Ultrafast endocytosis at mouse hippocampal synapses
To sustain neurotransmission, synaptic vesicles and their associated proteins must be recycled locally at synapses. Synaptic vesicles are thought to be regenerated approximately 20 s after fusion by the assembly of clathrin scaffolds or in approximately 1 s by the reversal of fusion pores via ‘kiss-...
Gespeichert in:
| Veröffentlicht in: | Nature (London) 2013-12, Vol.504 (7479), p.242-247 |
|---|---|
| Hauptverfasser: | , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 247 |
|---|---|
| container_issue | 7479 |
| container_start_page | 242 |
| container_title | Nature (London) |
| container_volume | 504 |
| creator | Watanabe, Shigeki Rost, Benjamin R. Camacho-Pérez, Marcial Davis, M. Wayne Söhl-Kielczynski, Berit Rosenmund, Christian Jorgensen, Erik M. |
| description | To sustain neurotransmission, synaptic vesicles and their associated proteins must be recycled locally at synapses. Synaptic vesicles are thought to be regenerated approximately 20 s after fusion by the assembly of clathrin scaffolds or in approximately 1 s by the reversal of fusion pores via ‘kiss-and-run’ endocytosis. Here we use optogenetics to stimulate cultured hippocampal neurons with a single stimulus, rapidly freeze them after fixed intervals and examine the ultrastructure using electron microscopy—‘flash-and-freeze’ electron microscopy. Docked vesicles fuse and collapse into the membrane within 30 ms of the stimulus. Compensatory endocytosis occurs within 50 to 100 ms at sites flanking the active zone. Invagination is blocked by inhibition of actin polymerization, and scission is blocked by inhibiting dynamin. Because intact synaptic vesicles are not recovered, this form of recycling is not compatible with kiss-and-run endocytosis; moreover, it is 200-fold faster than clathrin-mediated endocytosis. It is likely that ‘ultrafast endocytosis’ is specialized to restore the surface area of the membrane rapidly.
Sustained neurotransmission requires recycling of synaptic vesicles, but the proposed mechanisms have been controversial; here a ‘flash-and-freeze’ method for electron microscopy reveals a new ultrafast form of endocytosis that is actin- and dynamin-dependent and occurs within 100 milliseconds of stimulation.
A quick look at synaptic endocytosis
Sustained neurotransmission requires recycling of synaptic vesicles but the proposed mechanisms — clathrin-mediated endocytosis and 'kiss-and-run' reversal of fusion — have been controversial. Now Erik Jorgensen and colleagues, using ultrafast, 'flash-and-freeze' electron microscopy, have identified a previously unknown actin- and dynamin-dependent mechanism of endocytosis, occurring within 100 milliseconds of stimulation in mouse hippocampal neurons. This is 200-times faster than the clathrin-mediated process, and morphological characteristics rule out the 'kiss-and-run' model. This work suggests that rapid internalization of membrane from the surface is the first step in endocytosis. |
| doi_str_mv | 10.1038/nature12809 |
| format | Article |
| fullrecord | <record><control><sourceid>gale_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3957339</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A355558706</galeid><sourcerecordid>A355558706</sourcerecordid><originalsourceid>FETCH-LOGICAL-c675t-d74506559f1e1a467d536522d2137ec0bfb17299bb8aa99174fdddf3ceda4b9b3</originalsourceid><addsrcrecordid>eNqF0l1r1EAUBuAgit1Wr7yXRSkomnrmK5O5EUrxo1AQ1F4Pk8nJdkoyk2YScf-9s-za7krA5CKQefLmzJmTZS8InBFg5QdvxmlAQktQj7IF4bLIeVHKx9kCgJY5lKw4yo5jvAUAQSR_mh1RzkCAEIuMXbfjYBoTxyX6Otj1GKKLSzMuuzBFXN64vg_WdL1pl3HtTR8xPsueNKaN-Hz3PMmuP3_6efE1v_r25fLi_Cq3hRRjXksuoBBCNQSJ4YWsBSsEpTUlTKKFqqmIpEpVVWmMUqmypq7rhlmsDa9UxU6yj9vcfqo6rC36VGqr-8F1ZljrYJw-XPHuRq_CL82UkIypFPBmFzCEuwnjqDsXLbat8Zh2p4kUTNCCgvw_5YWiZNOzRF__Q2_DNPjUiaQkgOIE6INamRa1801IJdpNqD5nIl2lhCKpfEat0GPaT_DYuPT6wL-a8bZ3d3ofnc2gdNfYOTub-vbgg2RG_D2uzBSjvvzx_dC-21o7hBgHbO7Pg4DezKPem8ekX-4f4b39O4AJnO6Aida0zWC8dfHBlcB5ySG591sX05Jf4bDX9Jn__gEznfQX</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1470094102</pqid></control><display><type>article</type><title>Ultrafast endocytosis at mouse hippocampal synapses</title><source>MEDLINE</source><source>SpringerLink Journals</source><source>Nature</source><creator>Watanabe, Shigeki ; Rost, Benjamin R. ; Camacho-Pérez, Marcial ; Davis, M. Wayne ; Söhl-Kielczynski, Berit ; Rosenmund, Christian ; Jorgensen, Erik M.