Synergistic action of nectins and cadherins generates the mosaic cellular pattern of the olfactory epithelium
In the olfactory epithelium (OE), olfactory cells (OCs) and supporting cells (SCs), which express different cadherins, are arranged in a characteristic mosaic pattern in which OCs are enclosed by SCs. However, the mechanism underlying this cellular patterning is unclear. Here, we show that the cellu...
Gespeichert in:
| Veröffentlicht in: | The Journal of cell biology 2016-02, Vol.212 (5), p.561-575 |
|---|---|
| Hauptverfasser: | , , , , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 575 |
|---|---|
| container_issue | 5 |
| container_start_page | 561 |
| container_title | The Journal of cell biology |
| container_volume | 212 |
| creator | Katsunuma, Sayaka Honda, Hisao Shinoda, Tomoyasu Ishimoto, Yukitaka Miyata, Takaki Kiyonari, Hiroshi Abe, Takaya Nibu, Ken-Ichi Takai, Yoshimi Togashi, Hideru |
| description | In the olfactory epithelium (OE), olfactory cells (OCs) and supporting cells (SCs), which express different cadherins, are arranged in a characteristic mosaic pattern in which OCs are enclosed by SCs. However, the mechanism underlying this cellular patterning is unclear. Here, we show that the cellular pattern of the OE is established by cellular rearrangements during development. In the OE, OCs express nectin-2 and N-cadherin, and SCs express nectin-2, nectin-3, E-cadherin, and N-cadherin. Heterophilic trans-interaction between nectin-2 on OCs and nectin-3 on SCs preferentially recruits cadherin via α-catenin to heterotypic junctions, and the differential distributions of cadherins between junctions promote cellular intercalations, resulting in the formation of the mosaic pattern. These observations are confirmed by model cell systems, and various cellular patterns are generated by the combinatorial expression of nectins and cadherins. Collectively, the synergistic action of nectins and cadherins generates mosaic pattern, which cannot be achieved by a single mechanism. |
| doi_str_mv | 10.1083/jcb.201509020 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4772500</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1780499153</sourcerecordid><originalsourceid>FETCH-LOGICAL-c558t-ecf311a85b503e70837fb698bddf66426b83af043bca33715ec49ed9bfb3627f3</originalsourceid><addsrcrecordid>eNqNkc2LFDEQxYMo7jh69CoNXrz0WvnqTi6CLH7Bggf1HJJ0ZaaH7s6YpIX5782466CePKWS-tUjrx4hzylcU1D89cG7awZUggYGD8iGSgGtogIekg0Ao62WTF6RJzkfAED0gj8mV6zTTAvJNmT-clow7cZcRt9YX8a4NDE0C9ZyyY1dhsbbYY_pfNthZW3B3JQ9NnPMtg55nKZ1sqk52lIw_Ro_t-MUql5MpwaPY32YxnV-Sh4FO2V8dn9uybf3777efGxvP3_4dPP2tvVSqtKiD5xSq6STwLGvNvvgOq3cMISuE6xzitsAgjtvOe-pRC80DtoFxzvWB74lb-50j6ubcfC4lGQnc0zjbNPJRDuavzvLuDe7-MOIvmcSoAq8uhdI8fuKuZh5zGendsG4ZkN7BUJrKvl_oJ3WiqrqYkte_oMe4pqWuolK9YwKpiSrVHtH-RRzThgu_6Zgzpmbmrm5ZF75F3-avdC_Q-Y_AXB6qZ4</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1772142852</pqid></control><display><type>article</type><title>Synergistic action of nectins and cadherins generates the mosaic cellular pattern of the olfactory epithelium</title><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Alma/SFX Local Collection</source><creator>Katsunuma, Sayaka ; Honda, Hisao ; Shinoda, Tomoyasu ; Ishimoto, Yukitaka ; Miyata, Takaki ; Kiyonari, Hiroshi ; Abe, Takaya ; Nibu, Ken-Ichi ; Takai, Yoshimi ; Togashi, Hideru</creator><creatorcontrib>Katsunuma, Sayaka ; Honda, Hisao ; Shinoda, Tomoyasu ; Ishimoto, Yukitaka ; Miyata, Takaki ; Kiyonari, Hiroshi ; Abe, Takaya ; Nibu, Ken-Ichi ; Takai, Yoshimi ; Togashi, Hideru</creatorcontrib><description>In the olfactory epithelium (OE), olfactory cells (OCs) and supporting cells (SCs), which express different cadherins, are arranged in a characteristic mosaic pattern in which OCs are enclosed by SCs. However, the mechanism underlying this cellular patterning is unclear. Here, we show that the cellular pattern of the OE is established by cellular rearrangements during development. In the OE, OCs express nectin-2 and N-cadherin, and SCs express nectin-2, nectin-3, E-cadherin, and N-cadherin. Heterophilic trans-interaction between nectin-2 on OCs and nectin-3 on SCs preferentially recruits cadherin via α-catenin to heterotypic junctions, and the differential distributions of cadherins between junctions promote cellular intercalations, resulting in the formation of the mosaic pattern. These observations are confirmed by model cell systems, and various cellular patterns are generated by the combinatorial expression of nectins and cadherins. Collectively, the synergistic action of nectins and cadherins generates mosaic pattern, which cannot be achieved by a single mechanism.