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Endosome maturation factors Rabenosyn‐5/VPS45 and caveolin‐1 regulate ciliary membrane and polycystin‐2 homeostasis
Primary cilium structure and function relies on control of ciliary membrane homeostasis, regulated by membrane trafficking processes that deliver and retrieve ciliary components at the periciliary membrane. However, the molecular mechanisms controlling ciliary membrane establishment and maintenance,...
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Published in: | The EMBO journal 2018-05, Vol.37 (9), p.n/a |
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description | Primary cilium structure and function relies on control of ciliary membrane homeostasis, regulated by membrane trafficking processes that deliver and retrieve ciliary components at the periciliary membrane. However, the molecular mechanisms controlling ciliary membrane establishment and maintenance, especially in relation to endocytosis, remain poorly understood. Here, using Caenorhabditis elegans, we describe closely linked functions for early endosome (EE) maturation factors RABS‐5 (Rabenosyn‐5) and VPS‐45 (VPS45) in regulating cilium length and morphology, ciliary and periciliary membrane volume, and ciliary signalling‐related sensory behaviour. We demonstrate that RABS‐5 and VPS‐45 control periciliary vesicle number and levels of select EE/endocytic markers (WDFY‐2, CAV‐1) and the ciliopathy membrane receptor PKD‐2 (polycystin‐2). Moreover, we show that CAV‐1 (caveolin‐1) also controls PKD‐2 ciliary levels and associated sensory behaviour. These data link RABS‐5 and VPS‐45 ciliary functions to the processing of periciliary‐derived endocytic vesicles and regulation of ciliary membrane homeostasis. Our findings also provide insight into the regulation of PKD‐2 ciliary levels via integrated endosomal sorting and CAV‐1‐mediated endocytosis.
Synopsis
Sensory and developmental signaling events at the ciliary membrane regulate tissue formation and are disrupted in human ciliopathy disorders. Caenorhabditis elegans endosome maturation factors Rabenosyn‐5 (RABS‐5) and VPS‐45 regulate ciliary and peri‐ciliary membrane homeostasis, and, together with caveolin‐1 (CAV‐1), control the ciliary levels of polycystin‐2 (PKD‐2).
Loss of C. elegans RABS‐5 and VPS‐45 causes defects in cilium structure and function, including ciliary and peri‐ciliary membrane expansions.
RABS‐5 and VPS‐45 control peri‐ciliary vesicle number and levels of CAV‐1 and other endocytic markers near the ciliary base.
RABS‐5, VPS‐45 and CAV‐1 control endosomal sorting of ciliary PKD‐2.
RABS‐5, VPS‐45 and CAV‐1 are required for PKD‐2‐mediated male mating sensory behaviour.
Endosomal uptake and sorting affect male mating behaviour in Caenorhabditis elegans by regulating ciliary membrane dynamics and the localization of polycystic kidney disease‐associated factor polycystin‐2 in sensory cilia. |
doi_str_mv | 10.15252/embj.201798248 |
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Synopsis
Sensory and developmental signaling events at the ciliary membrane regulate tissue formation and are disrupted in human ciliopathy disorders. Caenorhabditis elegans endosome maturation factors Rabenosyn‐5 (RABS‐5) and VPS‐45 regulate ciliary and peri‐ciliary membrane homeostasis, and, together with caveolin‐1 (CAV‐1), control the ciliary levels of polycystin‐2 (PKD‐2).
Loss of C. elegans RABS‐5 and VPS‐45 causes defects in cilium structure and function, including ciliary and peri‐ciliary membrane expansions.
RABS‐5 and VPS‐45 control peri‐ciliary vesicle number and levels of CAV‐1 and other endocytic markers near the ciliary base.
RABS‐5, VPS‐45 and CAV‐1 control endosomal sorting of ciliary PKD‐2.
RABS‐5, VPS‐45 and CAV‐1 are required for PKD‐2‐mediated male mating sensory behaviour.
