Morphogenesis of neurons and glia within an epithelium

To sense the outside world, some neurons protrude across epithelia, the cellular barriers that line every surface of our bodies. To study the morphogenesis of such neurons, we examined the amphid, in which dendrites protrude through a glial channel at the nose. During development, amphid dendrites e...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Development (Cambridge) 2019-02, Vol.146 (4)
Hauptverfasser: Low, Isabel I C, Williams, Claire R, Chong, Megan K, McLachlan, Ian G, Wierbowski, Bradley M, Kolotuev, Irina, Heiman, Maxwell G
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue 4
container_start_page
container_title Development (Cambridge)
container_volume 146
creator Low, Isabel I C
Williams, Claire R
Chong, Megan K
McLachlan, Ian G
Wierbowski, Bradley M
Kolotuev, Irina
Heiman, Maxwell G
description To sense the outside world, some neurons protrude across epithelia, the cellular barriers that line every surface of our bodies. To study the morphogenesis of such neurons, we examined the amphid, in which dendrites protrude through a glial channel at the nose. During development, amphid dendrites extend by attaching to the nose via DYF-7, a type of protein typically found in epithelial apical ECM. Here, we show that amphid neurons and glia exhibit epithelial properties, including tight junctions and apical-basal polarity, and develop in a manner resembling other epithelia. We find that DYF-7 is a fibril-forming apical ECM component that promotes formation of the tube-shaped glial channel, reminiscent of roles for apical ECM in other narrow epithelial tubes. We also identify a requirement for FRM-2, a homolog of EPBL15/moe/Yurt that promotes epithelial integrity in other systems. Finally, we show that other environmentally exposed neurons share a requirement for DYF-7. Together, our results suggest that these neurons and glia can be viewed as part of an epithelium continuous with the skin, and are shaped by mechanisms shared with other epithelia.
doi_str_mv 10.1242/dev.171124
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6398450</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2179423497</sourcerecordid><originalsourceid>FETCH-LOGICAL-c412t-d824e2e112c9791d09c2cb95e6836114b139b5ee5ddfc7f95bc7beffbac5e4ac3</originalsourceid><addsrcrecordid>eNpdkV9LwzAUxYMobk5f_ADSRxWquUnaLC_CGOqEiS_6HNL0dot0zWzWid_ejM2hPt0_-eWchEPIOdAbYILdlri-AQmxPyB9EFKmCpg6JH2qMpqCUtAjJyG8U0p5LuUx6XGaD3me8z7Jn327nPsZNhhcSHyVNNi1vgmJacpkVjuTfLrV3DVxTnAZW6xdtzglR5WpA57t6oC8Pdy_jifp9OXxaTyaplYAW6XlkAlkGJ9mlVRQUmWZLVSGG3sAUQBXRYaYlWVlZaWywsoCq6owNkNhLB-Qu63usisWWFpsVq2p9bJ1C9N-aW-c_nvSuLme-bXOuRqKjEaBq63A_N-1yWiqNzvKgEmQcg2RvdyZtf6jw7DSCxcs1rVp0HdBM5BKMC6UjOj1FrWtD6HFaq8NVG9C0TEUvQ0lwhe_P7FHf1Lg30afiGs</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2179423497</pqid></control><display><type>article</type><title>Morphogenesis of neurons and glia within an epithelium</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>Low, Isabel I C ; Williams, Claire R ; Chong, Megan K ; McLachlan, Ian G ; Wierbowski, Bradley M ; Kolotuev, Irina ; Heiman, Maxwell G</creator><creatorcontrib>Low, Isabel I C ; Williams, Claire R ; Chong, Megan K ; McLachlan, Ian G ; Wierbowski, Bradley M ; Kolotuev, Irina ; Heiman, Maxwell G</creatorcontrib><description>To sense the outside world, some neurons protrude across epithelia, the cellular barriers that line every surface of our bodies. To study the morphogenesis of such neurons, we examined the amphid, in which dendrites protrude through a glial channel at the nose. During development, amphid dendrites extend by attaching to the nose via DYF-7, a type of protein typically found in epithelial apical ECM. Here, we show that amphid neurons and glia exhibit epithelial properties, including tight junctions and apical-basal polarity, and develop in a manner resembling other epithelia. We find that DYF-7 is a fibril-forming apical ECM component that promotes formation of the tube-shaped glial channel, reminiscent of roles for apical ECM in other narrow epithelial tubes. We also identify a requirement for FRM-2, a homolog of EPBL15/moe/Yurt that promotes epithelial integrity in other systems. Finally, we show that other environmentally exposed neurons share a requirement for DYF-7. Together, our results suggest that these neurons and glia can be viewed as part of an epithelium continuous with the skin, and are shaped by mechanisms shared with other epithelia.