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.201509020</identifier><identifier>PMID: 26929452</identifier><identifier>CODEN: JCLBA3</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animals ; Cadherins - metabolism ; Cell Adhesion Molecules - metabolism ; Cells ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Molecules ; Nectins ; Olfactory Mucosa - cytology ; Olfactory Mucosa - metabolism ; Protein expression</subject><ispartof>The Journal of cell biology, 2016-02, Vol.212 (5), p.561-575</ispartof><rights>2016 Katsunuma et al.</rights><rights>Copyright Rockefeller University Press Feb 29, 2016</rights><rights>2016 Katsunuma et al. 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c558t-ecf311a85b503e70837fb698bddf66426b83af043bca33715ec49ed9bfb3627f3</citedby><cites>FETCH-LOGICAL-c558t-ecf311a85b503e70837fb698bddf66426b83af043bca33715ec49ed9bfb3627f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26929452$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Katsunuma, Sayaka</creatorcontrib><creatorcontrib>Honda, Hisao</creatorcontrib><creatorcontrib>Shinoda, Tomoyasu</creatorcontrib><creatorcontrib>Ishimoto, Yukitaka</creatorcontrib><creatorcontrib>Miyata, Takaki</creatorcontrib><creatorcontrib>Kiyonari, Hiroshi</creatorcontrib><creatorcontrib>Abe, Takaya</creatorcontrib><creatorcontrib>Nibu, Ken-Ichi</creatorcontrib><creatorcontrib>Takai, Yoshimi</creatorcontrib><creatorcontrib>Togashi, Hideru</creatorcontrib><title>Synergistic action of nectins and cadherins generates the mosaic cellular pattern of the olfactory epithelium</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>In the olfactory epithelium (OE), olfactory cells (OCs) and supporting cells (SCs), which express different cadherins, are arranged in a characteristic mosaic pattern in which OCs are enclosed by SCs. However, the mechanism underlying this cellular patterning is unclear. Here, we show that the cellular pattern of the OE is established by cellular rearrangements during development. In the OE, OCs express nectin-2 and N-cadherin, and SCs express nectin-2, nectin-3, E-cadherin, and N-cadherin. Heterophilic trans-interaction between nectin-2 on OCs and nectin-3 on SCs preferentially recruits cadherin via α-catenin to heterotypic junctions, and the differential distributions of cadherins between junctions promote cellular intercalations, resulting in the formation of the mosaic pattern. These observations are confirmed by model cell systems, and various cellular patterns are generated by the combinatorial expression of nectins and cadherins. Collectively, the synergistic action of nectins and cadherins generates mosaic pattern, which cannot be achieved by a single mechanism.</description><subject>Animals</subject><subject>Cadherins - metabolism</subject><subject>Cell Adhesion Molecules - metabolism</subject><subject>Cells</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Molecules</subject><subject>Nectins</subject><subject>Olfactory Mucosa - cytology</subject><subject>Olfactory Mucosa - metabolism</subject><subject>Protein expression</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc2LFDEQxYMo7jh69CoNXrz0WvnqTi6CLH7Bggf1HJJ0ZaaH7s6YpIX5782466CePKWS-tUjrx4hzylcU1D89cG7awZUggYGD8iGSgGtogIekg0Ao62WTF6RJzkfAED0gj8mV6zTTAvJNmT-clow7cZcRt9YX8a4NDE0C9ZyyY1dhsbbYY_pfNthZW3B3JQ9NnPMtg55nKZ1sqk52lIw_Ro_t-MUql5MpwaPY32YxnV-Sh4FO2V8dn9uybf3777efGxvP3_4dPP2tvVSqtKiD5xSq6STwLGvNvvgOq3cMISuE6xzitsAgjtvOe-pRC80DtoFxzvWB74lb-50j6ubcfC4lGQnc0zjbNPJRDuavzvLuDe7-MOIvmcSoAq8uhdI8fuKuZh5zGendsG4ZkN7BUJrKvl_oJ3WiqrqYkte_oMe4pqWuolK9YwKpiSrVHtH-RRzThgu_6Zgzpmbmrm5ZF75F3-avdC_Q-Y_AXB6qZ4</recordid><startdate>20160229</startdate><enddate>20160229</enddate><creator>Katsunuma, Sayaka</creator><creator>Honda, Hisao</creator><creator>Shinoda, Tomoyasu</creator><creator>Ishimoto, Yukitaka</creator><creator>Miyata, Takaki</creator><creator>Kiyonari, Hiroshi</creator><creator>Abe, Takaya</creator><creator>Nibu, Ken-Ichi</creator><creator>Takai, Yoshimi</creator><creator>Togashi, Hideru</creator><general>Rockefeller University Press</general><general>The Rockefeller University Press</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20160229</creationdate><title>Synergistic action of nectins and