Loading…
Microtubules restrict F-actin polymerization to the immune synapse via GEF-H1 to maintain polarity in lymphocytes
Immune synapse formation is a key step for lymphocyte activation. In B lymphocytes, the immune synapse controls the production of high-affinity antibodies, thereby defining the efficiency of humoral immune responses. While the key roles played by both the actin and microtubule cytoskeletons in the f...
Saved in:
Published in: | eLife 2022-09, Vol.11 |
---|---|
Main Authors: | , , , , , |
Format: | Article |
Language: | English |
Subjects: | |
Citations: | Items that this one cites Items that cite this one |
Online Access: | Get full text |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
cited_by | cdi_FETCH-LOGICAL-c486t-d316358cf916fc72ab2a95f988f94debcabd71a348bca4afd182656512e27d693 |
---|---|
cites | cdi_FETCH-LOGICAL-c486t-d316358cf916fc72ab2a95f988f94debcabd71a348bca4afd182656512e27d693 |
container_end_page | |
container_issue | |
container_start_page | |
container_title | eLife |
container_volume | 11 |
creator | Pineau, Judith Pinon, Léa Mesdjian, Olivier Fattaccioli, Jacques Lennon Duménil, Ana-Maria Pierobon, Paolo |
description | Immune synapse formation is a key step for lymphocyte activation. In B lymphocytes, the immune synapse controls the production of high-affinity antibodies, thereby defining the efficiency of humoral immune responses. While the key roles played by both the actin and microtubule cytoskeletons in the formation and function of the immune synapse have become increasingly clear, how the different events involved in synapse formation are coordinated in space and time by actin–microtubule interactions is not understood. Using a microfluidic pairing device, we studied with unprecedented resolution the dynamics of the various events leading to immune synapse formation and maintenance in murine B cells. Our results identify two groups of events, local and global, dominated by actin and microtubules dynamics, respectively. They further highlight an unexpected role for microtubules and the GEF-H1-RhoA axis in restricting F-actin polymerization at the lymphocyte–antigen contact site, thereby allowing the formation and maintenance of a unique competent immune synapse. |
doi_str_mv | 10.7554/eLife.78330 |
format | article |
fullrecord | <record><control><sourceid>proquest_doaj_</sourceid><recordid>TN_cdi_doaj_primary_oai_doaj_org_article_8567b4f1384a47ec8f801b546e5ad540</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><doaj_id>oai_doaj_org_article_8567b4f1384a47ec8f801b546e5ad540</doaj_id><sourcerecordid>2730538712</sourcerecordid><originalsourceid>FETCH-LOGICAL-c486t-d316358cf916fc72ab2a95f988f94debcabd71a348bca4afd182656512e27d693</originalsourceid><addsrcrecordid>eNpdks1q3DAUhU1pacI0q76AoZuW4kSyfr0phJDJBCZ000J34lqWMxpsy5HkAefpqxmH0kQbXa6-eyR0TpZ9xuhSMEavzNa25lJIQtC77LxEDBVI0j_v_6vPsosQ9igtQaXE1cfsjHCMMRfoPHt6sNq7ONVTZ0LuTYje6pivC9DRDvnourk33j5DtG7Io8vjzuS276fB5GEeYAwmP1jI727XxQYfgR7sEGGZBW_jnKc6qYw7p-dowqfsQwtdMBcv-yr7vb79dbMptj_v7m-ut4WmkseiIZgTJnVbYd5qUUJdQsXaSsq2oo2pNdSNwECoTCWFtsGy5IwzXJpSNLwiq-x-0W0c7NXobQ9-Vg6sOjWcf1Tgo9WdUZJxUdMWE0mBCqNlKxGuGeWGQcMoSlo_Fq1xqnvTaDNED90r0dcng92pR3dQFatKlMxZZd8Wgd2bsc31Vh17iEhGKowOOLFfXy7z7mlKjqjeBm26DgbjpqBKUQpOmSQ8oV_eoHs3-SF9a6IIYkQKXCbq-0Ilp0Pwpv33AozUMUXqlCJ1ShH5C8O-ueY</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2730538712</pqid></control><display><type>article</type><title>Microtubules restrict F-actin polymerization to the immune synapse via GEF-H1 to maintain polarity in lymphocytes</title><source>PubMed Central Free</source><source>Publicly Available Content (ProQuest)</source><creator>Pineau, Judith ; Pinon, Léa ; Mesdjian, Olivier ; Fattaccioli, Jacques ; Lennon Duménil, Ana-Maria ; Pierobon, Paolo</creator><creatorcontrib>Pineau, Judith ; Pinon, Léa ; Mesdjian, Olivier ; Fattaccioli, Jacques ; Lennon Duménil, Ana-Maria ; Pierobon, Paolo</creatorcontrib><description>Immune synapse formation is a key step for lymphocyte activation. In B lymphocytes, the immune synapse controls the production of high-affinity antibodies, thereby defining the efficiency of humoral immune responses. While the key roles played by both the actin and microtubule cytoskeletons in the formation and function of the immune synapse have become increasingly clear, how the different events involved in synapse formation are coordinated in space and time by actin–microtubule interactions is not understood. Using a microfluidic pairing device, we studied with unprecedented resolution the dynamics of the various events leading to immune synapse formation and maintenance in murine B cells. Our results identify two groups of events, local and global, dominated by actin and microtubules dynamics, respectively. They further highlight an unexpected role for microtubules and the GEF-H1-RhoA axis in restricting F-actin polymerization at the lymphocyte–antigen contact site, thereby allowing the formation and maintenance of a unique competent immune synapse.</description><identifier>ISSN: 2050-084X</identifier><identifier>EISSN: 2050-084X</identifier><identifier>DOI: 10.7554/eLife.78330</identifier><identifier>PMID: 36111670</identifier><language>eng</language><publisher>Cambridge: eLife Sciences Publications Ltd</publisher><subject>Actin ; Adaptive immunology ; Antigens ; B lymphocytes ; Biochemistry, Molecular Biology ; Biophysics ; Cell activation ; Cell Biology ; cell polarity ; Cellular Biology ; Cytoskeleton ; Experiments ; GEF-H1 ; Immune response (humoral) ; immune synapse ; Immunology ; Immunology and Inflammation ; Life Sciences ; Ligands ; Lymphocytes ; Lymphocytes B ; Microfluidics ; Microtubules ; Polymerization ; RhoA protein ; Subcellular Processes ; Synapses</subject><ispartof>eLife, 2022-09, Vol.11</ispartof><rights>2022, Pineau et al. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2022, Pineau et al 2022 Pineau et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c486t-d316358cf916fc72ab2a95f988f94debcabd71a348bca4afd182656512e27d693</citedby><cites>FETCH-LOGICAL-c486t-d316358cf916fc72ab2a95f988f94debcabd71a348bca4afd182656512e27d693</cites><orcidid>0000-0002-3014-0181 ; 0000-0003-0665-1210 ; 0000-0002-0095-2576</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2730538712/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2730538712?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://hal.science/hal-03853910$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Pineau, Judith</creatorcontrib><creatorcontrib>Pinon, Léa</creatorcontrib><creatorcontrib>Mesdjian, Olivier</creatorcontrib><creatorcontrib>Fattaccioli, Jacques</creatorcontrib><creatorcontrib>Lennon Duménil, Ana-Maria</creatorcontrib><creatorcontrib>Pierobon, Paolo</creatorcontrib><title>Microtubules restrict F-actin polymerization to the immune synapse via GEF-H1 to maintain polarity in lymphocytes</title><title>eLife</title><description>Immune synapse formation is a key step for lymphocyte activation. In B lymphocytes, the immune synapse controls the production of high-affinity antibodies, thereby defining the efficiency of humoral immune responses. While the key roles played by both the actin and microtubule cytoskeletons in the formation and function of the immune synapse have become increasingly clear, how the different events involved in synapse formation are coordinated in space and time by actin–microtubule interactions is not understood. Using a microfluidic pairing device, we studied with unprecedented resolution the dynamics of the various events leading to immune synapse formation and maintenance in murine B cells. Our results identify two groups of events, local and global, dominated by actin and microtubules dynamics, respectively. They further highlight an unexpected role for microtubules and the GEF-H1-RhoA axis in restricting F-actin polymerization at the lymphocyte–antigen contact site, thereby allowing the formation and maintenance of a unique competent immune synapse.