TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo
LIM-domain-containing repeat (LCR) proteins are recruited to strained actin filaments within stress fibers in cultured cells, but their roles at cell-cell junctions in living organisms have not been extensively studied. Here, we show that the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX-1/Z...
Gespeichert in:
Veröffentlicht in: | Current biology 2022-12, Vol.32 (23), p.5189-5199.e6 |
---|---|
Hauptverfasser: | , , , , , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 5199.e6 |
---|---|
container_issue | 23 |
container_start_page | 5189 |
container_title | Current biology |
container_volume | 32 |
creator | Lynch, Allison M Zhu, Yuyun Lucas, Bethany G Winkelman, Jonathan D Bai, Keliya Martin, Sterling C T Block, Samuel Slabodnick, Mark M Audhya, Anjon Goldstein, Bob Pettitt, Jonathan Gardel, Margaret L Hardin, Jeff |
description | LIM-domain-containing repeat (LCR) proteins are recruited to strained actin filaments within stress fibers in cultured cells,
but their roles at cell-cell junctions in living organisms have not been extensively studied. Here, we show that the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX-1/Zyxin are recruited to apical junctions during embryonic elongation when junctions are under tension. In genetic backgrounds in which embryonic elongation fails, junctional recruitment is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed in lateral (seam) epidermal cells, whereas ZYX-1 is expressed in dorsal and ventral epidermal cells. tes-1 and zyx-1 mutant embryos display junctional F-actin defects. The loss of either protein strongly enhances morphogenetic defects in hypomorphic mutant backgrounds for cadherin/catenin complex (CCC) components. The LCR regions of TES-1 and ZYX-1 are recruited to stress fiber strain sites (SFSSs) in cultured vertebrate cells. Together, these data establish TES-1 and ZYX-1 as components of a multicellular, tension-sensitive system that stabilizes the junctional actin cytoskeleton during embryonic morphogenesis. |
doi_str_mv | 10.1016/j.cub.2022.10.045 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9729467</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2737465023</sourcerecordid><originalsourceid>FETCH-LOGICAL-c399t-79461cc6276f795642713cf21e55291c9d2e2e03eb459dab04f735e5cc2529c33</originalsourceid><addsrcrecordid>eNpVUctu1DAUtRCIDoUPYIO8ZJPUj9geb5DQqDykSiwYJOjGcpybGQ-JHeykMFu-hG_hy_CopYLVfZx7zrnSQeg5JTUlVF4care0NSOMlbkmjXiAVnStdEWaRjxEK6IlqfSasTP0JOcDIZSttXyMzrjk64ZyvUI_t5cfK3qxhYxt6PD1l89luj7-8AFPKc7gZnxYgpt9DHbAtjQBB5i_x_Q14yV0kPAMIRcYd0vyYYdh8mU7lusxpmkfdxAg-4wLcd4D3tS_f8EAOxsyhrFNx_gUPertkOHZXT1Hn95cbjfvqqsPb99vXl9Vjms9V0o3kjonmZK90kI2TFHuekZBCKap0x0DBoRD2wjd2ZY0veIChHOs4I7zc_TqVnda2hE6B2FOdjBT8qNNRxOtN_8jwe_NLt4YrVjxVkXg5Z1Ait8WyLMZfXYwDDZAXLJhiqtGCsJOXvT21KWYc4L-3oYSc8rOHEzJzpyyO61KdoXz4t__7hl_w-J_AEFbmNY</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2737465023</pqid></control><display><type>article</type><title>TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo</title><source>MEDLINE</source><source>Cell Press Free Archives</source><source>Access via ScienceDirect (Elsevier)</source><source>EZB-FREE-00999 freely available EZB journals</source><creator>Lynch, Allison M ; Zhu, Yuyun ; Lucas, Bethany G ; Winkelman, Jonathan D ; Bai, Keliya ; Martin, Sterling C T ; Block, Samuel ; Slabodnick, Mark M ; Audhya, Anjon ; Goldstein, Bob ; Pettitt, Jonathan ; Gardel, Margaret L ; Hardin, Jeff</creator><creatorcontrib>Lynch, Allison M ; Zhu, Yuyun ; Lucas, Bethany G ; Winkelman, Jonathan D ; Bai, Keliya ; Martin, Sterling C T ; Block, Samuel ; Slabodnick, Mark M ; Audhya, Anjon ; Goldstein, Bob ; Pettitt, Jonathan ; Gardel, Margaret L ; Hardin, Jeff</creatorcontrib><description>LIM-domain-containing repeat (LCR) proteins are recruited to strained actin filaments within stress fibers in cultured cells,
