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Myosin II isoforms play distinct roles in adherens junction biogenesis
Adherens junction (AJ) assembly under force is essential for many biological processes like epithelial monolayer bending, collective cell migration, cell extrusion and wound healing. The acto-myosin cytoskeleton acts as a major force-generator during the de novo formation and remodeling of AJ. Here,...
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creator | Heuzé, Mélina L Sankara Narayana, Gautham Hari Narayana D'Alessandro, Joseph Cellerin, Victor Dang, Tien Williams, David S Van Hest, Jan Cm Marcq, Philippe Mège, René-Marc Ladoux, Benoit |
description | Adherens junction (AJ) assembly under force is essential for many biological processes like epithelial monolayer bending, collective cell migration, cell extrusion and wound healing. The acto-myosin cytoskeleton acts as a major force-generator during the de novo formation and remodeling of AJ. Here, we investigated the role of non-muscle myosin II isoforms (NMIIA and NMIIB) in epithelial junction assembly. NMIIA and NMIIB differentially regulate biogenesis of AJ through association with distinct actin networks. Analysis of junction dynamics, actin organization, and mechanical forces of control and knockdown cells for myosins revealed that NMIIA provides the mechanical tugging force necessary for cell-cell junction reinforcement and maintenance. NMIIB is involved in E-cadherin clustering, maintenance of a branched actin layer connecting E-cadherin complexes and perijunctional actin fibres leading to the building-up of anisotropic stress. These data reveal unanticipated complementary functions of NMIIA and NMIIB in the biogenesis and integrity of AJ. |
doi_str_mv | 10.7554/eLife.46599 |
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The acto-myosin cytoskeleton acts as a major force-generator during the de novo formation and remodeling of AJ. Here, we investigated the role of non-muscle myosin II isoforms (NMIIA and NMIIB) in epithelial junction assembly. NMIIA and NMIIB differentially regulate biogenesis of AJ through association with distinct actin networks. Analysis of junction dynamics, actin organization, and mechanical forces of control and knockdown cells for myosins revealed that NMIIA provides the mechanical tugging force necessary for cell-cell junction reinforcement and maintenance. NMIIB is involved in E-cadherin clustering, maintenance of a branched actin layer connecting E-cadherin complexes and perijunctional actin fibres leading to the building-up of anisotropic stress. These data reveal unanticipated complementary functions of NMIIA and NMIIB in the biogenesis and integrity of AJ.</description><identifier>ISSN: 2050-084X</identifier><identifier>EISSN: 2050-084X</identifier><identifier>DOI: 10.7554/eLife.46599</identifier><identifier>PMID: 31486768</identifier><language>eng</language><publisher>England: eLife Science Publications, Ltd</publisher><subject>Actin ; adherens junctions ; Adherens Junctions - metabolism ; Animals ; Anisotropy ; Antigens, CD - metabolism ; Biosynthesis ; Cadherins - metabolism ; Cell adhesion & migration ; Cell Behavior ; Cell Biology ; Cell junctions ; Cell Line ; Cell migration ; Cellular Biology ; Cytoskeleton ; Dogs ; E-cadherin ; epithelial cells ; Epithelial Cells - metabolism ; Humans ; Isoforms ; Life Sciences ; mechanobiology ; Microscopy ; Morphogenesis ; Muscle proteins ; Myosin ; Myosin Heavy Chains - metabolism ; Nonmuscle Myosin Type IIB - metabolism ; Observations ; Physics of Living Systems ; Physiological aspects ; Protein Binding ; Wound care ; Wound healing ; Wounds</subject><ispartof>eLife, 2019-09, Vol.8</ispartof><rights>2019, Heuzé et al.