Developmental regulation of apical endocytosis controls epithelial patterning in vertebrate tubular organs
Epithelial organs develop through tightly coordinated events of cell proliferation and differentiation in which endocytosis plays a major role. Despite recent advances, how endocytosis regulates the development of vertebrate organs is still unknown. Here we describe a mechanism that facilitates the...
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| Veröffentlicht in: | Nature cell biology 2015-03, Vol.17 (3), p.241-250 |
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| creator | Rodríguez-Fraticelli, Alejo E. Bagwell, Jennifer Bosch-Fortea, Minerva Boncompain, Gaelle Reglero-Real, Natalia García-León, Maria J. Andrés, Germán Toribio, Maria L. Alonso, Miguel A. Millán, Jaime Perez, Franck Bagnat, Michel Martín-Belmonte, Fernando |
| description | Epithelial organs develop through tightly coordinated events of cell proliferation and differentiation in which endocytosis plays a major role. Despite recent advances, how endocytosis regulates the development of vertebrate organs is still unknown. Here we describe a mechanism that facilitates the apical availability of endosomal SNARE receptors for epithelial morphogenesis through the developmental upregulation of
plasmolipin
(
pllp
) in a highly endocytic segment of the zebrafish posterior midgut. The protein PLLP (Pllp in fish) recruits the clathrin adaptor EpsinR to sort the SNARE machinery of the endolysosomal pathway into the subapical compartment, which is a switch for polarized endocytosis. Furthermore, PLLP expression induces apical Crumbs internalization and the activation of the Notch signalling pathway, both crucial steps in the acquisition of cell polarity and differentiation of epithelial cells. We thus postulate that differential apical endosomal SNARE sorting is a mechanism that regulates epithelial patterning.
Bagnat, Martín-Belmonte and colleagues reveal that plasmolipin (PLLP) is upregulated in the zebrafish midgut during development and controls epithelial patterning by promoting polarized endocytosis. |
| doi_str_mv | 10.1038/ncb3106 |
| format | Article |
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plasmolipin
(
pllp
) in a highly endocytic segment of the zebrafish posterior midgut. The protein PLLP (Pllp in fish) recruits the clathrin adaptor EpsinR to sort the SNARE machinery of the endolysosomal pathway into the subapical compartment, which is a switch for polarized endocytosis. Furthermore, PLLP expression induces apical Crumbs internalization and the activation of the Notch signalling pathway, both crucial steps in the acquisition of cell polarity and differentiation of epithelial cells. We thus postulate that differential apical endosomal SNARE sorting is a mechanism that regulates epithelial patterning.
Bagnat, Martín-Belmonte and colleagues reveal that plasmolipin (PLLP) is upregulated in the zebrafish midgut during development and controls epithelial patterning by promoting polarized endocytosis.</description><identifier>ISSN: 1465-7392</identifier><identifier>EISSN: 1476-4679</identifier><identifier>DOI: 10.1038/ncb3106</identifier><identifier>PMID: 25706235</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/1 ; 13/109 ; 13/89 ; 13/95 ; 14/19 ; 14/28 ; 14/34 ; 14/69 ; 38 ; 38/39 ; 38/77 ; 38/88 ; 42 ; 45 ; 59 ; 631/136 ; 631/80/313/1461 ; 631/80/313/2104 ; 631/80/85/2361 ; 64/116 ; 64/60 ; 82/51 ; 96 ; 96/106 ; Adaptor Proteins, Vesicular Transport - genetics ; Adaptor Proteins, Vesicular Transport - metabolism ; Animals ; Artificial