but their roles at cell-cell junctions in living organisms have not been extensively studied. Here, we show that the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX-1/Zyxin are recruited to apical junctions during embryonic elongation when junctions are under tension. In genetic backgrounds in which embryonic elongation fails, junctional recruitment is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed in lateral (seam) epidermal cells, whereas ZYX-1 is expressed in dorsal and ventral epidermal cells. tes-1 and zyx-1 mutant embryos display junctional F-actin defects. The loss of either protein strongly enhances morphogenetic defects in hypomorphic mutant backgrounds for cadherin/catenin complex (CCC) components. The LCR regions of TES-1 and ZYX-1 are recruited to stress fiber strain sites (SFSSs) in cultured vertebrate cells. Together, these data establish TES-1 and ZYX-1 as components of a multicellular, tension-sensitive system that stabilizes the junctional actin cytoskeleton during embryonic morphogenesis.</description><identifier>ISSN: 0960-9822</identifier><identifier>ISSN: 1879-0445</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2022.10.045</identifier><identifier>PMID: 36384139</identifier><language>eng</language><publisher>England</publisher><subject>Actins - genetics ; Animals ; Caenorhabditis elegans - genetics</subject><ispartof>Current biology, 2022-12, Vol.32 (23), p.5189-5199.e6</ispartof><rights>Copyright © 2022 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c399t-79461cc6276f795642713cf21e55291c9d2e2e03eb459dab04f735e5cc2529c33</citedby><cites>FETCH-LOGICAL-c399t-79461cc6276f795642713cf21e55291c9d2e2e03eb459dab04f735e5cc2529c33</cites><orcidid>0000-0001-7399-6580</orcidid></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/36384139$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lynch, Allison M</creatorcontrib><creatorcontrib>Zhu, Yuyun</creatorcontrib><creatorcontrib>Lucas, Bethany G</creatorcontrib><creatorcontrib>Winkelman, Jonathan D</creatorcontrib><creatorcontrib>Bai, Keliya</creatorcontrib><creatorcontrib>Martin, Sterling C T</creatorcontrib><creatorcontrib>Block, Samuel</creatorcontrib><creatorcontrib>Slabodnick, Mark M</creatorcontrib><creatorcontrib>Audhya, Anjon</creatorcontrib><creatorcontrib>Goldstein, Bob</creatorcontrib><creatorcontrib>Pettitt, Jonathan</creatorcontrib><creatorcontrib>Gardel, Margaret L</creatorcontrib><creatorcontrib>Hardin, Jeff</creatorcontrib><title>TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>LIM-domain-containing repeat (LCR) proteins are recruited to strained actin filaments within stress fibers in cultured cells,
but their roles at cell-cell junctions in living organisms have not been extensively studied. Here, we show that the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX-1/Zyxin are recruited to apical junctions during embryonic elongation when junctions are under tension. In genetic backgrounds in which embryonic elongation fails, junctional recruitment is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed in lateral (seam) epidermal cells, whereas ZYX-1 is expressed in dorsal and ventral epidermal cells. tes-1 and zyx-1 mutant embryos display junctional F-actin defects. The loss of either protein strongly enhances morphogenetic defects in hypomorphic mutant backgrounds for cadherin/catenin complex (CCC) components. The LCR regions of TES-1 and ZYX-1 are recruited to stress fiber strain sites (SFSSs) in cultured vertebrate cells. Together, these data establish TES-1 and ZYX-1 as components of a multicellular, tension-sensitive system that stabilizes the junctional actin cytoskeleton during embryonic morphogenesis.</description><subject>Actins - genetics</subject><subject>Animals</subject><subject>Caenorhabditis elegans - genetics</subject><issn>0960-9822</issn><issn>1879-0445</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUctu1DAUtRCIDoUPYIO8ZJPUj9geb5DQqDykSiwYJOjGcpybGQ-JHeykMFu-hG_hy_CopYLVfZx7zrnSQeg5JTUlVF4care0NSOMlbkmjXiAVnStdEWaRjxEK6IlqfSasTP0JOcDIZSttXyMzrjk64ZyvUI_t5cfK3qxhYxt6PD1l89luj7-8AFPKc7gZnxYgpt9DHbAtjQBB5i_x_Q14yV0kPAMIRcYd0vyYYdh8mU7lusxpmkfdxAg-4wLcd4D3tS_f8EAOxsyhrFNx_gUPertkOHZXT1Hn95cbjfvqqsPb99vXl9Vjms9V0o3kjonmZK90kI2TFHuekZBCKap0x0DBoRD2wjd2ZY0veIChHOs4I7zc_TqVnda2hE6B2FOdjBT8qNNRxOtN_8jwe_NLt4YrVjxVkXg5Z1Ait8WyLMZfXYwDDZAXLJhiqtGCsJOXvT21KWYc4L-3oYSc8rOHEzJzpyyO61KdoXz4t__7hl_w-J_AEFbmNY</recordid><startdate>20221205</startdate><enddate>20221205</enddate><creator>Lynch, Allison M</creator><creator>Zhu, Yuyun</creator><creator>Lucas, Bethany G</creator><creator>Winkelman, Jonathan D</creator><creator>Bai, Keliya</creator><creator>Martin, Sterling C T</creator><creator>Block, Samuel</creator><creator>Slabodnick, Mark M</creator><creator>Audhya, Anjon</creator><creator>Goldstein, Bob</creator><creator>Pettitt, Jonathan</creator><creator>Gardel, Margaret L</creator><creator>Hardin, Jeff</creator><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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7399-6580</orcidid></search><sort><creationdate>20221205</creationdate><title>TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo</title><author>Lynch, Allison