</creator><creatorcontrib>Watanabe, Shigeki ; Rost, Benjamin R. ; Camacho-Pérez, Marcial ; Davis, M. Wayne ; Söhl-Kielczynski, Berit ; Rosenmund, Christian ; Jorgensen, Erik M.</creatorcontrib><description>To sustain neurotransmission, synaptic vesicles and their associated proteins must be recycled locally at synapses. Synaptic vesicles are thought to be regenerated approximately 20 s after fusion by the assembly of clathrin scaffolds or in approximately 1 s by the reversal of fusion pores via ‘kiss-and-run’ endocytosis. Here we use optogenetics to stimulate cultured hippocampal neurons with a single stimulus, rapidly freeze them after fixed intervals and examine the ultrastructure using electron microscopy—‘flash-and-freeze’ electron microscopy. Docked vesicles fuse and collapse into the membrane within 30 ms of the stimulus. Compensatory endocytosis occurs within 50 to 100 ms at sites flanking the active zone. Invagination is blocked by inhibition of actin polymerization, and scission is blocked by inhibiting dynamin. Because intact synaptic vesicles are not recovered, this form of recycling is not compatible with kiss-and-run endocytosis; moreover, it is 200-fold faster than clathrin-mediated endocytosis. It is likely that ‘ultrafast endocytosis’ is specialized to restore the surface area of the membrane rapidly.
Sustained neurotransmission requires recycling of synaptic vesicles, but the proposed mechanisms have been controversial; here a ‘flash-and-freeze’ method for electron microscopy reveals a new ultrafast form of endocytosis that is actin- and dynamin-dependent and occurs within 100 milliseconds of stimulation.
A quick look at synaptic endocytosis
Sustained neurotransmission requires recycling of synaptic vesicles but the proposed mechanisms — clathrin-mediated endocytosis and 'kiss-and-run' reversal of fusion — have been controversial. Now Erik Jorgensen and colleagues, using ultrafast, 'flash-and-freeze' electron microscopy, have identified a previously unknown actin- and dynamin-dependent mechanism of endocytosis, occurring within 100 milliseconds of stimulation in mouse hippocampal neurons. This is 200-times faster than the clathrin-mediated process, and morphological characteristics rule out the 'kiss-and-run' model. This work suggests that rapid internalization of membrane from the surface is the first step in endocytosis.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/nature12809</identifier><identifier>PMID: 24305055</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>101/28 ; 13/106 ; 14 ; 14/28 ; 147/143 ; 631/378/548/2588 ; 631/378/548/2589 ; 631/80/313/1461 ; 631/80/313/1481 ; 64/60 ; 9/74 ; Actins - metabolism ; Actins - ultrastructure ; Action Potentials ; Animals ; Biological and medical sciences ; Dynamins - metabolism ; Dynamins - ultrastructure ; Electron microscopy ; Endocytosis ; Exocytosis ; Experiments ; Fundamental and applied biological sciences. Psychology ; Hippocampus - cytology ; Humanities and Social Sciences ; Light ; Membrane Fusion ; Mice ; Microscopy, Electron ; multidisciplinary ; Neural transmission ; Physiological aspects ; Proteins ; Rhodopsin - genetics ; Rhodopsin - metabolism ; Science ; Synapses ; Synapses - metabolism ; Synapses - ultrastructure ; Synaptic Transmission ; Synaptic Vesicles - metabolism ; Synaptic Vesicles - ultrastructure ; Time Factors ; Vertebrates: nervous system and sense organs</subject><ispartof>Nature (London), 2013-12, Vol.504 (7479), p.242-247</ispartof><rights>Springer Nature Limited 2013</rights><rights>2015 INIST-CNRS</rights><rights>COPYRIGHT 2013 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Dec 12, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c675t-d74506559f1e1a467d536522d2137ec0bfb17299bb8aa99174fdddf3ceda4b9b3</citedby><cites>FETCH-LOGICAL-c675t-d74506559f1e1a467d536522d2137ec0bfb17299bb8aa99174fdddf3ceda4b9b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nature12809$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nature12809$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=28044840$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24305055$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Watanabe, Shigeki</creatorcontrib><creatorcontrib>Rost, Benjamin R.