Actin filaments regulate microtubule growth at the centrosome
The centrosome is the main microtubule‐organizing centre. It also organizes a local network of actin filaments. However, the precise function of the actin network at the centrosome is not well understood. Here, we show that increasing densities of actin filaments at the centrosome of lymphocytes are...
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description | The centrosome is the main microtubule‐organizing centre. It also organizes a local network of actin filaments. However, the precise function of the actin network at the centrosome is not well understood. Here, we show that increasing densities of actin filaments at the centrosome of lymphocytes are correlated with reduced amounts of microtubules. Furthermore, lymphocyte activation resulted in disassembly of centrosomal actin and an increase in microtubule number. To further investigate the direct crosstalk between actin and microtubules at the centrosome, we performed
in vitro
reconstitution assays based on (i) purified centrosomes and (ii) on the co‐micropatterning of microtubule seeds and actin filaments. These two assays demonstrated that actin filaments constitute a physical barrier blocking elongation of nascent microtubules. Finally, we showed that cell adhesion and cell spreading lead to lower densities of centrosomal actin, thus resulting in higher microtubule growth. We therefore propose a novel mechanism, by which the number of centrosomal microtubules is regulated by cell adhesion and actin‐network architecture.
Synopsis
Centrosomes, the main interphase microtubule‐organizing centers of the cell, also nucleate local actin filament networks, which are now found to form a physical barrier blocking microtubule elongation.
Activation of B lymphocytes is associated with reduction of centrosomal actin and increase in the number of microtubules.
The amount of centrosomal actin is negatively correlated to the amount of microtubules.
In vitro
reconstitutions show negative correlation between the amount of centrosomal actin and the number of microtubules.
Cell spreading proportionally affects the amount of centrosomal actin and the number of centrosomal microtubules.
Graphical Abstract
Increasing density of F‐actin nucleating from the main interphase microtubule‐organizing center creates a physical barrier for nascent microtubules in lymphocytes and
in vitro
. |
doi_str_mv | 10.15252/embj.201899630 |
format | Article |
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in vitro
reconstitution assays based on (i) purified centrosomes and (ii) on the co‐micropatterning of microtubule seeds and actin filaments. These two assays demonstrated that actin filaments constitute a physical barrier blocking elongation of nascent microtubules. Finally, we showed that cell adhesion and cell spreading lead to lower densities of centrosomal actin, thus resulting in higher microtubule growth. We therefore propose a novel mechanism, by which the number of centrosomal microtubules is regulated by cell adhesion and actin‐network architecture.
Synopsis
Centrosomes, the main interphase microtubule‐organizing centers of the cell, also nucleate local actin filament networks, which are now found to form a physical barrier blocking microtubule elongation.
Activation of B lymphocytes is associated with reduction of centrosomal actin and increase in the number of microtubules.
The amount of centrosomal actin is negatively correlated to the amount of microtubules.
In vitro
reconstitutions show negative correlation between the amount of centrosomal actin and the number of microtubules.
Cell spreading proportionally affects the amount of centrosomal actin and the number of centrosomal microtubules.
