Developmentally regulated GTP-binding protein 1 modulates ciliogenesis via an interaction with Dishevelled
Cilia are critical for proper embryonic development and maintaining homeostasis. Although extensively studied, there are still significant gaps regarding the proteins involved in regulating ciliogenesis. Using the embryo, we show that Dishevelled (Dvl), a key Wnt signaling scaffold that is critical...
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| Veröffentlicht in: | The Journal of cell biology 2019-08, Vol.218 (8), p.2659-2676 |
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| container_title | The Journal of cell biology |
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| creator | Lee, Moonsup Hwang, Yoo-Seok Yoon, Jaeho Sun, Jian Harned, Adam Nagashima, Kunio Daar, Ira O |
| description | Cilia are critical for proper embryonic development and maintaining homeostasis. Although extensively studied, there are still significant gaps regarding the proteins involved in regulating ciliogenesis. Using the
embryo, we show that Dishevelled (Dvl), a key Wnt signaling scaffold that is critical to proper ciliogenesis, interacts with Drg1 (developmentally regulated GTP-binding protein 1). The loss of Drg1 or disruption of the interaction with Dvl reduces the length and number of cilia and displays defects in basal body migration and docking to the apical surface of multiciliated cells (MCCs). Moreover, Drg1 morphants display abnormal rotational polarity of basal bodies and a decrease in apical actin and RhoA activity that can be attributed to disruption of the protein complex between Dvl and Daam1, as well as between Daam1 and RhoA. These results support the concept that the Drg1-Dvl interaction regulates apical actin polymerization and stability in MCCs. Thus, Drg1 is a newly identified partner of Dvl in regulating ciliogenesis. |
| doi_str_mv | 10.1083/jcb.201811147 |
| format | Article |
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embryo, we show that Dishevelled (Dvl), a key Wnt signaling scaffold that is critical to proper ciliogenesis, interacts with Drg1 (developmentally regulated GTP-binding protein 1). The loss of Drg1 or disruption of the interaction with Dvl reduces the length and number of cilia and displays defects in basal body migration and docking to the apical surface of multiciliated cells (MCCs). Moreover, Drg1 morphants display abnormal rotational polarity of basal bodies and a decrease in apical actin and RhoA activity that can be attributed to disruption of the protein complex between Dvl and Daam1, as well as between Daam1 and RhoA. These results support the concept that the Drg1-Dvl interaction regulates apical actin polymerization and stability in MCCs. Thus, Drg1 is a newly identified partner of Dvl in regulating ciliogenesis.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.201811147</identifier><identifier>PMID: 31270137</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Actin ; Actins - metabolism ; Adaptor Proteins, Signal Transducing - metabolism ; Animals ; Basal bodies ; Basal Bodies - metabolism ; Cell Line ; Cell Polarity ; Cilia ; Cilia - metabolism ; Dishevelled protein ; Dishevelled Proteins - chemistry ; Dishevelled Proteins - metabolism ; Disruption ; Docking ; Embryo, Nonmammalian - metabolism ; Embryogenesis ; Embryonic growth stage ; Embryos ; GTP-binding protein ; GTP-Binding Proteins - metabolism ; Homeostasis ; Humans ; Organogenesis ; Phenotype ; Polarity ; Polymerization ; Protein Binding ; Protein Domains ; Protein Transport ; Proteins ; RhoA protein ; Wnt protein ; Xenopus laevis - embryology ; Xenopus laevis - metabolism ; Xenopus Proteins - chemistry ; Xenopus Proteins - metabolism</subject><ispartof>The Journal of cell biology, 2019-08, Vol.218 (8), p.2659-2676</ispartof><rights>2019 Lee et al.</rights><rights>Copyright Rockefeller University Press Aug 2019</rights><rights>2019 Lee et al. 