Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis

During Caenorhabditis elegans vulval development, the uterine anchor cell (AC) first secretes an epidermal growth factor (EGF) to specify the vulval cell fates and then invades the underlying vulval epithelium. By doing so, the AC establishes direct contact with the invaginating primary vulF cells a...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Development (Cambridge) 2022-01, Vol.149 (1)
Hauptverfasser: Spiri, Silvan, Berger, Simon, Mereu, Louisa, DeMello, Andrew, Hajnal, Alex
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue 1
container_start_page
container_title Development (Cambridge)
container_volume 149
creator Spiri, Silvan
Berger, Simon
Mereu, Louisa
DeMello, Andrew
Hajnal, Alex
description During Caenorhabditis elegans vulval development, the uterine anchor cell (AC) first secretes an epidermal growth factor (EGF) to specify the vulval cell fates and then invades the underlying vulval epithelium. By doing so, the AC establishes direct contact with the invaginating primary vulF cells and attaches the developing uterus to the vulva. The signals involved and the exact sequence of events joining these two organs are not fully understood. Using a conditional let-23 EGF receptor (EGFR) allele along with novel microfluidic short- and long-term imaging methods, we discovered a specific function of the EGFR in the AC during vulval lumen morphogenesis. Tissue-specific inactivation of let-23 in the AC resulted in imprecise alignment of the AC with the primary vulval cells, delayed AC invasion and disorganized adherens junctions at the contact site forming between the AC and the dorsal vulF toroid. We propose that EGFR signaling, activated by a reciprocal EGF cue from the primary vulval cells, positions the AC at the vulval midline, guides it during invasion and assembles a cytoskeletal scaffold organizing the adherens junctions that connect the developing uterus to the dorsal vulF toroid. Thus, EGFR signaling in the AC ensures the precise alignment of the two developing organs.
doi_str_mv 10.1242/dev.199900
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8783044</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2616956115</sourcerecordid><originalsourceid>FETCH-LOGICAL-c378t-694e9c1d30fbd1cd4139f037eae3c88ed672cb03e051c3fb88c4dcb90f370c7d3</originalsourceid><addsrcrecordid>eNpVkUFr3DAQhUVoSbZpL_0BRcdScCpZXku6FMqSpIVAILRnIY_GtopXciV7IX8gv7taNg3taQ7vm_eGeYS85-yK10392eHhimutGTsjG95IWWle61dkw_SWVUXhF-RNzr8YY6KV8pxciEarWnGxIU8PCH5OEexEr29vHmj2Q7CTDwP1gS4jUhtgjIkCThPFkNeEmc6pbGUsyIKpimmwgUIMAWHxMVC3pqPBzmKIabSd84vPFCcsXKaHdTqUtH1M8xgHDJh9fkte93bK-O55XpKfN9c_dt-qu_vb77uvdxUIqZaq1Q1q4E6wvnMcXMOF7pmQaFGAUuhaWUPHBLItB9F3SkHjoNOsF5KBdOKSfDn5zmu3RwcYlmQnMye_t-nRROvN_0rwoxniwSipBGuaYvDx2SDF3yvmxex9Pv7GBoxrNnXLW71tOd8W9NMJhRRzTti_xHBmjsWZUpw5FVfgD_8e9oL-bUr8AVNEmPI</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2616956115</pqid></control><display><type>article</type><title>Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis</title><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Alma/SFX Local Collection</source><source>Company of Biologists</source><creator>Spiri, Silvan ; Berger, Simon ; Mereu, Louisa ; DeMello, Andrew ; Hajnal, Alex</creator><creatorcontrib>Spiri, Silvan ; Berger, Simon ; Mereu, Louisa ; DeMello, Andrew ; Hajnal, Alex</creatorcontrib><description>During Caenorhabditis elegans vulval development, the uterine anchor cell (AC) first secretes an epidermal growth factor (EGF) to specify the vulval cell fates and then invades the underlying vulval epithelium. By doing so, the AC establishes direct contact with the invaginating primary vulF cells and attaches the developing uterus to the vulva. The signals involved and the exact sequence of events joining these two organs are not fully understood. Using a conditional let-23 EGF receptor (EGFR) allele along with novel microfluidic short- and long-term imaging methods, we discovered a specific function of the EGFR in the AC during vulval lumen morphogenesis. Tissue-specific inactivation of let-23 in the AC resulted in imprecise alignment of the AC with the primary vulval cells, delayed AC invasion and disorganized adherens junctions at the contact site forming between the AC and the dorsal vulF toroid. We propose that EGFR signaling, activated by a reciprocal EGF cue from the primary vulval cells, positions the AC at the vulval midline, guides it during invasion and assembles a cytoskeletal scaffold organizing the adherens junctions that connect the developing uterus to the dorsal vulF toroid. Thus, EGFR signaling in the AC ensures the precise alignment of the two developing organs.