chromosomes ; Biology ; Cancer Research ; Cell Biology ; Cell Differentiation ; Cell Line ; Cell Polarity ; Cell Proliferation ; Cell research ; Cellular proteins ; Danio rerio ; Developmental Biology ; Embryo, Nonmammalian ; Endocytosis ; Endosomes - metabolism ; Endosomes - ultrastructure ; Epithelial Cells - metabolism ; Epithelial Cells - ultrastructure ; Epithelium - metabolism ; Epithelium - ultrastructure ; Gene Expression Regulation, Developmental ; Genes ; Kidney Tubules - metabolism ; Kidney Tubules - ultrastructure ; Life Sciences ; Lysosomes - metabolism ; Lysosomes - ultrastructure ; Mice ; Microscopy ; Morphogenesis ; Myelin and Lymphocyte-Associated Proteolipid Proteins - genetics ; Myelin and Lymphocyte-Associated Proteolipid Proteins - metabolism ; Nerve Tissue Proteins - genetics ; Nerve Tissue Proteins - metabolism ; Properties ; Proteins ; Receptors, Notch - genetics ; Receptors, Notch - metabolism ; Signal Transduction ; SNARE Proteins - genetics ; SNARE Proteins - metabolism ; Stem Cells ; Vertebrates ; Zebrafish</subject><ispartof>Nature cell biology, 2015-03, Vol.17 (3), p.241-250</ispartof><rights>Springer Nature Limited 2014</rights><rights>COPYRIGHT 2015 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Mar 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c630t-307bf1c419e7aea405db70a5c2053259e40cdb852637220f784152c1f1ffddbf3</citedby><cites>FETCH-LOGICAL-c630t-307bf1c419e7aea405db70a5c2053259e40cdb852637220f784152c1f1ffddbf3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,782,786,887,27931,27932</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25706235$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rodríguez-Fraticelli, Alejo E.</creatorcontrib><creatorcontrib>Bagwell, Jennifer</creatorcontrib><creatorcontrib>Bosch-Fortea, Minerva</creatorcontrib><creatorcontrib>Boncompain, Gaelle</creatorcontrib><creatorcontrib>Reglero-Real, Natalia</creatorcontrib><creatorcontrib>García-León, Maria J.</creatorcontrib><creatorcontrib>Andrés, Germán</creatorcontrib><creatorcontrib>Toribio, Maria L.</creatorcontrib><creatorcontrib>Alonso, Miguel A.</creatorcontrib><creatorcontrib>Millán, Jaime</creatorcontrib><creatorcontrib>Perez, Franck</creatorcontrib><creatorcontrib>Bagnat, Michel</creatorcontrib><creatorcontrib>Martín-Belmonte, Fernando</creatorcontrib><title>Developmental regulation of apical endocytosis controls epithelial patterning in vertebrate tubular organs</title><title>Nature cell biology</title><addtitle>Nat Cell Biol</addtitle><addtitle>Nat Cell Biol</addtitle><description>Epithelial organs develop through tightly coordinated events of cell proliferation and differentiation in which endocytosis plays a major role. Despite recent advances, how endocytosis regulates the development of vertebrate organs is still unknown. Here we describe a mechanism that facilitates the apical availability of endosomal SNARE receptors for epithelial morphogenesis through the developmental upregulation of
plasmolipin
(
pllp
) in a highly endocytic segment of the zebrafish posterior midgut. The protein PLLP (Pllp in fish) recruits the clathrin adaptor EpsinR to sort the SNARE machinery of the endolysosomal pathway into the subapical compartment, which is a switch for polarized endocytosis. Furthermore, PLLP expression induces apical Crumbs internalization and the activation of the Notch signalling pathway, both crucial steps in the acquisition of cell polarity and differentiation of epithelial cells. We thus postulate that differential apical endosomal SNARE sorting is a mechanism that regulates epithelial patterning.