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c415t-159ea8baa070273022f3cdec6bab2320eac6c11183568326d572e78b8c4e9bc43</citedby><cites>FETCH-LOGICAL-c415t-159ea8baa070273022f3cdec6bab2320eac6c11183568326d572e78b8c4e9bc43</cites><orcidid>0000-0003-2657-526X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31270137$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lee, Moonsup</creatorcontrib><creatorcontrib>Hwang, Yoo-Seok</creatorcontrib><creatorcontrib>Yoon, Jaeho</creatorcontrib><creatorcontrib>Sun, Jian</creatorcontrib><creatorcontrib>Harned, Adam</creatorcontrib><creatorcontrib>Nagashima, Kunio</creatorcontrib><creatorcontrib>Daar, Ira O</creatorcontrib><title>Developmentally regulated GTP-binding protein 1 modulates ciliogenesis via an interaction with Dishevelled</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Cilia are critical for proper embryonic development and maintaining homeostasis. Although extensively studied, there are still significant gaps regarding the proteins involved in regulating ciliogenesis. Using the
embryo, we show that Dishevelled (Dvl), a key Wnt signaling scaffold that is critical to proper ciliogenesis, interacts with Drg1 (developmentally regulated GTP-binding protein 1). The loss of Drg1 or disruption of the interaction with Dvl reduces the length and number of cilia and displays defects in basal body migration and docking to the apical surface of multiciliated cells (MCCs). Moreover, Drg1 morphants display abnormal rotational polarity of basal bodies and a decrease in apical actin and RhoA activity that can be attributed to disruption of the protein complex between Dvl and Daam1, as well as between Daam1 and RhoA. These results support the concept that the Drg1-Dvl interaction regulates apical actin polymerization and stability in MCCs. Thus, Drg1 is a newly identified partner of Dvl in regulating ciliogenesis.</description><subject>Actin</subject><subject>Actins - metabolism</subject><subject>Adaptor Proteins, Signal Transducing - metabolism</subject><subject>Animals</subject><subject>Basal bodies</subject><subject>Basal Bodies - metabolism</subject><subject>Cell Line</subject><subject>Cell Polarity</subject><subject>Cilia</subject><subject>Cilia - metabolism</subject><subject>Dishevelled protein</subject><subject>Dishevelled Proteins - chemistry</subject><subject>Dishevelled Proteins - metabolism</subject><subject>Disruption</subject><subject>Docking</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryogenesis</subject><subject>Embryonic growth stage</subject><subject>Embryos</subject><subject>GTP-binding protein</subject><subject>GTP-Binding Proteins - metabolism</subject><subject>Homeostasis</subject><subject>Humans</subject><subject>Organogenesis</subject><subject>Phenotype</subject><subject>Polarity</subject><subject>Polymerization</subject><subject>Protein Binding</subject><subject>Protein Domains</subject><subject>Protein Transport</subject><subject>Proteins</subject><subject>RhoA protein</subject><subject>Wnt protein</subject><subject>Xenopus laevis - embryology</subject><subject>Xenopus laevis - metabolism</subject><subject>Xenopus Proteins - chemistry</subject><subject>Xenopus Proteins - metabolism</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUFPGzEQRq2qqKShx16RpV64LIzt9dq5IFVAaSUkOMDZ8noniaNdO9i7Qfz7mkIjWvkwh3n6xk8fIV8ZnDLQ4mzj2lMOTDPGavWBzJisodKsho9kBsBZtZBcHpLPOW8AoFa1-EQOBeMKmFAzsrnEHfZxO2AYbd8_04SrqbcjdvT6_q5qfeh8WNFtiiP6QBkdYvdnn6nzvY8rDJh9pjtvqQ3UhxGTdaOPgT75cU0vfV6_XOixOyIHS9tn_PI25-Thx9X9xc_q5vb618X3m8rVTI4Vkwu0urUWFHAlgPOlcB26prUtFxzQusYVWy1kowVvOqk4Kt1qV-OidbWYk_PX3O3UDti5YpZsb7bJDzY9m2i9-XcT_Nqs4s40JU-VNycnbwEpPk6YRzP47IqDDRinbDiXnDeaSVbQb_-hmzilUPQKpTgHDXJRqOqVcinmnHC5_wwD89KiKS2afYuFP35vsKf_1iZ-A8CKmeM</recordid><startdate>20190805</startdate><enddate>20190805</enddate><creator>Lee, Moonsup</creator><creator>Hwang, Yoo-Seok</creator><creator>Yoon, Jaeho</creator><creator>Sun, Jian</creator><creator>Harned, Adam</creator><creator>Nagashima, Kunio</creator><creator>Daar, Ira O</creator><general>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><orcidid>https://orcid.org/0000-0003-2657-526X</orcidid></search><sort><creationdate>20190805</creationdate><title>Developmentally regulated GTP-binding protein 1 modulates ciliogenesis via an interaction with Dishevelled</title><author>Lee, Moonsup ; Hwang, Yoo-Seok ; Yoon, Jaeho ; Sun, Jian ; Harned, Adam ; Nagashima, Kunio ; Daar, Ira O</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c415t-159ea8baa070273022f3cdec6bab2320eac6c11183568326d572e78b8c4e9bc43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Actin</topic><topic>Actins - metabolism</topic><topic>Adaptor Proteins, Signal Transducing - metabolism</topic><topic>Animals</topic><topic>Basal bodies</topic><topic>Basal Bodies - metabolism</topic><topic>Cell Line</topic><topic>Cell Polarity</topic><topic>Cilia</topic><topic>Cilia - metabolism</topic><topic>Dishevelled protein</topic><topic>Dishevelled Proteins - chemistry</topic><topic>Dishevelled Proteins - metabolism</topic><topic>Disruption</topic><topic>Docking</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Embryogenesis</topic><topic>Embryonic growth stage</topic><topic>Embryos</topic><topic>GTP-binding protein</topic><topic>GTP-Binding Proteins - metabolism</topic><topic>Homeostasis</topic><topic>Humans</topic><topic>Organogenesis</topic><topic>Phenotype</topic><topic>Polarity</topic><topic>Polymerization</topic><topic>Protein Binding</topic><topic>Protein Domains</topic><topic>Protein Transport</topic><topic>Proteins</topic><topic>RhoA protein</topic><topic>Wnt protein</topic><topic>Xenopus laevis - embryology</topic><topic>Xenopus laevis - metabolism</topic><topic>Xenopus Proteins - chemistry</topic><topic>Xenopus Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Moonsup</creatorcontrib><creatorcontrib>Hwang, Yoo-Seok</creatorcontrib><creatorcontrib>Yoon, Jaeho</creatorcontrib><creatorcontrib>Sun, Jian</creatorcontrib><creatorcontrib>Harned, Adam</creatorcontrib><creatorcontrib>Nagashima, Kunio</creatorcontrib><creatorcontrib>Daar, Ira O</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>Lee, Moonsup</au><au>Hwang, Yoo-Seok</au><au>Yoon, Jaeho</au><au>Sun, Jian</au><au>Harned, Adam</au><au>Nagashima, Kunio</au><au>Daar, Ira O</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Developmentally regulated GTP-binding protein 1 modulates ciliogenesis via an interaction with Dishevelled</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2019-08-05</date><risdate>2019</risdate><volume>218</volume><issue>8</issue><spage>2659</spage><epage>2676</epage><pages>2659-2676</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><abstract>Cilia are critical for proper embryonic development and maintaining homeostasis. Although extensively studied, there are still significant gaps regarding the proteins involved in regulating ciliogenesis. Using the
embryo, we show that Dishevelled (Dvl), a key Wnt signaling scaffold that is critical to proper ciliogenesis, interacts with Drg1 (developmentally regulated GTP-binding protein 1). The loss of Drg1 or disruption of the interaction with Dvl reduces the length and number of cilia and displays defects in basal body migration and docking to the apical surface of multiciliated cells (MCCs). Moreover, Drg1 morphants display abnormal rotational polarity of basal bodies and a decrease in apical actin and RhoA activity that can be attributed to disruption of the protein complex between Dvl and Daam1, as well as between Daam1 and RhoA. These results support the concept that the Drg1-Dvl interaction regulates apical actin polymerization and stability in MCCs. Thus, Drg1 is a newly identified partner of Dvl in regulating ciliogenesis.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>31270137</pmid><doi>10.1083/jcb.201811147</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0003-2657-526X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Actin Actins - metabolism Adaptor Proteins, Signal Transducing - metabolism Animals Basal bodies Basal Bodies - metabolism Cell Line Cell Polarity Cilia Cilia - metabolism Dishevelled protein Dishevelled Proteins - chemistry Dishevelled Proteins - metabolism Disruption Docking Embryo, Nonmammalian - metabolism Embryogenesis Embryonic growth stage Embryos GTP-binding protein GTP-Binding Proteins - metabolism Homeostasis Humans Organogenesis Phenotype Polarity Polymerization Protein Binding Protein Domains Protein Transport Proteins RhoA protein Wnt protein Xenopus laevis - embryology Xenopus laevis - metabolism Xenopus Proteins - chemistry Xenopus Proteins - metabolism |
| title | Developmentally regulated GTP-binding protein 1 modulates ciliogenesis via an interaction with Dishevelled |
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