Graphical Abstract
Increasing density of F‐actin nucleating from the main interphase microtubule‐organizing center creates a physical barrier for nascent microtubules in lymphocytes and
in vitro
.</description><identifier>ISSN: 0261-4189</identifier><identifier>EISSN: 1460-2075</identifier><identifier>DOI: 10.15252/embj.201899630</identifier><identifier>PMID: 30902847</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Actin ; Actin Cytoskeleton - physiology ; Actins - metabolism ; Adhesion ; Animals ; Barriers ; Cattle ; Cell activation ; Cell adhesion ; Cell adhesion & migration ; Cell spreading ; Cells, Cultured ; centrosome ; Centrosome - metabolism ; Centrosomes ; Correlation ; Crosstalk ; Dismantling ; Elongation ; EMBO05 ; EMBO19 ; Filaments ; Humans ; Jurkat Cells ; Life Sciences ; Lymphocytes ; Lymphocytes B ; Mice ; Micropatterning ; microtubule ; Microtubule-Associated Proteins - metabolism ; Microtubules ; Microtubules - metabolism ; Seeds ; Spreading ; Vegetal Biology</subject><ispartof>The EMBO journal, 2019-06, Vol.38 (11), p.n/a</ispartof><rights>The Author(s) 2019</rights><rights>2019 The Authors</rights><rights>2019 The Authors.</rights><rights>2019 EMBO</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6130-f90634835b752e3ff95e2a0f7097474ff72bc049f1c47fead5fbcf67c2bcbda03</citedby><cites>FETCH-LOGICAL-c6130-f90634835b752e3ff95e2a0f7097474ff72bc049f1c47fead5fbcf67c2bcbda03</cites><orcidid>0000-0002-9968-1779 ; 0000-0002-4108-2714 ; 0000-0001-8146-9254 ; 0000-0003-4383-1034 ; 0000-0003-0665-1210 ; 0000-0002-5124-6970</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/PMC6545561/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6545561/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,1411,1427,27901,27902,41096,42165,45550,45551,46384,46808,51551,53766,53768</link.rule.ids><linktorsrc>$$Uhttps://doi.org/10.15252/embj.201899630$$EView_record_in_Springer_Nature$$FView_record_in_$$GSpringer_Nature</linktorsrc><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30902847$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02620702$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Inoue, Daisuke</creatorcontrib><creatorcontrib>Obino, Dorian</creatorcontrib><creatorcontrib>Pineau, Judith</creatorcontrib><creatorcontrib>Farina, Francesca</creatorcontrib><creatorcontrib>Gaillard, Jérémie</creatorcontrib><creatorcontrib>Guerin, Christophe</creatorcontrib><creatorcontrib>Blanchoin, Laurent</creatorcontrib><creatorcontrib>Lennon‐Duménil, Ana‐Maria</creatorcontrib><creatorcontrib>Théry, Manuel</creatorcontrib><title>Actin filaments regulate microtubule growth at the centrosome</title><title>The EMBO journal</title><addtitle>EMBO J</addtitle><addtitle>EMBO J</addtitle><description>The centrosome is the main microtubule‐organizing centre. It also organizes a local network of actin filaments. However, the precise function of the actin network at the centrosome is not well understood. Here, we show that increasing densities of actin filaments at the centrosome of lymphocytes are correlated with reduced amounts of microtubules. Furthermore, lymphocyte activation resulted in disassembly of centrosomal actin and an increase in microtubule number. To further investigate the direct crosstalk between actin and microtubules at the centrosome, we performed
in vitro
reconstitution assays based on (i) purified centrosomes and (ii) on the co‐micropatterning of microtubule seeds and actin filaments. These two assays demonstrated that actin filaments constitute a physical barrier blocking elongation of nascent microtubules. Finally, we showed that cell adhesion and cell spreading lead to lower densities of centrosomal actin, thus resulting in higher microtubule growth. We therefore propose a novel mechanism, by which the number of centrosomal microtubules is regulated by cell adhesion and actin‐network architecture.
Synopsis
Centrosomes, the main interphase microtubule‐organizing centers of the cell, also nucleate local actin filament networks, which are now found to form a physical barrier blocking microtubule elongation.
Activation of B lymphocytes is associated with reduction of centrosomal actin and increase in the number of microtubules.
The amount of centrosomal actin is negatively correlated to the amount of microtubules.
In vitro
reconstitutions show negative correlation between the amount of centrosomal actin and the number of microtubules.
Cell spreading proportionally affects the amount of centrosomal actin and the number of centrosomal microtubules.