</creatorcontrib><creatorcontrib>Camacho-Pérez, Marcial</creatorcontrib><creatorcontrib>Davis, M. Wayne</creatorcontrib><creatorcontrib>Söhl-Kielczynski, Berit</creatorcontrib><creatorcontrib>Rosenmund, Christian</creatorcontrib><creatorcontrib>Jorgensen, Erik M.</creatorcontrib><title>Ultrafast endocytosis at mouse hippocampal synapses</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>To sustain neurotransmission, synaptic vesicles and their associated proteins must be recycled locally at synapses. Synaptic vesicles are thought to be regenerated approximately 20 s after fusion by the assembly of clathrin scaffolds or in approximately 1 s by the reversal of fusion pores via ‘kiss-and-run’ endocytosis. Here we use optogenetics to stimulate cultured hippocampal neurons with a single stimulus, rapidly freeze them after fixed intervals and examine the ultrastructure using electron microscopy—‘flash-and-freeze’ electron microscopy. Docked vesicles fuse and collapse into the membrane within 30 ms of the stimulus. Compensatory endocytosis occurs within 50 to 100 ms at sites flanking the active zone. Invagination is blocked by inhibition of actin polymerization, and scission is blocked by inhibiting dynamin. Because intact synaptic vesicles are not recovered, this form of recycling is not compatible with kiss-and-run endocytosis; moreover, it is 200-fold faster than clathrin-mediated endocytosis. It is likely that ‘ultrafast endocytosis’ is specialized to restore the surface area of the membrane rapidly.
Sustained neurotransmission requires recycling of synaptic vesicles, but the proposed mechanisms have been controversial; here a ‘flash-and-freeze’ method for electron microscopy reveals a new ultrafast form of endocytosis that is actin- and dynamin-dependent and occurs within 100 milliseconds of stimulation.
A quick look at synaptic endocytosis
Sustained neurotransmission requires recycling of synaptic vesicles but the proposed mechanisms — clathrin-mediated endocytosis and 'kiss-and-run' reversal of fusion — have been controversial. Now Erik Jorgensen and colleagues, using ultrafast, 'flash-and-freeze' electron microscopy, have identified a previously unknown actin- and dynamin-dependent mechanism of endocytosis, occurring within 100 milliseconds of stimulation in mouse hippocampal neurons. This is 200-times faster than the clathrin-mediated process, and morphological characteristics rule out the 'kiss-and-run' model. This work suggests that rapid internalization of membrane from the surface is the first step in endocytosis.</description><subject>101/28</subject><subject>13/106</subject><subject>14</subject><subject>14/28</subject><subject>147/143</subject><subject>631/378/548/2588</subject><subject>631/378/548/2589</subject><subject>631/80/313/1461</subject><subject>631/80/313/1481</subject><subject>64/60</subject><subject>9/74</subject><subject>Actins - metabolism</subject><subject>Actins - ultrastructure</subject><subject>Action Potentials</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Dynamins - metabolism</subject><subject>Dynamins - ultrastructure</subject><subject>Electron microscopy</subject><subject>Endocytosis</subject><subject>Exocytosis</subject><subject>Experiments</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Hippocampus - cytology</subject><subject>Humanities and Social Sciences</subject><subject>Light</subject><subject>Membrane Fusion</subject><subject>Mice</subject><subject>Microscopy, Electron</subject><subject>multidisciplinary</subject><subject>Neural transmission</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Rhodopsin - genetics</subject><subject>Rhodopsin - metabolism</subject><subject>Science</subject><subject>Synapses</subject><subject>Synapses - metabolism</subject><subject>Synapses - ultrastructure</subject><subject>Synaptic Transmission</subject><subject>Synaptic Vesicles - metabolism</subject><subject>Synaptic Vesicles - ultrastructure</subject><subject>Time Factors</subject><subject>Vertebrates: nervous system and sense organs</subject><issn>0028-0836</issn><issn>1476-4687</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqF0l1r1EAUBuAgit1Wr7yXRSkomnrmK5O5EUrxo1AQ1F4Pk8nJdkoyk2YScf-9s-za7krA5CKQefLmzJmTZS8InBFg5QdvxmlAQktQj7IF4bLIeVHKx9kCgJY5lKw4yo5jvAUAQSR_mh1RzkCAEIuMXbfjYBoTxyX6Otj1GKKLSzMuuzBFXN64vg_WdL1pl3HtTR8xPsueNKaN-Hz3PMmuP3_6efE1v_r25fLi_Cq3hRRjXksuoBBCNQSJ4YWsBSsEpTUlTKKFqqmIpEpVVWmMUqmypq7rhlmsDa9UxU6yj9vcfqo6rC36VGqr-8F1ZljrYJw-XPHuRq_CL82UkIypFPBmFzCEuwnjqDsXLbat8Zh2p4kUTNCCgvw_5YWiZNOzRF__Q2_DNPjUiaQkgOIE6INamRa1801IJdpNqD5nIl2lhCKpfEat0GPaT_DYuPT6wL-a8bZ3d3ofnc2gdNfYOTub-vbgg2RG_D2uzBSjvvzx_dC-21o7hBgHbO7Pg4DezKPem8ekX-4f4b39O4AJnO6Aida0zWC8dfHBlcB5ySG591sX05Jf4bDX9Jn__gEznfQX</recordid><startdate>20131212</startdate><enddate>20131212</enddate><creator>Watanabe, Shigeki</creator><creator>Rost, Benjamin R.