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High-resolution electron cryomicroscopy of V-ATPase in native synaptic vesicles
Intercellular communication in the nervous system occurs through the release of neurotransmitters into the synaptic cleft between neurons. In the presynaptic neuron, the proton pumping vesicular- or vacuolar-type ATPase (V-ATPase) powers neurotransmitter loading into synaptic vesicles (SVs), with th...
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| Published in: | Science (American Association for the Advancement of Science) 2024-07, Vol.385 (6705), p.168-174 |
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| creator | Coupland, Claire E. Karimi, Ryan Bueler, Stephanie A. Liang, Yingke Courbon, Gautier M. Di Trani, Justin M. Wong, Cassandra J. Saghian, Rayan Youn, Ji-Young Wang, Lu-Yang Rubinstein, John L. |
| description | Intercellular communication in the nervous system occurs through the release of neurotransmitters into the synaptic cleft between neurons. In the presynaptic neuron, the proton pumping vesicular- or vacuolar-type ATPase (V-ATPase) powers neurotransmitter loading into synaptic vesicles (SVs), with the V 1 complex dissociating from the membrane region of the enzyme before exocytosis. We isolated SVs from rat brain using SidK, a V-ATPase–binding bacterial effector protein. Single-particle electron cryomicroscopy allowed high-resolution structure determination of V-ATPase within the native SV membrane. In the structure, regularly spaced cholesterol molecules decorate the enzyme’s rotor and the abundant SV protein synaptophysin binds the complex stoichiometrically. ATP hydrolysis during vesicle loading results in a loss of the V 1 region of V-ATPase from the SV membrane, suggesting that loading is sufficient to induce dissociation of the enzyme.
Editor’s summary Chemical communication between neurons involves the rapid release of neurotransmitters into the synapse. Vesicular-type ATPase (V-ATPase) uses ATP to pump protons into synaptic vesicles, enabling neurotransmitter uptake from the cytosol before release. Coupland et al . isolated whole synaptic vesicles from rat brain and were able to determine high-resolution electron cryomicroscopy structures of the V-ATPase in its native membrane. The authors found several unexpected features that were not seen in structures of purified V-ATPase, including a stoichiometric complex with the protein synaptophysin. They also observed dissociation of the V1 head group under active conditions, consistent with prior biochemical work. —Michael A. Funk |
| doi_str_mv | 10.1126/science.adp5577 |
| format | article |
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Editor’s summary Chemical communication between neurons involves the rapid release of neurotransmitters into the synapse. Vesicular-type ATPase (V-ATPase) uses ATP to pump protons into synaptic vesicles, enabling neurotransmitter uptake from the cytosol before release. Coupland et al . isolated whole synaptic vesicles from rat brain and were able to determine high-resolution electron cryomicroscopy structures of the V-ATPase in its native membrane. The authors found several unexpected features that were not seen in structures of purified V-ATPase, including a stoichiometric complex with the protein synaptophysin. They also observed dissociation of the V1 head group under active conditions, consistent with prior biochemical work. —Michael A. Funk</description><identifier>ISSN: 0036-8075</identifier><identifier>ISSN: 1095-9203</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.adp5577</identifier><language>eng</language><publisher>Washington: The American Association for the Advancement of Science</publisher><subject>Adenosine triphosphatase ; Chemical communication ; Cytosol ; H+-transporting ATPase ; High resolution ; Membrane proteins ; Membrane vesicles ; Neurotransmitters ; Protons ; Synaptic vesicles ; Synaptophysin ; Vesicles</subject><ispartof>Science (American Association for the Advancement of Science), 2024-07, Vol.385 (6705), p.168-174</ispartof><rights>Copyright © 2024 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c1014-2d2bba7c87d6e60ebcf076d133311b4f442b15538c4264f5ac29cadc4a7a80ee3</cites><orcidid>0000-0003-2300-4824 ; 0009-0000-3726-7014 ; 0000-0002-5399-944X ; 0009-0009-7292-3780 ; 0000-0002-6041-7532 ; 0000-0001-6799-5709 ; 0000-0001-6628-9087 ; 0000-0001-6247-8294 ; 0000-0003-0566-2209</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,2902,2903,27957,27958</link.rule.ids></links><search><creatorcontrib>Coupland, Claire E.