Bagnat, Martín-Belmonte and colleagues reveal that plasmolipin (PLLP) is upregulated in the zebrafish midgut during development and controls epithelial patterning by promoting polarized endocytosis.</description><subject>13/1</subject><subject>13/109</subject><subject>13/89</subject><subject>13/95</subject><subject>14/19</subject><subject>14/28</subject><subject>14/34</subject><subject>14/69</subject><subject>38</subject><subject>38/39</subject><subject>38/77</subject><subject>38/88</subject><subject>42</subject><subject>45</subject><subject>59</subject><subject>631/136</subject><subject>631/80/313/1461</subject><subject>631/80/313/2104</subject><subject>631/80/85/2361</subject><subject>64/116</subject><subject>64/60</subject><subject>82/51</subject><subject>96</subject><subject>96/106</subject><subject>Adaptor Proteins, Vesicular Transport - genetics</subject><subject>Adaptor Proteins, Vesicular Transport - metabolism</subject><subject>Animals</subject><subject>Artificial chromosomes</subject><subject>Biology</subject><subject>Cancer Research</subject><subject>Cell Biology</subject><subject>Cell Differentiation</subject><subject>Cell Line</subject><subject>Cell Polarity</subject><subject>Cell Proliferation</subject><subject>Cell research</subject><subject>Cellular proteins</subject><subject>Danio rerio</subject><subject>Developmental Biology</subject><subject>Embryo, Nonmammalian</subject><subject>Endocytosis</subject><subject>Endosomes - metabolism</subject><subject>Endosomes - ultrastructure</subject><subject>Epithelial Cells - metabolism</subject><subject>Epithelial Cells - ultrastructure</subject><subject>Epithelium - metabolism</subject><subject>Epithelium - ultrastructure</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Genes</subject><subject>Kidney Tubules - metabolism</subject><subject>Kidney Tubules - ultrastructure</subject><subject>Life Sciences</subject><subject>Lysosomes - metabolism</subject><subject>Lysosomes - ultrastructure</subject><subject>Mice</subject><subject>Microscopy</subject><subject>Morphogenesis</subject><subject>Myelin and Lymphocyte-Associated Proteolipid Proteins - genetics</subject><subject>Myelin and Lymphocyte-Associated Proteolipid Proteins - metabolism</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Properties</subject><subject>Proteins</subject><subject>Receptors, Notch - genetics</subject><subject>Receptors, Notch - metabolism</subject><subject>Signal Transduction</subject><subject>SNARE Proteins - genetics</subject><subject>SNARE Proteins - metabolism</subject><subject>Stem Cells</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><issn>1465-7392</issn><issn>1476-4679</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqFkt1qFTEQxxdRbK3iG8iCF-rFqZNsPnZvhFK_CgXBj-uQzU62qXuSNckW-zY-i09mDj22PUWQXCTM_OZP5j9TVU8JHBJo2tfe9A0Bca_aJ0yKFROyu795C76STUf3qkcpnQMQxkA-rPYolyBow_er72_xAqcwr9FnPdURx2XS2QVfB1vr2ZkSRD8Ec5lDcqk2wecYplTj7PIZTq7kZ50zRu_8WDtfX2DM2Eedsc5LX9Ti718hjtqnx9UDq6eET7b3QfXt_buvxx9Xp58-nBwfna6MaCCvGpC9JYaRDqVGzYAPvQTNDQXeUN4hAzP0LaeikZSClS0jnBpiibXD0NvmoHpzpTsv_RoHU1qLelJzdGsdL1XQTu1mvDtTY7hQnFDRSV4EXm4FYvixYMpq7ZLBadIew5IUkcBBFHPh_6gQRBBCuw36_A56HpboixOF4m0rAVp2Q416QuW8DeWLZiOqjhgwKnkrZKEO_0GVM-DalRmhdSW-U_Bqp2AzR_yZR72kpE6-fN5lX1yxJoaUItpr6wiozbqp7boV8tltp6-5v_t1Y08qKT9ivNXzHa0_zgfeHg</recordid><startdate>20150301</startdate><enddate>20150301</enddate><creator>Rodríguez-Fraticelli, Alejo E.</creator><creator>Bagwell, Jennifer</creator><creator>Bosch-Fortea, Minerva</creator><creator>Boncompain, Gaelle</creator><creator>Reglero-Real, Natalia</creator><creator>García-León, Maria J.</creator><creator>Andrés, Germán</creator><creator>Toribio, Maria L.</creator><creator>Alonso, Miguel A.