Endosomal uptake and sorting affect male mating behaviour in Caenorhabditis elegans by regulating ciliary membrane dynamics and the localization of polycystic kidney disease‐associated factor polycystin‐2 in sensory cilia.</description><identifier>ISSN: 0261-4189</identifier><identifier>EISSN: 1460-2075</identifier><identifier>DOI: 10.15252/embj.201798248</identifier><identifier>PMID: 29572244</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Animals ; Caenorhabditis elegans ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; Caveolin ; Caveolin 1 - genetics ; Caveolin 1 - metabolism ; caveolin‐1 ; Cell Membrane - genetics ; Cell Membrane - metabolism ; cilia ; Cilia - genetics ; Cilia - metabolism ; Control ; Endocytosis ; Homeostasis ; Markers ; Mating behavior ; Maturation ; Membrane trafficking ; Molecular modelling ; Nematodes ; PKD2 ; Rabenosyn‐5 ; Signaling ; Structure-function relationships ; TRPP Cation Channels - genetics ; TRPP Cation Channels - metabolism ; Vesicular Transport Proteins - genetics ; Vesicular Transport Proteins - metabolism ; VPS45</subject><ispartof>The EMBO journal, 2018-05, Vol.37 (9), p.n/a</ispartof><rights>2018 The Authors</rights><rights>2018 The Authors.</rights><rights>2018 EMBO</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4988-53043331639bccaff6dab424f7c08f7528680a42cc12dbfded082861b7ebae953</citedby><cites>FETCH-LOGICAL-c4988-53043331639bccaff6dab424f7c08f7528680a42cc12dbfded082861b7ebae953</cites><orcidid>0000-0002-7090-4123 ; 0000-0003-1598-2695</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.15252%2Fembj.201798248$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.15252%2Fembj.201798248$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,50923,51032,53827,53829</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29572244$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Scheidel, Noémie</creatorcontrib><creatorcontrib>Kennedy, Julie</creatorcontrib><creatorcontrib>Blacque, Oliver E</creatorcontrib><title>Endosome maturation factors Rabenosyn‐5/VPS45 and caveolin‐1 regulate ciliary membrane and polycystin‐2 homeostasis</title><title>The EMBO journal</title><addtitle>EMBO J</addtitle><description>Primary cilium structure and function relies on control of ciliary membrane homeostasis, regulated by membrane trafficking processes that deliver and retrieve ciliary components at the periciliary membrane. However, the molecular mechanisms controlling ciliary membrane establishment and maintenance, especially in relation to endocytosis, remain poorly understood. Here, using Caenorhabditis elegans, we describe closely linked functions for early endosome (EE) maturation factors RABS‐5 (Rabenosyn‐5) and VPS‐45 (VPS45) in regulating cilium length and morphology, ciliary and periciliary membrane volume, and ciliary signalling‐related sensory behaviour. We demonstrate that RABS‐5 and VPS‐45 control periciliary vesicle number and levels of select EE/endocytic markers (WDFY‐2, CAV‐1) and the ciliopathy membrane receptor PKD‐2 (polycystin‐2). Moreover, we show that CAV‐1 (caveolin‐1) also controls PKD‐2 ciliary levels and associated sensory behaviour. These data link RABS‐5 and VPS‐45 ciliary functions to the processing of periciliary‐derived endocytic vesicles and regulation of ciliary membrane homeostasis. Our findings also provide insight into the regulation of PKD‐2 ciliary levels via integrated endosomal sorting and CAV‐1‐mediated endocytosis.
Synopsis
Sensory and developmental signaling events at the ciliary membrane regulate tissue formation and are disrupted in human ciliopathy disorders. Caenorhabditis elegans endosome maturation factors Rabenosyn‐5 (RABS‐5) and VPS‐45 regulate ciliary and peri‐ciliary membrane homeostasis, and, together with caveolin‐1 (CAV‐1), control the ciliary levels of polycystin‐2 (PKD‐2).
Loss of C. elegans RABS‐5 and VPS‐45 causes defects in cilium structure and function, including ciliary and peri‐ciliary membrane expansions.
RABS‐5 and VPS‐45 control peri‐ciliary vesicle number and levels of CAV‐1 and other endocytic markers near the ciliary base.
RABS‐5, VPS‐45 and CAV‐1 control endosomal sorting of ciliary PKD‐2.
RABS‐5, VPS‐45 and CAV‐1 are required for PKD‐2‐mediated male mating sensory behaviour.