</creatorcontrib><creatorcontrib>Karimi, Ryan</creatorcontrib><creatorcontrib>Bueler, Stephanie A.</creatorcontrib><creatorcontrib>Liang, Yingke</creatorcontrib><creatorcontrib>Courbon, Gautier M.</creatorcontrib><creatorcontrib>Di Trani, Justin M.</creatorcontrib><creatorcontrib>Wong, Cassandra J.</creatorcontrib><creatorcontrib>Saghian, Rayan</creatorcontrib><creatorcontrib>Youn, Ji-Young</creatorcontrib><creatorcontrib>Wang, Lu-Yang</creatorcontrib><creatorcontrib>Rubinstein, John L.</creatorcontrib><title>High-resolution electron cryomicroscopy of V-ATPase in native synaptic vesicles</title><title>Science (American Association for the Advancement of Science)</title><description>Intercellular communication in the nervous system occurs through the release of neurotransmitters into the synaptic cleft between neurons. In the presynaptic neuron, the proton pumping vesicular- or vacuolar-type ATPase (V-ATPase) powers neurotransmitter loading into synaptic vesicles (SVs), with the V 1 complex dissociating from the membrane region of the enzyme before exocytosis. We isolated SVs from rat brain using SidK, a V-ATPase–binding bacterial effector protein. Single-particle electron cryomicroscopy allowed high-resolution structure determination of V-ATPase within the native SV membrane. In the structure, regularly spaced cholesterol molecules decorate the enzyme’s rotor and the abundant SV protein synaptophysin binds the complex stoichiometrically. ATP hydrolysis during vesicle loading results in a loss of the V 1 region of V-ATPase from the SV membrane, suggesting that loading is sufficient to induce dissociation of the enzyme.
Editor’s summary Chemical communication between neurons involves the rapid release of neurotransmitters into the synapse. Vesicular-type ATPase (V-ATPase) uses ATP to pump protons into synaptic vesicles, enabling neurotransmitter uptake from the cytosol before release. Coupland et al . isolated whole synaptic vesicles from rat brain and were able to determine high-resolution electron cryomicroscopy structures of the V-ATPase in its native membrane. The authors found several unexpected features that were not seen in structures of purified V-ATPase, including a stoichiometric complex with the protein synaptophysin. They also observed dissociation of the V1 head group under active conditions, consistent with prior biochemical work. —Michael A. Funk</description><subject>Adenosine triphosphatase</subject><subject>Chemical communication</subject><subject>Cytosol</subject><subject>H+-transporting ATPase</subject><subject>High resolution</subject><subject>Membrane proteins</subject><subject>Membrane vesicles</subject><subject>Neurotransmitters</subject><subject>Protons</subject><subject>Synaptic vesicles</subject><subject>Synaptophysin</subject><subject>Vesicles</subject><issn>0036-8075</issn><issn>1095-9203</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNpdkE1Lw0AQhhdRsFbPXgNevKTdr-xujqWoFQr1UL2GzWSiW9Js3E0L-femtCdPMzAPw_s-hDwyOmOMq3kEhy3gzFZdlml9RSaM5lmacyquyYRSoVJDdXZL7mLcUTrecjEhm5X7_kkDRt8ceufbBBuEPowLhMHvHQQfwXdD4uvkK11sP2zExLVJa3t3xCQOre16B8kRo4MG4z25qW0T8eEyp-Tz9WW7XKXrzdv7crFOgVEmU17xsrQajK4UKool1FSrigkhGCtlLSUvWZYJA5IrWWcWeA62Amm1NRRRTMnz-W8X_O8BY1_sXQRsGtuiP8RCUE2NMEbJEX36h-78IbRjuhNllDKcZyM1P1OnxjFgXXTB7W0YCkaLk-DiIri4CBZ_NGdxNQ</recordid><startdate>20240712</startdate><enddate>20240712</enddate><creator>Coupland, Claire E.</creator><creator>Karimi, Ryan</creator><creator>Bueler, Stephanie A.</creator><creator>Liang, Yingke</creator><creator>Courbon, Gautier M.</creator><creator>Di Trani, Justin M.</creator><creator>Wong, Cassandra J.</creator><creator>Saghian, Rayan</creator><creator>Youn, Ji-Young</creator><creator>Wang, Lu-Yang</creator><creator>Rubinstein, John L.