</rights><rights>COPYRIGHT 2019 eLife Science Publications, Ltd.</rights><rights>2019, Heuzé et al. This work is published under http://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>2019, Heuzé et al 2019 Heuzé et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c676t-6d2a9c8237749afb9f92a33f3c3b9d311bdb0ec3dce488acda95c7951cc41d363</citedby><cites>FETCH-LOGICAL-c676t-6d2a9c8237749afb9f92a33f3c3b9d311bdb0ec3dce488acda95c7951cc41d363</cites><orcidid>0000-0001-8128-5543 ; 0000-0002-1585-3255 ; 0000-0003-2086-1556 ; 0000-0002-4271-2706 ; 0000-0002-2534-5836 ; 0000-0002-3232-9156</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2299406839/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2299406839?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25751,27922,27923,37010,37011,44588,53789,53791,74896</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31486768$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.sorbonne-universite.fr/hal-02312237$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Heuzé, Mélina L</creatorcontrib><creatorcontrib>Sankara Narayana, Gautham Hari Narayana</creatorcontrib><creatorcontrib>D'Alessandro, Joseph</creatorcontrib><creatorcontrib>Cellerin, Victor</creatorcontrib><creatorcontrib>Dang, Tien</creatorcontrib><creatorcontrib>Williams, David S</creatorcontrib><creatorcontrib>Van Hest, Jan Cm</creatorcontrib><creatorcontrib>Marcq, Philippe</creatorcontrib><creatorcontrib>Mège, René-Marc</creatorcontrib><creatorcontrib>Ladoux, Benoit</creatorcontrib><title>Myosin II isoforms play distinct roles in adherens junction biogenesis</title><title>eLife</title><addtitle>Elife</addtitle><description>Adherens junction (AJ) assembly under force is essential for many biological processes like epithelial monolayer bending, collective cell migration, cell extrusion and wound healing. The acto-myosin cytoskeleton acts as a major force-generator during the de novo formation and remodeling of AJ. Here, we investigated the role of non-muscle myosin II isoforms (NMIIA and NMIIB) in epithelial junction assembly. NMIIA and NMIIB differentially regulate biogenesis of AJ through association with distinct actin networks. Analysis of junction dynamics, actin organization, and mechanical forces of control and knockdown cells for myosins revealed that NMIIA provides the mechanical tugging force necessary for cell-cell junction reinforcement and maintenance. NMIIB is involved in E-cadherin clustering, maintenance of a branched actin layer connecting E-cadherin complexes and perijunctional actin fibres leading to the building-up of anisotropic stress. These data reveal unanticipated complementary functions of NMIIA and NMIIB in the biogenesis and integrity of AJ.</description><subject>Actin</subject><subject>adherens junctions</subject><subject>Adherens Junctions - metabolism</subject><subject>Animals</subject><subject>Anisotropy</subject><subject>Antigens, CD - metabolism</subject><subject>Biosynthesis</subject><subject>Cadherins - metabolism</subject><subject>Cell adhesion & migration</subject><subject>Cell Behavior</subject><subject>Cell Biology</subject><subject>Cell junctions</subject><subject>Cell Line</subject><subject>Cell migration</subject><subject>Cellular Biology</subject><subject>Cytoskeleton</subject><subject>Dogs</subject><subject>E-cadherin</subject><subject>epithelial cells</subject><subject>Epithelial Cells - metabolism</subject><subject>Humans</subject><subject>Isoforms</subject><subject>Life Sciences</subject><subject>mechanobiology</subject><subject>Microscopy</subject><subject>Morphogenesis</subject><subject>Muscle