Endosomal uptake and sorting affect male mating behaviour in Caenorhabditis elegans by regulating ciliary membrane dynamics and the localization of polycystic kidney disease‐associated factor polycystin‐2 in sensory cilia.</description><subject>Animals</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans - metabolism</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Caveolin</subject><subject>Caveolin 1 - genetics</subject><subject>Caveolin 1 - metabolism</subject><subject>caveolin‐1</subject><subject>Cell Membrane - genetics</subject><subject>Cell Membrane - metabolism</subject><subject>cilia</subject><subject>Cilia - genetics</subject><subject>Cilia - metabolism</subject><subject>Control</subject><subject>Endocytosis</subject><subject>Homeostasis</subject><subject>Markers</subject><subject>Mating behavior</subject><subject>Maturation</subject><subject>Membrane trafficking</subject><subject>Molecular modelling</subject><subject>Nematodes</subject><subject>PKD2</subject><subject>Rabenosyn‐5</subject><subject>Signaling</subject><subject>Structure-function relationships</subject><subject>TRPP Cation Channels - genetics</subject><subject>TRPP Cation Channels - metabolism</subject><subject>Vesicular Transport Proteins - genetics</subject><subject>Vesicular Transport Proteins - metabolism</subject><subject>VPS45</subject><issn>0261-4189</issn><issn>1460-2075</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNqFkctu1DAYhS0EosPAmh2yxIZNOr4mNgskqAZaVATitrUcx2k9cuzBToqy4xF4Rp4Ed6YMlw0rS78_H5_zHwAeYnSMOeFkZYd2c0wQbqQgTNwCC8xqVBHU8NtggUiNK4aFPAL3ct4ghLho8F1wRCRvCGFsAeZ16GKOg4WDHqekRxcD7LUZY8rwvW5tiHkOP75956vP7z4wDnXooNFXNnp3PcYw2YvJ69FC47zTaYZD8ZR0sDt0G_1s5jzuYAIvy08xjzq7fB_c6bXP9sHNuQSfXq4_npxW529fnZ08P68Mk0JUnCJGKcU1la0xuu_rTreMsL4xSPQNJ6IWSDNiDCZd23e2Q6LMcNvYVlvJ6RI82-tup3awnbFhTNqrbXJDcauidurvm-Au1UW8UlwSRGhTBJ7cCKT4ZbJ5VIPLxnpfMsYpq7J9gSiTmBX08T_oJk4plHiFopjUkpQwS7DaUybFnJPtD2YwUrta1XWt6lBrefHozwwH_lePBXi6B746b-f_6an1mxevf6v_BKQrtKU</recordid><startdate>20180502</startdate><enddate>20180502</enddate><creator>Scheidel, Noémie</creator><creator>Kennedy, Julie</creator><creator>Blacque, Oliver E</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7090-4123</orcidid><orcidid>https://orcid.org/0000-0003-1598-2695</orcidid></search><sort><creationdate>20180502</creationdate><title>Endosome maturation factors Rabenosyn‐5/VPS45 and caveolin‐1 regulate ciliary membrane and polycystin‐2 homeostasis</title><author>Scheidel, Noémie ; Kennedy, Julie ; Blacque, Oliver E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4988-53043331639bccaff6dab424f7c08f7528680a42cc12dbfded082861b7ebae953</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Caenorhabditis elegans</topic><topic>Caenorhabditis elegans - genetics</topic><topic>Caenorhabditis elegans - metabolism</topic><topic>Caenorhabditis elegans Proteins - genetics</topic><topic>Caenorhabditis elegans Proteins - metabolism</topic><topic>Caveolin</topic><topic>Caveolin 1 - genetics</topic><topic>Caveolin 1 - metabolism</topic><topic>caveolin‐1</topic><topic>Cell Membrane - genetics</topic><topic>Cell Membrane - metabolism</topic><topic>cilia</topic><topic>Cilia - genetics</topic><topic>Cilia - metabolism</topic><topic>Control</topic><topic>Endocytosis</topic><topic>Homeostasis</topic><topic>Markers</topic><topic>Mating behavior</topic><topic>Maturation</topic><topic>Membrane trafficking</topic><topic>Molecular modelling</topic><topic>Nematodes</topic><topic>PKD2</topic><topic>Rabenosyn‐5</topic><topic>Signaling</topic><topic>Structure-function relationships</topic><topic>TRPP Cation Channels - genetics</topic><topic>TRPP Cation Channels - metabolism</topic><topic>Vesicular Transport Proteins - genetics</topic><topic>Vesicular Transport Proteins - metabolism</topic><topic>VPS45</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Scheidel, Noémie</creatorcontrib><creatorcontrib>Kennedy, Julie</creatorcontrib><creatorcontrib>Blacque, Oliver