</creator><creator>Camacho-Pérez, Marcial</creator><creator>Davis, M. Wayne</creator><creator>Söhl-Kielczynski, Berit</creator><creator>Rosenmund, Christian</creator><creator>Jorgensen, Erik M.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>IQODW</scope><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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T5</scope><scope>7TG</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88G</scope><scope>88I</scope><scope>8AF</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BEC</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>MBDVC</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PCBAR</scope><scope>PDBOC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PSYQQ</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>Q9U</scope><scope>R05</scope><scope>RC3</scope><scope>S0X</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20131212</creationdate><title>Ultrafast endocytosis at mouse hippocampal synapses</title><author>Watanabe, Shigeki ; Rost, Benjamin R. ; Camacho-Pérez, Marcial ; Davis, M. Wayne ; Söhl-Kielczynski, Berit ; Rosenmund, Christian ; Jorgensen, Erik M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c675t-d74506559f1e1a467d536522d2137ec0bfb17299bb8aa99174fdddf3ceda4b9b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>101/28</topic><topic>13/106</topic><topic>14</topic><topic>14/28</topic><topic>147/143</topic><topic>631/378/548/2588</topic><topic>631/378/548/2589</topic><topic>631/80/313/1461</topic><topic>631/80/313/1481</topic><topic>64/60</topic><topic>9/74</topic><topic>Actins - metabolism</topic><topic>Actins - ultrastructure</topic><topic>Action Potentials</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Dynamins - metabolism</topic><topic>Dynamins - ultrastructure</topic><topic>Electron microscopy</topic><topic>Endocytosis</topic><topic>Exocytosis</topic><topic>Experiments</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Hippocampus - cytology</topic><topic>Humanities and Social Sciences</topic><topic>Light</topic><topic>Membrane Fusion</topic><topic>Mice</topic><topic>Microscopy, Electron</topic><topic>multidisciplinary</topic><topic>Neural transmission</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Rhodopsin - genetics</topic><topic>Rhodopsin - metabolism</topic><topic>Science</topic><topic>Synapses</topic><topic>Synapses - metabolism</topic><topic>Synapses - ultrastructure</topic><topic>Synaptic Transmission</topic><topic>Synaptic Vesicles - metabolism</topic><topic>Synaptic Vesicles - ultrastructure</topic><topic>Time Factors</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Watanabe, Shigeki</creatorcontrib><creatorcontrib>Rost, Benjamin R.</creatorcontrib><creatorcontrib>Camacho-Pérez, Marcial</creatorcontrib><creatorcontrib>Davis, M. Wayne</creatorcontrib><creatorcontrib>Söhl-Kielczynski, Berit</creatorcontrib><creatorcontrib>Rosenmund, Christian</creatorcontrib><creatorcontrib>Jorgensen, Erik M.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical 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>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>eLibrary</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Research Library</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Research Library (Corporate)</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Earth, Atmospheric & Aquatic Science Database</collection><collection>Materials Science Collection</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest One Psychology</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>ProQuest Central Basic</collection><collection>University of Michigan</collection><collection>Genetics Abstracts</collection><collection>SIRS Editorial</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Watanabe, Shigeki</au><au>Rost, Benjamin R.