proteins</subject><subject>Myosin</subject><subject>Myosin Heavy Chains - metabolism</subject><subject>Nonmuscle Myosin Type IIB - metabolism</subject><subject>Observations</subject><subject>Physics of Living Systems</subject><subject>Physiological aspects</subject><subject>Protein Binding</subject><subject>Wound care</subject><subject>Wound healing</subject><subject>Wounds</subject><issn>2050-084X</issn><issn>2050-084X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkstrGzEQh5fS0gQ3p97LQi8Nxa5eq11dCiY0zYJLoQ_oTWj1sGXWkivthvi_79hO0zhUOkiMvvnNQ1MUrzGa1VXFPtiFd3bGeCXEs-KcoApNUcN-PX90Pysucl4jWDVrGixeFmcUs4bXvDkvrr_sYvahbNvS5-hi2uRy26tdaXwefNBDmWJvcwmIMiubbMjlegS7j6HsfFzaYLPPr4oXTvXZXtyfk-Ln9acfVzfTxdfP7dV8MdUQbphyQ5TQDaF1zYRynXCCKEod1bQThmLcmQ5ZTY22kKrSRolK16LCWjNsKKeToj3qmqjWcpv8RqWdjMrLgyGmpVRp8Lq3kjpHjSEYE8YZpUIRTZjoONcgzCDmpPh41NqO3cZCyDAk1Z-Inr4Ev5LLeCt5XfG6ESBweRRYPXG7mS_k3oYIxQSKvcXAvrsPluLv0eZBbnzWtu9VsHHMkpCmwogwhgB9-wRdxzEFaCtQQjDEGyr-UUsFxfrgIuSo96JyzhH8PXB7avYfCraxG69jsM6D_cTh8sQBmMHeDUs15izb799O2fdHVqeYc7LuoQkYyf10ysN0ysN0Av3mcbsf2L-zSP8A5ObdPg</recordid><startdate>20190905</startdate><enddate>20190905</enddate><creator>Heuzé, Mélina L</creator><creator>Sankara Narayana, Gautham Hari Narayana</creator><creator>D'Alessandro, Joseph</creator><creator>Cellerin, Victor</creator><creator>Dang, Tien</creator><creator>Williams, David S</creator><creator>Van Hest, Jan Cm</creator><creator>Marcq, Philippe</creator><creator>Mège, René-Marc</creator><creator>Ladoux, Benoit</creator><general>eLife Science Publications, Ltd</general><general>eLife Sciences Publications Ltd</general><general>eLife Sciences Publication</general><general>eLife Sciences Publications, Ltd</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>ISR</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/0000-0001-8128-5543</orcidid><orcidid>https://orcid.org/0000-0002-1585-3255</orcidid><orcidid>https://orcid.org/0000-0003-2086-1556</orcidid><orcidid>https://orcid.org/0000-0002-4271-2706</orcidid><orcidid>https://orcid.org/0000-0002-2534-5836</orcidid><orcidid>https://orcid.org/0000-0002-3232-9156</orcidid></search><sort><creationdate>20190905</creationdate><title>Myosin II isoforms play distinct roles in adherens junction biogenesis</title><author>Heuzé, Mélina L ; Sankara Narayana, Gautham Hari Narayana ; D'Alessandro, Joseph ; Cellerin, Victor ; Dang, Tien ; Williams, David S ; Van Hest, Jan Cm ; Marcq, Philippe ; Mège, René-Marc ; Ladoux, Benoit</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c676t-6d2a9c8237749afb9f92a33f3c3b9d311bdb0ec3dce488acda95c7951cc41d363</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Actin</topic><topic>adherens junctions</topic><topic>Adherens Junctions - metabolism</topic><topic>Animals</topic><topic>Anisotropy</topic><topic>Antigens, CD - metabolism</topic><topic>Biosynthesis</topic><topic>Cadherins - metabolism</topic><topic>Cell adhesion & migration</topic><topic>Cell Behavior</topic><topic>Cell Biology</topic><topic>Cell junctions</topic><topic>Cell Line</topic><topic>Cell migration</topic><topic>Cellular Biology</topic><topic>Cytoskeleton</topic><topic>Dogs</topic><topic>E-cadherin</topic><topic>epithelial cells</topic><topic>Epithelial Cells - metabolism</topic><topic>Humans</topic><topic>Isoforms</topic><topic>Life Sciences</topic><topic>mechanobiology</topic><topic>Microscopy</topic><topic>Morphogenesis</topic><topic>Muscle proteins</topic><topic>Myosin</topic><topic>Myosin Heavy Chains - metabolism</topic><topic>Nonmuscle Myosin Type IIB - metabolism</topic><topic>Observations</topic><topic>Physics of Living Systems</topic><topic>Physiological aspects</topic><topic>Protein Binding</topic><topic>Wound care</topic><topic>Wound