Synaptophysin Regulates Clathrin-Independent Endocytosis of Synaptic Vesicles
The GTPase dynamin I is required for synaptic vesicle (SV) endocytosis. Our observation that dynamin binds to the SV protein synaptophysin in a Ca2+-dependent fashion suggested the possibility that a dynamin/synaptophysin complex functions in SV recycling. In this paper we show that disruption of th...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2000-05, Vol.97 (11), p.6120-6125 |
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creator | Daly, Christopher Sugimori, Mutsuyuki Moreira, Jorge E. Ziff, Edward B. Llinas, Rodolfo |
description | The GTPase dynamin I is required for synaptic vesicle (SV) endocytosis. Our observation that dynamin binds to the SV protein synaptophysin in a Ca2+-dependent fashion suggested the possibility that a dynamin/synaptophysin complex functions in SV recycling. In this paper we show that disruption of the dynamin/synaptophysin interaction by peptide injection into the squid giant synapse preterminal results in a decrease in transmitter release during high-frequency stimulation, indicating an inhibition of SV recycling. Electron microscopy of these synapses reveals a depletion of SVs, demonstrating a block of vesicle retrieval after fusion. In addition, we observed an increase in clathrin-coated vesicles, indicating that the peptide does not block clathrin-dependent endocytosis. We conclude that the dynamin/synaptophysin complex functions in a clathrin-independent mechanism of SV endocytosis that is required for efficient synaptic transmission. |
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Our observation that dynamin binds to the SV protein synaptophysin in a Ca2+-dependent fashion suggested the possibility that a dynamin/synaptophysin complex functions in SV recycling. In this paper we show that disruption of the dynamin/synaptophysin interaction by peptide injection into the squid giant synapse preterminal results in a decrease in transmitter release during high-frequency stimulation, indicating an inhibition of SV recycling. Electron microscopy of these synapses reveals a depletion of SVs, demonstrating a block of vesicle retrieval after fusion. In addition, we observed an increase in clathrin-coated vesicles, indicating that the peptide does not block clathrin-dependent endocytosis. We conclude that the dynamin/synaptophysin complex functions in a clathrin-independent mechanism of SV endocytosis that is required for efficient synaptic transmission.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.97.11.6120</identifier><identifier>PMID: 10823955</identifier><language>eng</language><publisher>United States: National Academy of Sciences of the United States of America</publisher><subject>Action potentials ; Animals ; Biological Sciences ; Calcium - physiology ; Cell membranes ; Clathrin - physiology ; Decapodiformes ; dynamin ; Dynamin I ; Dynamins ; Endocytosis ; Endocytosis - physiology ; GTP Phosphohydrolases - physiology ; Macromolecular Substances ; Membrane Fusion ; Nerve Tissue Proteins - physiology ; Neurology ; Neuroscience ; Peptides ; Proteins ; Radio transmitters ; Recombinant Fusion Proteins - physiology ; Recycling ; Squid ; Stellate Ganglion - cytology ; Synapses ; Synaptic Transmission - physiology ; Synaptic Vesicles - physiology ; Synaptophysin - physiology ; Transmitters</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2000-05, Vol.97 (11), p.6120-6125</ispartof><rights>Copyright 1993-2000 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences May 23, 2000</rights><rights>Copyright © 2000, The National Academy of Sciences 2000</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c586t-e986ffac364406e34d3902f5c259c7550dbbf6d21e64b0542d62620ee74ab4953</citedby><cites>FETCH-LOGICAL-c586t-e986ffac364406e34d3902f5c259c7550dbbf6d21e64b0542d62620ee74ab4953</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/97/11.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/122591$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/122591$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,728,781,785,804,886,27929,27930,53796,53798,58022,58255</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/10823955$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Daly, Christopher</creatorcontrib><creatorcontrib>Sugimori, Mutsuyuki</creatorcontrib><creatorcontrib>Moreira, Jorge E.</creatorcontrib><creatorcontrib>Ziff, Edward B.</creatorcontrib><creatorcontrib>Llinas, Rodolfo</creatorcontrib><title>Synaptophysin Regulates Clathrin-Independent Endocytosis of Synaptic Vesicles</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The GTPase dynamin I is required for synaptic vesicle (SV) endocytosis. Our observation that dynamin binds to the SV protein synaptophysin in a Ca2+-dependent fashion suggested the possibility that a dynamin/synaptophysin complex functions in SV recycling. In this paper we show that disruption of the dynamin/synaptophysin interaction by peptide injection into the squid giant synapse preterminal results in a decrease in transmitter release during high-frequency stimulation, indicating an inhibition of SV recycling. Electron microscopy of these synapses reveals a depletion of SVs, demonstrating a block of vesicle retrieval after fusion. In addition, we observed an increase in clathrin-coated vesicles, indicating that the peptide does not block clathrin-dependent endocytosis. We conclude that the dynamin/synaptophysin complex functions in a clathrin-independent mechanism of SV endocytosis that is required for efficient synaptic transmission.