</description><identifier>ISSN: 0950-1991</identifier><identifier>ISSN: 1477-9129</identifier><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.199900</identifier><identifier>PMID: 34982813</identifier><language>eng</language><publisher>England: The Company of Biologists Ltd</publisher><subject>Adherens Junctions - metabolism ; Animals ; Caenorhabditis elegans ; Cytoskeleton - metabolism ; Epidermal Growth Factor - metabolism ; ErbB Receptors - metabolism ; Female ; Morphogenesis ; Signal Transduction ; Vulva - cytology ; Vulva - growth &amp; development ; Vulva - metabolism</subject><ispartof>Development (Cambridge), 2022-01, Vol.149 (1)</ispartof><rights>2022. Published by The Company of Biologists Ltd.</rights><rights>2022. Published by The Company of Biologists Ltd 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c378t-694e9c1d30fbd1cd4139f037eae3c88ed672cb03e051c3fb88c4dcb90f370c7d3</citedby><cites>FETCH-LOGICAL-c378t-694e9c1d30fbd1cd4139f037eae3c88ed672cb03e051c3fb88c4dcb90f370c7d3</cites><orcidid>0000-0003-1333-4029 ; 0000-0002-7124-3056 ; 0000-0003-1943-1356 ; 0000-0002-4098-3721</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,3676,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34982813$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Spiri, Silvan</creatorcontrib><creatorcontrib>Berger, Simon</creatorcontrib><creatorcontrib>Mereu, Louisa</creatorcontrib><creatorcontrib>DeMello, Andrew</creatorcontrib><creatorcontrib>Hajnal, Alex</creatorcontrib><title>Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis</title><title>Development (Cambridge)</title><addtitle>Development</addtitle><description>During Caenorhabditis elegans vulval development, the uterine anchor cell (AC) first secretes an epidermal growth factor (EGF) to specify the vulval cell fates and then invades the underlying vulval epithelium. By doing so, the AC establishes direct contact with the invaginating primary vulF cells and attaches the developing uterus to the vulva. The signals involved and the exact sequence of events joining these two organs are not fully understood. Using a conditional let-23 EGF receptor (EGFR) allele along with novel microfluidic short- and long-term imaging methods, we discovered a specific function of the EGFR in the AC during vulval lumen morphogenesis. Tissue-specific inactivation of let-23 in the AC resulted in imprecise alignment of the AC with the primary vulval cells, delayed AC invasion and disorganized adherens junctions at the contact site forming between the AC and the dorsal vulF toroid. We propose that EGFR signaling, activated by a reciprocal EGF cue from the primary vulval cells, positions the AC at the vulval midline, guides it during invasion and assembles a cytoskeletal scaffold organizing the adherens junctions that connect the developing uterus to the dorsal vulF toroid. Thus, EGFR signaling in the AC ensures the precise alignment of the two developing organs.</description><subject>Adherens Junctions - metabolism</subject><subject>Animals</subject><subject>Caenorhabditis elegans</subject><subject>Cytoskeleton - metabolism</subject><subject>Epidermal Growth Factor - metabolism</subject><subject>ErbB Receptors - metabolism</subject><subject>Female</subject><subject>Morphogenesis</subject><subject>Signal Transduction</subject><subject>Vulva - cytology</subject><subject>Vulva - growth &amp; development</subject><subject>Vulva - metabolism</subject><issn>0950-1991</issn><issn>1477-9129</issn><issn>1477-9129</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUFr3DAQhUVoSbZpL_0BRcdScCpZXku6FMqSpIVAILRnIY_GtopXciV7IX8gv7taNg3taQ7vm_eGeYS85-yK10392eHhimutGTsjG95IWWle61dkw_SWVUXhF-RNzr8YY6KV8pxciEarWnGxIU8PCH5OEexEr29vHmj2Q7CTDwP1gS4jUhtgjIkCThPFkNeEmc6pbGUsyIKpimmwgUIMAWHxMVC3pqPBzmKIabSd84vPFCcsXKaHdTqUtH1M8xgHDJh9fkte93bK-O55XpKfN9c_dt-qu_vb77uvdxUIqZaq1Q1q4E6wvnMcXMOF7pmQaFGAUuhaWUPHBLItB9F3SkHjoNOsF5KBdOKSfDn5zmu3RwcYlmQnMye_t-nRROvN_0rwoxniwSipBGuaYvDx2SDF3yvmxex9Pv7GBoxrNnXLW71tOd8W9NMJhRRzTti_xHBmjsWZUpw5FVfgD_8e9oL-bUr8AVNEmPI</recordid><startdate>20220101</startdate><enddate>20220101</enddate><creator>Spiri, Silvan</creator><creator>Berger, Simon</creator><creator>Mereu, Louisa</creator><creator>DeMello, Andrew</creator><creator>Hajnal, Alex</creator><general>The Company of Biologists 