E</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors 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>ProQuest Health & Medical Complete (Alumni)</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 EMBO journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Scheidel, Noémie</au><au>Kennedy, Julie</au><au>Blacque, Oliver E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Endosome maturation factors Rabenosyn‐5/VPS45 and caveolin‐1 regulate ciliary membrane and polycystin‐2 homeostasis</atitle><jtitle>The EMBO journal</jtitle><addtitle>EMBO J</addtitle><date>2018-05-02</date><risdate>2018</risdate><volume>37</volume><issue>9</issue><epage>n/a</epage><issn>0261-4189</issn><eissn>1460-2075</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Primary cilium structure and function relies on control of ciliary membrane homeostasis, regulated by membrane trafficking processes that deliver and retrieve ciliary components at the periciliary membrane. However, the molecular mechanisms controlling ciliary membrane establishment and maintenance, especially in relation to endocytosis, remain poorly understood. Here, using Caenorhabditis elegans, we describe closely linked functions for early endosome (EE) maturation factors RABS‐5 (Rabenosyn‐5) and VPS‐45 (VPS45) in regulating cilium length and morphology, ciliary and periciliary membrane volume, and ciliary signalling‐related sensory behaviour. We demonstrate that RABS‐5 and VPS‐45 control periciliary vesicle number and levels of select EE/endocytic markers (WDFY‐2, CAV‐1) and the ciliopathy membrane receptor PKD‐2 (polycystin‐2). Moreover, we show that CAV‐1 (caveolin‐1) also controls PKD‐2 ciliary levels and associated sensory behaviour. These data link RABS‐5 and VPS‐45 ciliary functions to the processing of periciliary‐derived endocytic vesicles and regulation of ciliary membrane homeostasis. Our findings also provide insight into the regulation of PKD‐2 ciliary levels via integrated endosomal sorting and CAV‐1‐mediated endocytosis.
Synopsis
Sensory and developmental signaling events at the ciliary membrane regulate tissue formation and are disrupted in human ciliopathy disorders. Caenorhabditis elegans endosome maturation factors Rabenosyn‐5 (RABS‐5) and VPS‐45 regulate ciliary and peri‐ciliary membrane homeostasis, and, together with caveolin‐1 (CAV‐1), control the ciliary levels of polycystin‐2 (PKD‐2).
Loss of C. elegans RABS‐5 and VPS‐45 causes defects in cilium structure and function, including ciliary and peri‐ciliary membrane expansions.
RABS‐5 and VPS‐45 control peri‐ciliary vesicle number and levels of CAV‐1 and other endocytic markers near the ciliary base.
RABS‐5, VPS‐45 and CAV‐1 control endosomal sorting of ciliary PKD‐2.
RABS‐5, VPS‐45 and CAV‐1 are required for PKD‐2‐mediated male mating sensory behaviour.
Endosomal uptake and sorting affect male mating behaviour in Caenorhabditis elegans by regulating ciliary membrane dynamics and the localization of polycystic kidney disease‐associated factor polycystin‐2 in sensory cilia.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>29572244</pmid><doi>10.15252/embj.201798248</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-7090-4123</orcidid><orcidid>https://orcid.org/0000-0003-1598-2695</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Caveolin Caveolin 1 - genetics Caveolin 1 - metabolism caveolin‐1 Cell Membrane - genetics Cell Membrane - metabolism cilia Cilia - genetics Cilia - metabolism Control Endocytosis Homeostasis Markers Mating behavior Maturation Membrane trafficking Molecular modelling Nematodes PKD2 Rabenosyn‐5 Signaling Structure-function relationships TRPP Cation Channels - genetics TRPP Cation Channels - metabolism Vesicular Transport Proteins - genetics Vesicular Transport Proteins - metabolism VPS45 |
title | Endosome maturation factors Rabenosyn‐5/VPS45 and caveolin‐1 regulate ciliary membrane and polycystin‐2 homeostasis |
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