</description><subject>Action potentials</subject><subject>Animals</subject><subject>Biological Sciences</subject><subject>Calcium - physiology</subject><subject>Cell membranes</subject><subject>Clathrin - physiology</subject><subject>Decapodiformes</subject><subject>dynamin</subject><subject>Dynamin I</subject><subject>Dynamins</subject><subject>Endocytosis</subject><subject>Endocytosis - physiology</subject><subject>GTP Phosphohydrolases - physiology</subject><subject>Macromolecular Substances</subject><subject>Membrane Fusion</subject><subject>Nerve Tissue Proteins - physiology</subject><subject>Neurology</subject><subject>Neuroscience</subject><subject>Peptides</subject><subject>Proteins</subject><subject>Radio transmitters</subject><subject>Recombinant Fusion Proteins - physiology</subject><subject>Recycling</subject><subject>Squid</subject><subject>Stellate Ganglion - cytology</subject><subject>Synapses</subject><subject>Synaptic Transmission - physiology</subject><subject>Synaptic Vesicles - physiology</subject><subject>Synaptophysin - physiology</subject><subject>Transmitters</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2000</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1v1DAQxS1ERZfCmQMSijjAKdsZxx-xxAWtCq1UhMTX1XIcp5tV1k7jBLH_PV5labcIicvMYX7vzdiPkBcISwRZnPfexKWSS8SlQAqPyAJBYS6YgsdkAUBlXjLKTsnTGDcAoHgJT8gpQkkLxfmCfPq686YfQ7_exdZnX9zN1JnRxWyV2npofX7la9e7VPyYXfg62N0YYhuz0GSztrXZDxdb27n4jJw0povu-aGfke8fLr6tLvPrzx-vVu-vc8tLMeZOlaJpjC0EYyBcwepCAW24pVxZyTnUVdWImqITrALOaC2ooOCcZKZiihdn5N3s20_V1tU23TaYTvdDuzXDTgfT6ocT3671TfipseSiTPI3B_kQbicXR71to3VdZ7wLU9QSkfJCqv-CKDmVrMQEvv4L3IRp8OkPNAUsEqZEgs5nyA4hxsE1dwcj6H2ceh-nVlIj6n2cSfHq-J1H_JxfAt4egL3yz_jeQTdT143u13hk9W8yAS9nYBPHMNyvoikULH4DioG92A</recordid><startdate>20000523</startdate><enddate>20000523</enddate><creator>Daly, Christopher</creator><creator>Sugimori, Mutsuyuki</creator><creator>Moreira, Jorge E.</creator><creator>Ziff, Edward B.</creator><creator>Llinas, Rodolfo</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><general>National Academy of Sciences</general><general>The National Academy of Sciences</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>7QR</scope><scope>7SN</scope><scope>7SS</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>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20000523</creationdate><title>Synaptophysin Regulates Clathrin-Independent Endocytosis of Synaptic Vesicles</title><author>Daly, Christopher ; Sugimori, Mutsuyuki ; Moreira, Jorge E. ; Ziff, Edward B. ; Llinas, Rodolfo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c586t-e986ffac364406e34d3902f5c259c7550dbbf6d21e64b0542d62620ee74ab4953</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2000</creationdate><topic>Action potentials</topic><topic>Animals</topic><topic>Biological Sciences</topic><topic>Calcium - physiology</topic><topic>Cell membranes</topic><topic>Clathrin - physiology</topic><topic>Decapodiformes</topic><topic>dynamin</topic><topic>Dynamin I</topic><topic>Dynamins</topic><topic>Endocytosis</topic><topic>Endocytosis - physiology</topic><topic>GTP Phosphohydrolases - physiology</topic><topic>Macromolecular Substances</topic><topic>Membrane Fusion</topic><topic>Nerve Tissue Proteins - physiology</topic><topic>Neurology</topic><topic>Neuroscience</topic><topic>Peptides</topic><topic>Proteins</topic><topic>Radio transmitters</topic><topic>Recombinant Fusion Proteins - physiology</topic><topic>Recycling</topic><topic>Squid</topic><topic>Stellate Ganglion - cytology</topic><topic>Synapses</topic><topic>Synaptic Transmission - physiology</topic><topic>Synaptic Vesicles - physiology</topic><topic>Synaptophysin - physiology</topic><topic>Transmitters</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Daly, Christopher</creatorcontrib><creatorcontrib>Sugimori, Mutsuyuki</creatorcontrib><creatorcontrib>Moreira, Jorge E.</creatorcontrib><creatorcontrib>Ziff, Edward B.</creatorcontrib><creatorcontrib>Llinas, Rodolfo</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>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</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>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>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Daly, Christopher</au><au>Sugimori, Mutsuyuki</au><au>Moreira, Jorge E.</au><au>Ziff, Edward B.</au><au>Llinas, Rodolfo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Synaptophysin Regulates Clathrin-Independent Endocytosis of Synaptic Vesicles</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2000-05-23</date><risdate>2000</risdate><volume>97</volume><issue>11</issue><spage>6120</spage><epage>6125</epage><pages>6120-6125</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>The GTPase dynamin I is required for synaptic vesicle (SV) endocytosis. 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subjects | Action potentials Animals Biological Sciences Calcium - physiology Cell membranes Clathrin - physiology Decapodiformes dynamin Dynamin I Dynamins Endocytosis Endocytosis - physiology GTP Phosphohydrolases - physiology Macromolecular Substances Membrane Fusion Nerve Tissue Proteins - physiology Neurology Neuroscience Peptides Proteins Radio transmitters Recombinant Fusion Proteins - physiology Recycling Squid Stellate Ganglion - cytology Synapses Synaptic Transmission - physiology Synaptic Vesicles - physiology Synaptophysin - physiology Transmitters |
title | Synaptophysin Regulates Clathrin-Independent Endocytosis of Synaptic Vesicles |
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