M ; Zhu, Yuyun ; Lucas, Bethany G ; Winkelman, Jonathan D ; Bai, Keliya ; Martin, Sterling C T ; Block, Samuel ; Slabodnick, Mark M ; Audhya, Anjon ; Goldstein, Bob ; Pettitt, Jonathan ; Gardel, Margaret L ; Hardin, Jeff</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c399t-79461cc6276f795642713cf21e55291c9d2e2e03eb459dab04f735e5cc2529c33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Actins - genetics</topic><topic>Animals</topic><topic>Caenorhabditis elegans - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lynch, Allison M</creatorcontrib><creatorcontrib>Zhu, Yuyun</creatorcontrib><creatorcontrib>Lucas, Bethany G</creatorcontrib><creatorcontrib>Winkelman, Jonathan D</creatorcontrib><creatorcontrib>Bai, Keliya</creatorcontrib><creatorcontrib>Martin, Sterling C T</creatorcontrib><creatorcontrib>Block, Samuel</creatorcontrib><creatorcontrib>Slabodnick, Mark M</creatorcontrib><creatorcontrib>Audhya, Anjon</creatorcontrib><creatorcontrib>Goldstein, Bob</creatorcontrib><creatorcontrib>Pettitt, Jonathan</creatorcontrib><creatorcontrib>Gardel, Margaret L</creatorcontrib><creatorcontrib>Hardin, Jeff</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lynch, Allison M</au><au>Zhu, Yuyun</au><au>Lucas, Bethany G</au><au>Winkelman, Jonathan D</au><au>Bai, Keliya</au><au>Martin, Sterling C T</au><au>Block, Samuel</au><au>Slabodnick, Mark M</au><au>Audhya, Anjon</au><au>Goldstein, Bob</au><au>Pettitt, Jonathan</au><au>Gardel, Margaret L</au><au>Hardin, Jeff</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2022-12-05</date><risdate>2022</risdate><volume>32</volume><issue>23</issue><spage>5189</spage><epage>5199.e6</epage><pages>5189-5199.e6</pages><issn>0960-9822</issn><issn>1879-0445</issn><eissn>1879-0445</eissn><abstract>LIM-domain-containing repeat (LCR) proteins are recruited to strained actin filaments within stress fibers in cultured cells,
but their roles at cell-cell junctions in living organisms have not been extensively studied. Here, we show that the Caenorhabditis elegans LCR proteins TES-1/Tes and ZYX-1/Zyxin are recruited to apical junctions during embryonic elongation when junctions are under tension. In genetic backgrounds in which embryonic elongation fails, junctional recruitment is severely compromised. The two proteins display complementary patterns of expression: TES-1 is expressed in lateral (seam) epidermal cells, whereas ZYX-1 is expressed in dorsal and ventral epidermal cells. tes-1 and zyx-1 mutant embryos display junctional F-actin defects. The loss of either protein strongly enhances morphogenetic defects in hypomorphic mutant backgrounds for cadherin/catenin complex (CCC) components. The LCR regions of TES-1 and ZYX-1 are recruited to stress fiber strain sites (SFSSs) in cultured vertebrate cells. Together, these data establish TES-1 and ZYX-1 as components of a multicellular, tension-sensitive system that stabilizes the junctional actin cytoskeleton during embryonic morphogenesis.</abstract><cop>England</cop><pmid>36384139</pmid><doi>10.1016/j.cub.2022.10.045</doi><orcidid>https://orcid.org/0000-0001-7399-6580</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0960-9822 |
ispartof | Current biology, 2022-12, Vol.32 (23), p.5189-5199.e6 |
issn | 0960-9822 1879-0445 1879-0445 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9729467 |
source | MEDLINE; Cell Press Free Archives; Access via ScienceDirect (Elsevier); EZB-FREE-00999 freely available EZB journals |
subjects | Actins - genetics Animals Caenorhabditis elegans - genetics |
title | TES-1/Tes and ZYX-1/Zyxin protect junctional actin networks under tension during epidermal morphogenesis in the C. elegans embryo |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-26T14%3A42%3A22IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=TES-1/Tes%20and%20ZYX-1/Zyxin%20protect%20junctional%20actin%20networks%20under%20tension%20during%20epidermal%20morphogenesis%20in%20the%20C.%C2%A0elegans%20embryo&rft.jtitle=Current%20biology&rft.au=Lynch,%20Allison%20M&rft.date=2022-12-05&rft.volume=32&rft.issue=23&rft.spage=5189&rft.epage=5199.e6&rft.pages=5189-5199.e6&rft.issn=0960-9822&rft.eissn=1879-0445&rft_id=info:doi/10.1016/j.cub.2022.10.045&rft_dat=%3Cproquest_pubme%3E2737465023%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2737465023&rft_id=info:pmid/36384139&rfr_iscdi=true |