topic>Centrosome - physiology</topic><topic>Centrosomes</topic><topic>Cytoskeletal Proteins</topic><topic>Dynactin Complex</topic><topic>Dyneins - antagonists & inhibitors</topic><topic>Dyneins - metabolism</topic><topic>Epithelial cells</topic><topic>Fibroblasts - cytology</topic><topic>Fibroblasts - physiology</topic><topic>Green Fluorescent Proteins</topic><topic>GTP-Binding Proteins - drug effects</topic><topic>GTP-Binding Proteins - metabolism</topic><topic>GTP-Binding Proteins - physiology</topic><topic>HeLa Cells</topic><topic>Humans</topic><topic>Indicators and Reagents</topic><topic>Kinetics</topic><topic>Locomotion</topic><topic>Luminescent Proteins - metabolism</topic><topic>Mice</topic><topic>Microfilaments</topic><topic>Microscopy, Video - methods</topic><topic>Microtubule-Associated Proteins - antagonists & inhibitors</topic><topic>Microtubule-Associated Proteins - metabolism</topic><topic>Microtubules</topic><topic>Microtubules - metabolism</topic><topic>Microtubules - physiology</topic><topic>Nocodazole - pharmacology</topic><topic>Nuclear Proteins</topic><topic>Polymerization</topic><topic>Regrowth</topic><topic>Skin - cytology</topic><topic>Time Factors</topic><topic>Trajectories</topic><topic>Tumor Cells, Cultured</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Abal, Miguel</creatorcontrib><creatorcontrib>Piel, Matthieu</creatorcontrib><creatorcontrib>Bouckson-Castaing, Veronique</creatorcontrib><creatorcontrib>Mogensen, Mette</creatorcontrib><creatorcontrib>Sibarita, Jean-Baptiste</creatorcontrib><creatorcontrib>Bornens, Michel</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>Abal, Miguel</au><au>Piel, Matthieu</au><au>Bouckson-Castaing, Veronique</au><au>Mogensen, Mette</au><au>Sibarita, Jean-Baptiste</au><au>Bornens, Michel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Microtubule Release from the Centrosome in Migrating Cells</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2002-12-09</date><risdate>2002</risdate><volume>159</volume><issue>5</issue><spage>731</spage><epage>737</epage><pages>731-737</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><coden>JCLBA3</coden><abstract>In migrating cells, force production relies essentially on a polarized actomyosin system, whereas the spatial regulation of actomyosin contraction and substrate contact turnover involves a complex cooperation between the microtubule (MT) and the actin filament networks. Targeting and capture of MT plus ends at the cell periphery has been described, but whether or not the minus ends of these MTs are anchored at the centrosome is not known. Here, we show that release of short MTs from the centrosome is frequent in migrating cells and that their transport toward the cell periphery is blocked when dynein activity is impaired. We further show that MT release, but not MT nucleation or polymerization dynamics, is abolished by overexpression of the centrosomal MT-anchoring protein ninein. In addition, a dramatic inhibition of cell migration was observed; but, contrary to cells treated by drugs inhibiting MT dynamics, polarized membrane ruffling activity was not affected in ninein overexpressing cells. We thus propose that the balance between MT minus-end capture and release from the centrosome is critical for efficient cell migration.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>12473683</pmid><doi>10.1083/jcb.200207076</doi><tpages>7</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animal cells Animals Cell Line Cell Movement Cells Cellular biology Centrosome - metabolism Centrosome - physiology Centrosomes Cytoskeletal Proteins Dynactin Complex Dyneins - antagonists & inhibitors Dyneins - metabolism Epithelial cells Fibroblasts - cytology Fibroblasts - physiology Green Fluorescent Proteins GTP-Binding Proteins - drug effects GTP-Binding Proteins - metabolism GTP-Binding Proteins - physiology HeLa Cells Humans Indicators and Reagents Kinetics Locomotion Luminescent Proteins - metabolism Mice Microfilaments Microscopy, Video - methods Microtubule-Associated Proteins - antagonists & inhibitors Microtubule-Associated Proteins - metabolism Microtubules Microtubules - metabolism Microtubules - physiology Nocodazole - pharmacology Nuclear Proteins Polymerization Regrowth Skin - cytology Time Factors Trajectories Tumor Cells, Cultured |
title | Microtubule Release from the Centrosome in Migrating Cells |
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