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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1333-4029</orcidid><orcidid>https://orcid.org/0000-0002-7124-3056</orcidid><orcidid>https://orcid.org/0000-0003-1943-1356</orcidid><orcidid>https://orcid.org/0000-0002-4098-3721</orcidid></search><sort><creationdate>20220101</creationdate><title>Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis</title><author>Spiri, Silvan ; Berger, Simon ; Mereu, Louisa ; DeMello, Andrew ; Hajnal, Alex</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c378t-694e9c1d30fbd1cd4139f037eae3c88ed672cb03e051c3fb88c4dcb90f370c7d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adherens Junctions - metabolism</topic><topic>Animals</topic><topic>Caenorhabditis elegans</topic><topic>Cytoskeleton - metabolism</topic><topic>Epidermal Growth Factor - metabolism</topic><topic>ErbB Receptors - metabolism</topic><topic>Female</topic><topic>Morphogenesis</topic><topic>Signal Transduction</topic><topic>Vulva - cytology</topic><topic>Vulva - growth &amp; development</topic><topic>Vulva - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Spiri, Silvan</creatorcontrib><creatorcontrib>Berger, Simon</creatorcontrib><creatorcontrib>Mereu, Louisa</creatorcontrib><creatorcontrib>DeMello, Andrew</creatorcontrib><creatorcontrib>Hajnal, Alex</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>Development (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Spiri, Silvan</au><au>Berger, Simon</au><au>Mereu, Louisa</au><au>DeMello, Andrew</au><au>Hajnal, Alex</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2022-01-01</date><risdate>2022</risdate><volume>149</volume><issue>1</issue><issn>0950-1991</issn><issn>1477-9129</issn><eissn>1477-9129</eissn><abstract>During Caenorhabditis elegans vulval development, the uterine anchor cell (AC) first secretes an epidermal growth factor (EGF) to specify the vulval cell fates and then invades the underlying vulval epithelium. By doing so, the AC establishes direct contact with the invaginating primary vulF cells and attaches the developing uterus to the vulva. The signals involved and the exact sequence of events joining these two organs are not fully understood. Using a conditional let-23 EGF receptor (EGFR) allele along with novel microfluidic short- and long-term imaging methods, we discovered a specific function of the EGFR in the AC during vulval lumen morphogenesis. Tissue-specific inactivation of let-23 in the AC resulted in imprecise alignment of the AC with the primary vulval cells, delayed AC invasion and disorganized adherens junctions at the contact site forming between the AC and the dorsal vulF toroid. We propose that EGFR signaling, activated by a reciprocal EGF cue from the primary vulval cells, positions the AC at the vulval midline, guides it during invasion and assembles a cytoskeletal scaffold organizing the adherens junctions that connect the developing uterus to the dorsal vulF toroid. Thus, EGFR signaling in the AC ensures the precise alignment of the two developing organs.</abstract><cop>England</cop><pub>The Company of Biologists Ltd</pub><pmid>34982813</pmid><doi>10.1242/dev.199900</doi><orcidid>https://orcid.org/0000-0003-1333-4029</orcidid><orcidid>https://orcid.org/0000-0002-7124-3056</orcidid><orcidid>https://orcid.org/0000-0003-1943-1356</orcidid><orcidid>https://orcid.org/0000-0002-4098-3721</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0950-1991
ispartof Development (Cambridge), 2022-01, Vol.149 (1)
issn 0950-1991
1477-9129
1477-9129
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8783044
source MEDLINE; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection; Company of Biologists
subjects Adherens Junctions - metabolism
Animals
Caenorhabditis elegans
Cytoskeleton - metabolism
Epidermal Growth Factor - metabolism
ErbB Receptors - metabolism
Female
Morphogenesis
Signal Transduction
Vulva - cytology
Vulva - growth & development
Vulva - metabolism
title Reciprocal EGFR signaling in the anchor cell ensures precise inter-organ connection during Caenorhabditis elegans vulval morphogenesis
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-10T15%3A42%3A46IST&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=Reciprocal%20EGFR%20signaling%20in%20the%20anchor%20cell%20ensures%20precise%20inter-organ%20connection%20during%20Caenorhabditis%20elegans%20vulval%20morphogenesis&rft.jtitle=Development%20(Cambridge)&rft.au=Spiri,%20Silvan&rft.date=2022-01-01&rft.volume=149&rft.issue=1&rft.issn=0950-1991&rft.eissn=1477-9129&rft_id=info:doi/10.1242/dev.199900&rft_dat=%3Cproquest_pubme%3E2616956115%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=2616956115&rft_id=info:pmid/34982813&rfr_iscdi=true