</au><au>Camacho-Pérez, Marcial</au><au>Davis, M. Wayne</au><au>Söhl-Kielczynski, Berit</au><au>Rosenmund, Christian</au><au>Jorgensen, Erik M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ultrafast endocytosis at mouse hippocampal synapses</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2013-12-12</date><risdate>2013</risdate><volume>504</volume><issue>7479</issue><spage>242</spage><epage>247</epage><pages>242-247</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><coden>NATUAS</coden><abstract>To sustain neurotransmission, synaptic vesicles and their associated proteins must be recycled locally at synapses. Synaptic vesicles are thought to be regenerated approximately 20 s after fusion by the assembly of clathrin scaffolds or in approximately 1 s by the reversal of fusion pores via ‘kiss-and-run’ endocytosis. Here we use optogenetics to stimulate cultured hippocampal neurons with a single stimulus, rapidly freeze them after fixed intervals and examine the ultrastructure using electron microscopy—‘flash-and-freeze’ electron microscopy. Docked vesicles fuse and collapse into the membrane within 30 ms of the stimulus. Compensatory endocytosis occurs within 50 to 100 ms at sites flanking the active zone. Invagination is blocked by inhibition of actin polymerization, and scission is blocked by inhibiting dynamin. Because intact synaptic vesicles are not recovered, this form of recycling is not compatible with kiss-and-run endocytosis; moreover, it is 200-fold faster than clathrin-mediated endocytosis. It is likely that ‘ultrafast endocytosis’ is specialized to restore the surface area of the membrane rapidly.
Sustained neurotransmission requires recycling of synaptic vesicles, but the proposed mechanisms have been controversial; here a ‘flash-and-freeze’ method for electron microscopy reveals a new ultrafast form of endocytosis that is actin- and dynamin-dependent and occurs within 100 milliseconds of stimulation.
A quick look at synaptic endocytosis
Sustained neurotransmission requires recycling of synaptic vesicles but the proposed mechanisms — clathrin-mediated endocytosis and 'kiss-and-run' reversal of fusion — have been controversial. Now Erik Jorgensen and colleagues, using ultrafast, 'flash-and-freeze' electron microscopy, have identified a previously unknown actin- and dynamin-dependent mechanism of endocytosis, occurring within 100 milliseconds of stimulation in mouse hippocampal neurons. This is 200-times faster than the clathrin-mediated process, and morphological characteristics rule out the 'kiss-and-run' model. This work suggests that rapid internalization of membrane from the surface is the first step in endocytosis.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>24305055</pmid><doi>10.1038/nature12809</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0028-0836 |
| ispartof | Nature (London), 2013-12, Vol.504 (7479), p.242-247 |
| issn | 0028-0836 1476-4687 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3957339 |
| source | MEDLINE; SpringerLink Journals; Nature |
| subjects | 101/28 13/106 14 14/28 147/143 631/378/548/2588 631/378/548/2589 631/80/313/1461 631/80/313/1481 64/60 9/74 Actins - metabolism Actins - ultrastructure Action Potentials Animals Biological and medical sciences Dynamins - metabolism Dynamins - ultrastructure Electron microscopy Endocytosis Exocytosis Experiments Fundamental and applied biological sciences. Psychology Hippocampus - cytology Humanities and Social Sciences Light Membrane Fusion Mice Microscopy, Electron multidisciplinary Neural transmission Physiological aspects Proteins Rhodopsin - genetics Rhodopsin - metabolism Science Synapses Synapses - metabolism Synapses - ultrastructure Synaptic Transmission Synaptic Vesicles - metabolism Synaptic Vesicles - ultrastructure Time Factors Vertebrates: nervous system and sense organs |
| title | Ultrafast endocytosis at mouse hippocampal synapses |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-03T07%3A45%3A11IST&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=Ultrafast%20endocytosis%20at%20mouse%20hippocampal%20synapses&rft.jtitle=Nature%20(London)&rft.au=Watanabe,%20Shigeki&rft.date=2013-12-12&rft.volume=504&rft.issue=7479&rft.spage=242&rft.epage=247&rft.pages=242-247&rft.issn=0028-0836&rft.eissn=1476-4687&rft.coden=NATUAS&rft_id=info:doi/10.1038/nature12809&rft_dat=%3Cgale_pubme%3EA355558706%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=1470094102&rft_id=info:pmid/24305055&rft_galeid=A355558706&rfr_iscdi=true |