Graphical Abstract
Increasing density of F‐actin nucleating from the main interphase microtubule‐organizing center creates a physical barrier for nascent microtubules in lymphocytes and
in vitro
.</description><subject>Actin</subject><subject>Actin Cytoskeleton - physiology</subject><subject>Actins - metabolism</subject><subject>Adhesion</subject><subject>Animals</subject><subject>Barriers</subject><subject>Cattle</subject><subject>Cell activation</subject><subject>Cell adhesion</subject><subject>Cell adhesion & migration</subject><subject>Cell spreading</subject><subject>Cells, Cultured</subject><subject>centrosome</subject><subject>Centrosome - metabolism</subject><subject>Centrosomes</subject><subject>Correlation</subject><subject>Crosstalk</subject><subject>Dismantling</subject><subject>Elongation</subject><subject>EMBO05</subject><subject>EMBO19</subject><subject>Filaments</subject><subject>Humans</subject><subject>Jurkat Cells</subject><subject>Life Sciences</subject><subject>Lymphocytes</subject><subject>Lymphocytes B</subject><subject>Mice</subject><subject>Micropatterning</subject><subject>microtubule</subject><subject>Microtubule-Associated Proteins - metabolism</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Seeds</subject><subject>Spreading</subject><subject>Vegetal Biology</subject><issn>0261-4189</issn><issn>1460-2075</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1u1DAUhS0EotOBNTsUiU27SHv9n7CoNFSFggaxgbXleK5nMspPsZNWfRuehSfD05ShVEKsLF1_5_j4HkJeUTihkkl2im21PWFAi7JUHJ6QGRUKcgZaPiUzYIrmIt0dkMMYtwAgC02fkwMOJbBC6Bk5W7ih7jJfN7bFbohZwPXY2AGztnahH8ZqbDBbh_5m2GR2yIYN_vzhEhn62Lf4gjzzton48v6ck2_vL76eX-bLLx8-ni-WuVOUQ-5LUFwUXFZaMuTelxKZBa-h1EIL7zWrHIjSUye0R7uSvnJeaZfG1coCn5OzyfdqrFpc3QWwjbkKdWvDreltbf6-6eqNWffXRkkhZcowJ8eTweaR7HKxNLtZ2lXaGrDrHXt0_1jov48YB9PW0WHT2A77MRpGSyU5B6oT-uYRuu3H0KVVGMY416KAQiXqdKLSRmMM6PcJKJi7Hs2uR7PvMSleP_zvnv9dXALeTsBN3eDt__zMxed3nx66wySOSdetMfxJ_a9AvwAMx7rj</recordid><startdate>20190603</startdate><enddate>20190603</enddate><creator>Inoue, Daisuke</creator><creator>Obino, Dorian</creator><creator>Pineau, Judith</creator><creator>Farina, Francesca</creator><creator>Gaillard, Jérémie</creator><creator>Guerin, Christophe</creator><creator>Blanchoin, Laurent</creator><creator>Lennon‐Duménil, Ana‐Maria</creator><creator>Théry, Manuel</creator><general>Nature Publishing Group UK</general><general>Springer Nature B.V</general><general>EMBO Press</general><general>John Wiley and Sons Inc</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</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>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9968-1779</orcidid><orcidid>https://orcid.org/0000-0002-4108-2714</orcidid><orcidid>https://orcid.org/0000-0001-8146-9254</orcidid><orcidid>https://orcid.org/0000-0003-4383-1034</orcidid><orcidid>https://orcid.org/0000-0003-0665-1210</orcidid><orcidid>https://orcid.org/0000-0002-5124-6970</orcidid></search><sort><creationdate>20190603</creationdate><title>Actin filaments regulate microtubule growth at the centrosome</title><author>Inoue, Daisuke ; Obino, Dorian ; Pineau, Judith ; Farina, Francesca ; Gaillard, Jérémie ; Guerin, Christophe ; Blanchoin, Laurent ; Lennon‐Duménil, Ana‐Maria ; Théry, Manuel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6130-f90634835b752e3ff95e2a0f7097474ff72bc049f1c47fead5fbcf67c2bcbda03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Actin</topic><topic>Actin Cytoskeleton - physiology</topic><topic>Actins - metabolism</topic><topic>Adhesion</topic><topic>Animals</topic><topic>Barriers</topic><topic>Cattle</topic><topic>Cell activation</topic><topic>Cell adhesion</topic><topic>Cell adhesion & migration</topic><topic>Cell spreading</topic><topic>Cells, Cultured</topic><topic>centrosome</topic><topic>Centrosome - metabolism</topic><topic>Centrosomes</topic><topic>Correlation</topic><topic>Crosstalk</topic><topic>Dismantling</topic><topic>Elongation</topic><topic>EMBO05</topic><topic>EMBO19</topic><topic>Filaments</topic><topic>Humans</topic><topic>Jurkat Cells</topic><topic>Life Sciences</topic><topic>Lymphocytes</topic><topic>Lymphocytes B</topic><topic>Mice</topic><topic>Micropatterning</topic><topic>microtubule</topic><topic>Microtubule-Associated Proteins - metabolism</topic><topic>Microtubules</topic><topic>Microtubules - metabolism</topic><topic>Seeds</topic><topic>Spreading</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Inoue, Daisuke</creatorcontrib><creatorcontrib>Obino, Dorian</creatorcontrib><creatorcontrib>Pineau, Judith</creatorcontrib><creatorcontrib>Farina, Francesca</creatorcontrib><creatorcontrib>Gaillard, Jérémie</creatorcontrib><creatorcontrib>Guerin, Christophe</creatorcontrib><creatorcontrib>Blanchoin, Laurent</creatorcontrib><creatorcontrib>Lennon‐Duménil, Ana‐Maria</creatorcontrib><creatorcontrib>Théry, Manuel</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences 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>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The EMBO journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Inoue, Daisuke</au><au>Obino, Dorian</au><au>Pineau, Judith</au><au>Farina, Francesca</au><au>Gaillard, Jérémie</au><au>Guerin, Christophe</au><au>Blanchoin, Laurent</au><au>Lennon‐Duménil, Ana‐Maria</au><au>Théry, Manuel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Actin filaments regulate microtubule growth at the centrosome</atitle><jtitle>The EMBO journal</jtitle><stitle>EMBO J</stitle><addtitle>EMBO J</addtitle><date>2019-06-03</date><risdate>2019</risdate><volume>38</volume><issue>11</issue><epage>n/a</epage><issn>0261-4189</issn><eissn>1460-2075</eissn><abstract>The centrosome is the main microtubule‐organizing centre. It also organizes a local network of actin filaments. However, the precise function of the actin network at the centrosome is not well understood. Here, we show that increasing densities of actin filaments at the centrosome of lymphocytes are correlated with reduced amounts of microtubules. Furthermore, lymphocyte activation resulted in disassembly of centrosomal actin and an increase in microtubule number. To further investigate the direct crosstalk between actin and microtubules at the centrosome, we performed
in vitro
reconstitution assays based on (i) purified centrosomes and (ii) on the co‐micropatterning of microtubule seeds and actin filaments. These two assays demonstrated that actin filaments constitute a physical barrier blocking elongation of nascent microtubules. Finally, we showed that cell adhesion and cell spreading lead to lower densities of centrosomal actin, thus resulting in higher microtubule growth. We therefore propose a novel mechanism, by which the number of centrosomal microtubules is regulated by cell adhesion and actin‐network architecture.
Synopsis
Centrosomes, the main interphase microtubule‐organizing centers of the cell, also nucleate local actin filament networks, which are now found to form a physical barrier blocking microtubule elongation.
Activation of B lymphocytes is associated with reduction of centrosomal actin and increase in the number of microtubules.
The amount of centrosomal actin is negatively correlated to the amount of microtubules.
In vitro
reconstitutions show negative correlation between the amount of centrosomal actin and the number of microtubules.
Cell spreading proportionally affects the amount of centrosomal actin and the number of centrosomal microtubules.
Graphical Abstract
Increasing density of F‐actin nucleating from the main interphase microtubule‐organizing center creates a physical barrier for nascent microtubules in lymphocytes and
in vitro
.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>30902847</pmid><doi>10.15252/embj.201899630</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-9968-1779</orcidid><orcidid>https://orcid.org/0000-0002-4108-2714</orcidid><orcidid>https://orcid.org/0000-0001-8146-9254</orcidid><orcidid>https://orcid.org/0000-0003-4383-1034</orcidid><orcidid>https://orcid.org/0000-0003-0665-1210</orcidid><orcidid>https://orcid.org/0000-0002-5124-6970</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Actin Actin Cytoskeleton - physiology Actins - metabolism Adhesion Animals Barriers Cattle Cell activation Cell adhesion Cell adhesion & migration Cell spreading Cells, Cultured centrosome Centrosome - metabolism Centrosomes Correlation Crosstalk Dismantling Elongation EMBO05 EMBO19 Filaments Humans Jurkat Cells Life Sciences Lymphocytes Lymphocytes B Mice Micropatterning microtubule Microtubule-Associated Proteins - metabolism Microtubules Microtubules - metabolism Seeds Spreading Vegetal Biology |
title | Actin filaments regulate microtubule growth at the centrosome |
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