</description><subject>Actin</subject><subject>Adaptive immunology</subject><subject>Antigens</subject><subject>B lymphocytes</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biophysics</subject><subject>Cell activation</subject><subject>Cell Biology</subject><subject>cell polarity</subject><subject>Cellular Biology</subject><subject>Cytoskeleton</subject><subject>Experiments</subject><subject>GEF-H1</subject><subject>Immune response (humoral)</subject><subject>immune synapse</subject><subject>Immunology</subject><subject>Immunology and Inflammation</subject><subject>Life Sciences</subject><subject>Ligands</subject><subject>Lymphocytes</subject><subject>Lymphocytes B</subject><subject>Microfluidics</subject><subject>Microtubules</subject><subject>Polymerization</subject><subject>RhoA protein</subject><subject>Subcellular Processes</subject><subject>Synapses</subject><issn>2050-084X</issn><issn>2050-084X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNpdks1q3DAUhU1pacI0q76AoZuW4kSyfr0phJDJBCZ000J34lqWMxpsy5HkAefpqxmH0kQbXa6-eyR0TpZ9xuhSMEavzNa25lJIQtC77LxEDBVI0j_v_6vPsosQ9igtQaXE1cfsjHCMMRfoPHt6sNq7ONVTZ0LuTYje6pivC9DRDvnourk33j5DtG7Io8vjzuS276fB5GEeYAwmP1jI727XxQYfgR7sEGGZBW_jnKc6qYw7p-dowqfsQwtdMBcv-yr7vb79dbMptj_v7m-ut4WmkseiIZgTJnVbYd5qUUJdQsXaSsq2oo2pNdSNwECoTCWFtsGy5IwzXJpSNLwiq-x-0W0c7NXobQ9-Vg6sOjWcf1Tgo9WdUZJxUdMWE0mBCqNlKxGuGeWGQcMoSlo_Fq1xqnvTaDNED90r0dcng92pR3dQFatKlMxZZd8Wgd2bsc31Vh17iEhGKowOOLFfXy7z7mlKjqjeBm26DgbjpqBKUQpOmSQ8oV_eoHs3-SF9a6IIYkQKXCbq-0Ilp0Pwpv33AozUMUXqlCJ1ShH5C8O-ueY</recordid><startdate>20220916</startdate><enddate>20220916</enddate><creator>Pineau, Judith</creator><creator>Pinon, Léa</creator><creator>Mesdjian, Olivier</creator><creator>Fattaccioli, Jacques</creator><creator>Lennon Duménil, Ana-Maria</creator><creator>Pierobon, Paolo</creator><general>eLife Sciences Publications Ltd</general><general>eLife Sciences Publication</general><general>eLife Sciences Publications, Ltd</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-3014-0181</orcidid><orcidid>https://orcid.org/0000-0003-0665-1210</orcidid><orcidid>https://orcid.org/0000-0002-0095-2576</orcidid></search><sort><creationdate>20220916</creationdate><title>Microtubules restrict F-actin polymerization to the immune synapse via GEF-H1 to maintain polarity in lymphocytes</title><author>Pineau, Judith ; Pinon, Léa ; Mesdjian, Olivier ; Fattaccioli, Jacques ; Lennon Duménil, Ana-Maria ; Pierobon, Paolo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c486t-d316358cf916fc72ab2a95f988f94debcabd71a348bca4afd182656512e27d693</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Actin</topic><topic>Adaptive immunology</topic><topic>Antigens</topic><topic>B lymphocytes</topic><topic>Biochemistry, Molecular Biology</topic><topic>Biophysics</topic><topic>Cell activation</topic><topic>Cell Biology</topic><topic>cell polarity</topic><topic>Cellular Biology</topic><topic>Cytoskeleton</topic><topic>Experiments</topic><topic>GEF-H1</topic><topic>Immune response (humoral)</topic><topic>immune synapse</topic><topic>Immunology</topic><topic>Immunology and Inflammation</topic><topic>Life Sciences</topic><topic>Ligands</topic><topic>Lymphocytes</topic><topic>Lymphocytes B</topic><topic>Microfluidics</topic><topic>Microtubules</topic><topic>Polymerization</topic><topic>RhoA protein</topic><topic>Subcellular Processes</topic><topic>Synapses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pineau, Judith</creatorcontrib><creatorcontrib>Pinon, Léa</creatorcontrib><creatorcontrib>Mesdjian, Olivier</creatorcontrib><creatorcontrib>Fattaccioli, Jacques</creatorcontrib><creatorcontrib>Lennon