</creator><creator>Millán, Jaime</creator><creator>Perez, Franck</creator><creator>Bagnat, Michel</creator><creator>Martín-Belmonte, Fernando</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope></search><sort><creationdate>20150301</creationdate><title>Developmental regulation of apical endocytosis controls epithelial patterning in vertebrate tubular organs</title><author>Rodríguez-Fraticelli, Alejo E. ; Bagwell, Jennifer ; Bosch-Fortea, Minerva ; Boncompain, Gaelle ; Reglero-Real, Natalia ; García-León, Maria J. ; Andrés, Germán ; Toribio, Maria L. ; Alonso, Miguel A. ; Millán, Jaime ; Perez, Franck ; Bagnat, Michel ; Martín-Belmonte, Fernando</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c630t-307bf1c419e7aea405db70a5c2053259e40cdb852637220f784152c1f1ffddbf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>13/1</topic><topic>13/109</topic><topic>13/89</topic><topic>13/95</topic><topic>14/19</topic><topic>14/28</topic><topic>14/34</topic><topic>14/69</topic><topic>38</topic><topic>38/39</topic><topic>38/77</topic><topic>38/88</topic><topic>42</topic><topic>45</topic><topic>59</topic><topic>631/136</topic><topic>631/80/313/1461</topic><topic>631/80/313/2104</topic><topic>631/80/85/2361</topic><topic>64/116</topic><topic>64/60</topic><topic>82/51</topic><topic>96</topic><topic>96/106</topic><topic>Adaptor Proteins, Vesicular Transport - 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Despite recent advances, how endocytosis regulates the development of vertebrate organs is still unknown. Here we describe a mechanism that facilitates the apical availability of endosomal SNARE receptors for epithelial morphogenesis through the developmental upregulation of
plasmolipin
(
pllp
) in a highly endocytic segment of the zebrafish posterior midgut. The protein PLLP (Pllp in fish) recruits the clathrin adaptor EpsinR to sort the SNARE machinery of the endolysosomal pathway into the subapical compartment, which is a switch for polarized endocytosis. Furthermore, PLLP expression induces apical Crumbs internalization and the activation of the Notch signalling pathway, both crucial steps in the acquisition of cell polarity and differentiation of epithelial cells. We thus postulate that differential apical endosomal SNARE sorting is a mechanism that regulates epithelial patterning.
Bagnat, Martín-Belmonte and colleagues reveal that plasmolipin (PLLP) is upregulated in the zebrafish midgut during development and controls epithelial patterning by promoting polarized endocytosis.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>25706235</pmid><doi>10.1038/ncb3106</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1465-7392 |
| ispartof | Nature cell biology, 2015-03, Vol.17 (3), p.241-250 |
| issn | 1465-7392 1476-4679 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5126975 |
| source | MEDLINE; Nature Journals Online; Alma/SFX Local Collection |
| subjects | 13/1 13/109 13/89 13/95 14/19 14/28 14/34 14/69 38 38/39 38/77 38/88 42 45 59 631/136 631/80/313/1461 631/80/313/2104 631/80/85/2361 64/116 64/60 82/51 96 96/106 Adaptor Proteins, Vesicular Transport - genetics Adaptor Proteins, Vesicular Transport - metabolism Animals Artificial chromosomes Biology Cancer Research Cell Biology Cell Differentiation Cell Line Cell Polarity Cell Proliferation Cell research Cellular proteins Danio rerio Developmental Biology Embryo, Nonmammalian Endocytosis Endosomes - metabolism Endosomes - ultrastructure Epithelial Cells - metabolism Epithelial Cells - ultrastructure Epithelium - metabolism Epithelium - ultrastructure Gene Expression Regulation, Developmental Genes Kidney Tubules - metabolism Kidney Tubules - ultrastructure Life Sciences Lysosomes - metabolism Lysosomes - ultrastructure Mice Microscopy Morphogenesis Myelin and Lymphocyte-Associated Proteolipid Proteins - genetics Myelin and Lymphocyte-Associated Proteolipid Proteins - metabolism Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism Properties Proteins Receptors, Notch - genetics Receptors, Notch - metabolism Signal Transduction SNARE Proteins - genetics SNARE Proteins - metabolism Stem Cells Vertebrates Zebrafish |
| title | Developmental regulation of apical endocytosis controls epithelial patterning in vertebrate tubular organs |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-05T00%3A08%3A46IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Developmental%20regulation%20of%20apical%20endocytosis%20controls%20epithelial%20patterning%20in%20vertebrate%20tubular%C2%A0organs&rft.jtitle=Nature%20cell%20biology&rft.au=Rodr%C3%ADguez-Fraticelli,%20Alejo%20E.&rft.date=2015-03-01&rft.volume=17&rft.issue=3&rft.spage=241&rft.epage=250&rft.pages=241-250&rft.issn=1465-7392&rft.eissn=1476-4679&rft_id=info:doi/10.1038/ncb3106&rft_dat=%3Cgale_pubme%3EA404275867%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1658870084&rft_id=info:pmid/25706235&rft_galeid=A404275867&rfr_iscdi=true |