healing</topic><topic>Wounds</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Heuzé, Mélina L</creatorcontrib><creatorcontrib>Sankara Narayana, Gautham Hari Narayana</creatorcontrib><creatorcontrib>D'Alessandro, Joseph</creatorcontrib><creatorcontrib>Cellerin, Victor</creatorcontrib><creatorcontrib>Dang, Tien</creatorcontrib><creatorcontrib>Williams, David S</creatorcontrib><creatorcontrib>Van Hest, Jan Cm</creatorcontrib><creatorcontrib>Marcq, Philippe</creatorcontrib><creatorcontrib>Mège, René-Marc</creatorcontrib><creatorcontrib>Ladoux, Benoit</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest_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 (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest Science Journals</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</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>Heuzé, Mélina L</au><au>Sankara Narayana, Gautham Hari Narayana</au><au>D'Alessandro, Joseph</au><au>Cellerin, Victor</au><au>Dang, Tien</au><au>Williams, David S</au><au>Van Hest, Jan Cm</au><au>Marcq, Philippe</au><au>Mège, René-Marc</au><au>Ladoux, Benoit</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Myosin II isoforms play distinct roles in adherens junction biogenesis</atitle><jtitle>eLife</jtitle><addtitle>Elife</addtitle><date>2019-09-05</date><risdate>2019</risdate><volume>8</volume><issn>2050-084X</issn><eissn>2050-084X</eissn><abstract>Adherens junction (AJ) assembly under force is essential for many biological processes like epithelial monolayer bending, collective cell migration, cell extrusion and wound healing. The acto-myosin cytoskeleton acts as a major force-generator during the de novo formation and remodeling of AJ. Here, we investigated the role of non-muscle myosin II isoforms (NMIIA and NMIIB) in epithelial junction assembly. NMIIA and NMIIB differentially regulate biogenesis of AJ through association with distinct actin networks. Analysis of junction dynamics, actin organization, and mechanical forces of control and knockdown cells for myosins revealed that NMIIA provides the mechanical tugging force necessary for cell-cell junction reinforcement and maintenance. NMIIB is involved in E-cadherin clustering, maintenance of a branched actin layer connecting E-cadherin complexes and perijunctional actin fibres leading to the building-up of anisotropic stress. These data reveal unanticipated complementary functions of NMIIA and NMIIB in the biogenesis and integrity of AJ.</abstract><cop>England</cop><pub>eLife Science Publications, Ltd</pub><pmid>31486768</pmid><doi>10.7554/eLife.46599</doi><orcidid>https://orcid.org/0000-0001-8128-5543</orcidid><orcidid>https://orcid.org/0000-0002-1585-3255</orcidid><orcidid>https://orcid.org/0000-0003-2086-1556</orcidid><orcidid>https://orcid.org/0000-0002-4271-2706</orcidid><orcidid>https://orcid.org/0000-0002-2534-5836</orcidid><orcidid>https://orcid.org/0000-0002-3232-9156</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Actin adherens junctions Adherens Junctions - metabolism Animals Anisotropy Antigens, CD - metabolism Biosynthesis Cadherins - metabolism Cell adhesion & migration Cell Behavior Cell Biology Cell junctions Cell Line Cell migration Cellular Biology Cytoskeleton Dogs E-cadherin epithelial cells Epithelial Cells - metabolism Humans Isoforms Life Sciences mechanobiology Microscopy Morphogenesis Muscle proteins Myosin Myosin Heavy Chains - metabolism Nonmuscle Myosin Type IIB - metabolism Observations Physics of Living Systems Physiological aspects Protein Binding Wound care Wound healing Wounds |
title | Myosin II isoforms play distinct roles in adherens junction biogenesis |
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