</description><identifier>ISSN: 0950-1991</identifier><identifier>ISSN: 1477-9129</identifier><identifier>EISSN: 1477-9129</identifier><identifier>DOI: 10.1242/dev.171124</identifier><identifier>PMID: 30683663</identifier><language>eng</language><publisher>England: Company of Biologists</publisher><subject>Animals ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans Proteins - metabolism ; Cytoskeleton - metabolism ; Dendrites - metabolism ; Development Biology ; Drosophila melanogaster - metabolism ; Epithelial Cells - metabolism ; Epithelium - metabolism ; Female ; Life Sciences ; Male ; Membrane Proteins - metabolism ; Morphogenesis ; Mutation ; Neurobiology ; Neuroglia - metabolism ; Neurons - metabolism ; Neurons and Cognition ; Tight Junctions - metabolism</subject><ispartof>Development (Cambridge), 2019-02, Vol.146 (4)</ispartof><rights>2019. Published by The Company of Biologists Ltd.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2019. Published by The Company of Biologists Ltd 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-d824e2e112c9791d09c2cb95e6836114b139b5ee5ddfc7f95bc7beffbac5e4ac3</citedby><cites>FETCH-LOGICAL-c412t-d824e2e112c9791d09c2cb95e6836114b139b5ee5ddfc7f95bc7beffbac5e4ac3</cites><orcidid>0000-0001-5467-149X ; 0000-0002-4271-4365 ; 0000-0003-1433-8048 ; 0000-0002-2557-6490 ; 0000-0002-1967-5919</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,3678,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30683663$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://univ-rennes.hal.science/hal-02127177$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Low, Isabel I C</creatorcontrib><creatorcontrib>Williams, Claire R</creatorcontrib><creatorcontrib>Chong, Megan K</creatorcontrib><creatorcontrib>McLachlan, Ian G</creatorcontrib><creatorcontrib>Wierbowski, Bradley M</creatorcontrib><creatorcontrib>Kolotuev, Irina</creatorcontrib><creatorcontrib>Heiman, Maxwell G</creatorcontrib><title>Morphogenesis of neurons and glia within an epithelium</title><title>Development (Cambridge)</title><addtitle>Development</addtitle><description>To sense the outside world, some neurons protrude across epithelia, the cellular barriers that line every surface of our bodies. To study the morphogenesis of such neurons, we examined the amphid, in which dendrites protrude through a glial channel at the nose. During development, amphid dendrites extend by attaching to the nose via DYF-7, a type of protein typically found in epithelial apical ECM. Here, we show that amphid neurons and glia exhibit epithelial properties, including tight junctions and apical-basal polarity, and develop in a manner resembling other epithelia. We find that DYF-7 is a fibril-forming apical ECM component that promotes formation of the tube-shaped glial channel, reminiscent of roles for apical ECM in other narrow epithelial tubes. We also identify a requirement for FRM-2, a homolog of EPBL15/moe/Yurt that promotes epithelial integrity in other systems. Finally, we show that other environmentally exposed neurons share a requirement for DYF-7. Together, our results suggest that these neurons and glia can be viewed as part of an epithelium continuous with the skin, and are shaped by mechanisms shared with other epithelia.</description><subject>Animals</subject><subject>Caenorhabditis elegans - metabolism</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Cytoskeleton - metabolism</subject><subject>Dendrites - metabolism</subject><subject>Development Biology</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Epithelial Cells - metabolism</subject><subject>Epithelium - metabolism</subject><subject>Female</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Membrane Proteins - metabolism</subject><subject>Morphogenesis</subject><subject>Mutation</subject><subject>Neurobiology</subject><subject>Neuroglia - metabolism</subject><subject>Neurons - metabolism</subject><subject>Neurons and Cognition</subject><subject>Tight Junctions - metabolism</subject><issn>0950-1991</issn><issn>1477-9129</issn><issn>1477-9129</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkV9LwzAUxYMobk5f_ADSRxWquUnaLC_CGOqEiS_6HNL0dot0zWzWid_ejM2hPt0_-eWchEPIOdAbYILdlri-AQmxPyB9EFKmCpg6JH2qMpqCUtAjJyG8U0p5LuUx6XGaD3me8z7Jn327nPsZNhhcSHyVNNi1vgmJacpkVjuTfLrV3DVxTnAZW6xdtzglR5WpA57t6oC8Pdy_jifp9OXxaTyaplYAW6XlkAlkGJ9mlVRQUmWZLVSGG3sAUQBXRYaYlWVlZaWywsoCq6owNkNhLB-Qu63usisWWFpsVq2p9bJ1C9N-aW-c_nvSuLme-bXOuRqKjEaBq63A_N-1yWiqNzvKgEmQcg2RvdyZtf6jw7DSCxcs1rVp0HdBM5BKMC6UjOj1FrWtD6HFaq8NVG9C0TEUvQ0lwhe_P7FHf1Lg30afiGs</recordid><startdate>20190220</startdate><enddate>20190220</enddate><creator>Low, Isabel I C</creator><creator>Williams, Claire R</creator><creator>Chong, Megan K</creator><creator>McLachlan, Ian G</creator><creator>Wierbowski, Bradley M</creator><creator>Kolotuev, Irina</creator><creator>Heiman, Maxwell G</creator><general>Company of Biologists</general><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>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5467-149X</orcidid><orcidid>https://orcid.org/0000-0002-4271-4365</orcidid><orcidid>https://orcid.org/0000-0003-1433-8048</orcidid><orcidid>https://orcid.org/0000-0002-2557-6490</orcidid><orcidid>https://orcid.org/0000-0002-1967-5919</orcidid></search><sort><creationdate>20190220</creationdate><title>Morphogenesis of neurons and glia within