Duménil, Ana-Maria</creatorcontrib><creatorcontrib>Pierobon, Paolo</creatorcontrib><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>ProQuest Biological Science Journals</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</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><collection>DOAJ Directory of Open Access Journals</collection><jtitle>eLife</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pineau, Judith</au><au>Pinon, Léa</au><au>Mesdjian, Olivier</au><au>Fattaccioli, Jacques</au><au>Lennon Duménil, Ana-Maria</au><au>Pierobon, Paolo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Microtubules restrict F-actin polymerization to the immune synapse via GEF-H1 to maintain polarity in lymphocytes</atitle><jtitle>eLife</jtitle><date>2022-09-16</date><risdate>2022</risdate><volume>11</volume><issn>2050-084X</issn><eissn>2050-084X</eissn><abstract>Immune synapse formation is a key step for lymphocyte activation. In B lymphocytes, the immune synapse controls the production of high-affinity antibodies, thereby defining the efficiency of humoral immune responses. While the key roles played by both the actin and microtubule cytoskeletons in the formation and function of the immune synapse have become increasingly clear, how the different events involved in synapse formation are coordinated in space and time by actin–microtubule interactions is not understood. Using a microfluidic pairing device, we studied with unprecedented resolution the dynamics of the various events leading to immune synapse formation and maintenance in murine B cells. Our results identify two groups of events, local and global, dominated by actin and microtubules dynamics, respectively. They further highlight an unexpected role for microtubules and the GEF-H1-RhoA axis in restricting F-actin polymerization at the lymphocyte–antigen contact site, thereby allowing the formation and maintenance of a unique competent immune synapse.</abstract><cop>Cambridge</cop><pub>eLife Sciences Publications Ltd</pub><pmid>36111670</pmid><doi>10.7554/eLife.78330</doi><orcidid>https://orcid.org/0000-0002-3014-0181</orcidid><orcidid>https://orcid.org/0000-0003-0665-1210</orcidid><orcidid>https://orcid.org/0000-0002-0095-2576</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 2050-084X |
ispartof | eLife, 2022-09, Vol.11 |
issn | 2050-084X 2050-084X |
language | eng |
recordid | cdi_doaj_primary_oai_doaj_org_article_8567b4f1384a47ec8f801b546e5ad540 |
source | PubMed Central Free; Publicly Available Content (ProQuest) |
subjects | Actin Adaptive immunology Antigens B lymphocytes Biochemistry, Molecular Biology Biophysics Cell activation Cell Biology cell polarity Cellular Biology Cytoskeleton Experiments GEF-H1 Immune response (humoral) immune synapse Immunology Immunology and Inflammation Life Sciences Ligands Lymphocytes Lymphocytes B Microfluidics Microtubules Polymerization RhoA protein Subcellular Processes Synapses |
title | Microtubules restrict F-actin polymerization to the immune synapse via GEF-H1 to maintain polarity in lymphocytes |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-29T05%3A54%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_doaj_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Microtubules%20restrict%20F-actin%20polymerization%20to%20the%20immune%20synapse%20via%20GEF-H1%20to%20maintain%20polarity%20in%20lymphocytes&rft.jtitle=eLife&rft.au=Pineau,%20Judith&rft.date=2022-09-16&rft.volume=11&rft.issn=2050-084X&rft.eissn=2050-084X&rft_id=info:doi/10.7554/eLife.78330&rft_dat=%3Cproquest_doaj_%3E2730538712%3C/proquest_doaj_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c486t-d316358cf916fc72ab2a95f988f94debcabd71a348bca4afd182656512e27d693%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2730538712&rft_id=info:pmid/36111670&rfr_iscdi=true |