cadherins generates the mosaic cellular pattern of the olfactory epithelium</title><author>Katsunuma, Sayaka ; Honda, Hisao ; Shinoda, Tomoyasu ; Ishimoto, Yukitaka ; Miyata, Takaki ; Kiyonari, Hiroshi ; Abe, Takaya ; Nibu, Ken-Ichi ; Takai, Yoshimi ; Togashi, Hideru</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c558t-ecf311a85b503e70837fb698bddf66426b83af043bca33715ec49ed9bfb3627f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Cadherins - metabolism</topic><topic>Cell Adhesion Molecules - metabolism</topic><topic>Cells</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Molecules</topic><topic>Nectins</topic><topic>Olfactory Mucosa - cytology</topic><topic>Olfactory Mucosa - metabolism</topic><topic>Protein expression</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Katsunuma, Sayaka</creatorcontrib><creatorcontrib>Honda, Hisao</creatorcontrib><creatorcontrib>Shinoda, Tomoyasu</creatorcontrib><creatorcontrib>Ishimoto, Yukitaka</creatorcontrib><creatorcontrib>Miyata, Takaki</creatorcontrib><creatorcontrib>Kiyonari, Hiroshi</creatorcontrib><creatorcontrib>Abe, Takaya</creatorcontrib><creatorcontrib>Nibu, Ken-Ichi</creatorcontrib><creatorcontrib>Takai, Yoshimi</creatorcontrib><creatorcontrib>Togashi, Hideru</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Katsunuma, Sayaka</au><au>Honda, Hisao</au><au>Shinoda, Tomoyasu</au><au>Ishimoto, Yukitaka</au><au>Miyata, Takaki</au><au>Kiyonari, Hiroshi</au><au>Abe, Takaya</au><au>Nibu, Ken-Ichi</au><au>Takai, Yoshimi</au><au>Togashi, Hideru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Synergistic action of nectins and cadherins generates the mosaic cellular pattern of the olfactory epithelium</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2016-02-29</date><risdate>2016</risdate><volume>212</volume><issue>5</issue><spage>561</spage><epage>575</epage><pages>561-575</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><coden>JCLBA3</coden><abstract>In the olfactory epithelium (OE), olfactory cells (OCs) and supporting cells (SCs), which express different cadherins, are arranged in a characteristic mosaic pattern in which OCs are enclosed by SCs. However, the mechanism underlying this cellular patterning is unclear. Here, we show that the cellular pattern of the OE is established by cellular rearrangements during development. In the OE, OCs express nectin-2 and N-cadherin, and SCs express nectin-2, nectin-3, E-cadherin, and N-cadherin. Heterophilic trans-interaction between nectin-2 on OCs and nectin-3 on SCs preferentially recruits cadherin via α-catenin to heterotypic junctions, and the differential distributions of cadherins between junctions promote cellular intercalations, resulting in the formation of the mosaic pattern. These observations are confirmed by model cell systems, and various cellular patterns are generated by the combinatorial expression of nectins and cadherins. Collectively, the synergistic action of nectins and cadherins generates mosaic pattern, which cannot be achieved by a single mechanism.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>26929452</pmid><doi>10.1083/jcb.201509020</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0021-9525 |
| ispartof | The Journal of cell biology, 2016-02, Vol.212 (5), p.561-575 |
| issn | 0021-9525 1540-8140 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4772500 |
| source | MEDLINE; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection |
| subjects | Animals Cadherins - metabolism Cell Adhesion Molecules - metabolism Cells Mice Mice, Inbred C57BL Mice, Knockout Molecules Nectins Olfactory Mucosa - cytology Olfactory Mucosa - metabolism Protein expression |
| title | Synergistic action of nectins and cadherins generates the mosaic cellular pattern of the olfactory epithelium |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-09T04%3A16%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=Synergistic%20action%20of%20nectins%20and%20cadherins%20generates%20the%20mosaic%20cellular%20pattern%20of%20the%20olfactory%20epithelium&rft.jtitle=The%20Journal%20of%20cell%20biology&rft.au=Katsunuma,%20Sayaka&rft.date=2016-02-29&rft.volume=212&rft.issue=5&rft.spage=561&rft.epage=575&rft.pages=561-575&rft.issn=0021-9525&rft.eissn=1540-8140&rft.coden=JCLBA3&rft_id=info:doi/10.1083/jcb.201509020&rft_dat=%3Cproquest_pubme%3E1780499153%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=1772142852&rft_id=info:pmid/26929452&rfr_iscdi=true |