an epithelium</title><author>Low, Isabel I C ; Williams, Claire R ; Chong, Megan K ; McLachlan, Ian G ; Wierbowski, Bradley M ; Kolotuev, Irina ; Heiman, Maxwell G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-d824e2e112c9791d09c2cb95e6836114b139b5ee5ddfc7f95bc7beffbac5e4ac3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Caenorhabditis elegans - metabolism</topic><topic>Caenorhabditis elegans Proteins - metabolism</topic><topic>Cytoskeleton - metabolism</topic><topic>Dendrites - metabolism</topic><topic>Development Biology</topic><topic>Drosophila melanogaster - metabolism</topic><topic>Epithelial Cells - metabolism</topic><topic>Epithelium - metabolism</topic><topic>Female</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Membrane Proteins - metabolism</topic><topic>Morphogenesis</topic><topic>Mutation</topic><topic>Neurobiology</topic><topic>Neuroglia - metabolism</topic><topic>Neurons - metabolism</topic><topic>Neurons and Cognition</topic><topic>Tight Junctions - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Low, Isabel I C</creatorcontrib><creatorcontrib>Williams, Claire R</creatorcontrib><creatorcontrib>Chong, Megan K</creatorcontrib><creatorcontrib>McLachlan, Ian G</creatorcontrib><creatorcontrib>Wierbowski, Bradley M</creatorcontrib><creatorcontrib>Kolotuev, Irina</creatorcontrib><creatorcontrib>Heiman, Maxwell G</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>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</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>Low, Isabel I C</au><au>Williams, Claire R</au><au>Chong, Megan K</au><au>McLachlan, Ian G</au><au>Wierbowski, Bradley M</au><au>Kolotuev, Irina</au><au>Heiman, Maxwell G</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Morphogenesis of neurons and glia within an epithelium</atitle><jtitle>Development (Cambridge)</jtitle><addtitle>Development</addtitle><date>2019-02-20</date><risdate>2019</risdate><volume>146</volume><issue>4</issue><issn>0950-1991</issn><issn>1477-9129</issn><eissn>1477-9129</eissn><abstract>To sense the outside world, some neurons protrude across epithelia, the cellular barriers that line every surface of our bodies. To study the morphogenesis of such neurons, we examined the amphid, in which dendrites protrude through a glial channel at the nose. During development, amphid dendrites extend by attaching to the nose via DYF-7, a type of protein typically found in epithelial apical ECM. Here, we show that amphid neurons and glia exhibit epithelial properties, including tight junctions and apical-basal polarity, and develop in a manner resembling other epithelia. We find that DYF-7 is a fibril-forming apical ECM component that promotes formation of the tube-shaped glial channel, reminiscent of roles for apical ECM in other narrow epithelial tubes. We also identify a requirement for FRM-2, a homolog of EPBL15/moe/Yurt that promotes epithelial integrity in other systems. Finally, we show that other environmentally exposed neurons share a requirement for DYF-7. Together, our results suggest that these neurons and glia can be viewed as part of an epithelium continuous with the skin, and are shaped by mechanisms shared with other epithelia.</abstract><cop>England</cop><pub>Company of Biologists</pub><pmid>30683663</pmid><doi>10.1242/dev.171124</doi><orcidid>https://orcid.org/0000-0001-5467-149X</orcidid><orcidid>https://orcid.org/0000-0002-4271-4365</orcidid><orcidid>https://orcid.org/0000-0003-1433-8048</orcidid><orcidid>https://orcid.org/0000-0002-2557-6490</orcidid><orcidid>https://orcid.org/0000-0002-1967-5919</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0950-1991
ispartof Development (Cambridge), 2019-02, Vol.146 (4)
issn 0950-1991
1477-9129
1477-9129
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6398450
source MEDLINE; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection; Company of Biologists
subjects Animals
Caenorhabditis elegans - metabolism
Caenorhabditis elegans Proteins - metabolism
Cytoskeleton - metabolism
Dendrites - metabolism
Development Biology
Drosophila melanogaster - metabolism
Epithelial Cells - metabolism
Epithelium - metabolism
Female
Life Sciences
Male
Membrane Proteins - metabolism
Morphogenesis
Mutation
Neurobiology
Neuroglia - metabolism
Neurons - metabolism
Neurons and Cognition
Tight Junctions - metabolism
title Morphogenesis of neurons and glia within an epithelium
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-28T02%3A50%3A56IST&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=Morphogenesis%20of%20neurons%20and%20glia%20within%20an%20epithelium&rft.jtitle=Development%20(Cambridge)&rft.au=Low,%20Isabel%20I%20C&rft.date=2019-02-20&rft.volume=146&rft.issue=4&rft.issn=0950-1991&rft.eissn=1477-9129&rft_id=info:doi/10.1242/dev.171124&rft_dat=%3Cproquest_pubme%3E2179423497%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=2179423497&rft_id=info:pmid/30683663&rfr_iscdi=true