</creator><general>The American Association for the Advancement of Science</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-2300-4824</orcidid><orcidid>https://orcid.org/0009-0000-3726-7014</orcidid><orcidid>https://orcid.org/0000-0002-5399-944X</orcidid><orcidid>https://orcid.org/0009-0009-7292-3780</orcidid><orcidid>https://orcid.org/0000-0002-6041-7532</orcidid><orcidid>https://orcid.org/0000-0001-6799-5709</orcidid><orcidid>https://orcid.org/0000-0001-6628-9087</orcidid><orcidid>https://orcid.org/0000-0001-6247-8294</orcidid><orcidid>https://orcid.org/0000-0003-0566-2209</orcidid></search><sort><creationdate>20240712</creationdate><title>High-resolution electron cryomicroscopy of V-ATPase in native synaptic vesicles</title><author>Coupland, Claire E. ; Karimi, Ryan ; Bueler, Stephanie A. ; Liang, Yingke ; Courbon, Gautier M. ; Di Trani, Justin M. ; Wong, Cassandra J. ; Saghian, Rayan ; Youn, Ji-Young ; Wang, Lu-Yang ; Rubinstein, John L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c1014-2d2bba7c87d6e60ebcf076d133311b4f442b15538c4264f5ac29cadc4a7a80ee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adenosine triphosphatase</topic><topic>Chemical communication</topic><topic>Cytosol</topic><topic>H+-transporting ATPase</topic><topic>High resolution</topic><topic>Membrane proteins</topic><topic>Membrane vesicles</topic><topic>Neurotransmitters</topic><topic>Protons</topic><topic>Synaptic vesicles</topic><topic>Synaptophysin</topic><topic>Vesicles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Coupland, Claire E.</creatorcontrib><creatorcontrib>Karimi, Ryan</creatorcontrib><creatorcontrib>Bueler, Stephanie A.</creatorcontrib><creatorcontrib>Liang, Yingke</creatorcontrib><creatorcontrib>Courbon, Gautier M.</creatorcontrib><creatorcontrib>Di Trani, Justin M.</creatorcontrib><creatorcontrib>Wong, Cassandra J.</creatorcontrib><creatorcontrib>Saghian, Rayan</creatorcontrib><creatorcontrib>Youn, Ji-Young</creatorcontrib><creatorcontrib>Wang, Lu-Yang</creatorcontrib><creatorcontrib>Rubinstein, John L.</creatorcontrib><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Coupland, Claire E.</au><au>Karimi, Ryan</au><au>Bueler, Stephanie A.</au><au>Liang, Yingke</au><au>Courbon, Gautier M.</au><au>Di Trani, Justin M.</au><au>Wong, Cassandra J.</au><au>Saghian, Rayan</au><au>Youn, Ji-Young</au><au>Wang, Lu-Yang</au><au>Rubinstein, John L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>High-resolution electron cryomicroscopy of V-ATPase in native synaptic vesicles</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><date>2024-07-12</date><risdate>2024</risdate><volume>385</volume><issue>6705</issue><spage>168</spage><epage>174</epage><pages>168-174</pages><issn>0036-8075</issn><issn>1095-9203</issn><eissn>1095-9203</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Intercellular communication in the nervous system occurs through the release of neurotransmitters into the synaptic cleft between neurons. In the presynaptic neuron, the proton pumping vesicular- or vacuolar-type ATPase (V-ATPase) powers neurotransmitter loading into synaptic vesicles (SVs), with the V 1 complex dissociating from the membrane region of the enzyme before exocytosis. We isolated SVs from rat brain using SidK, a V-ATPase–binding bacterial effector protein. Single-particle electron cryomicroscopy allowed high-resolution structure determination of V-ATPase within the native SV membrane. In the structure, regularly spaced cholesterol molecules decorate the enzyme’s rotor and the abundant SV protein synaptophysin binds the complex stoichiometrically. ATP hydrolysis during vesicle loading results in a loss of the V 1 region of V-ATPase from the SV membrane, suggesting that loading is sufficient to induce dissociation of the enzyme.
Editor’s summary Chemical communication between neurons involves the rapid release of neurotransmitters into the synapse. Vesicular-type ATPase (V-ATPase) uses ATP to pump protons into synaptic vesicles, enabling neurotransmitter uptake from the cytosol before release. Coupland et al . isolated whole synaptic vesicles from rat brain and were able to determine high-resolution electron cryomicroscopy structures of the V-ATPase in its native membrane. The authors found several unexpected features that were not seen in structures of purified V-ATPase, including a stoichiometric complex with the protein synaptophysin. They also observed dissociation of the V1 head group under active conditions, consistent with prior biochemical work. —Michael A. Funk</abstract><cop>Washington</cop><pub>The American Association for the Advancement of Science</pub><doi>10.1126/science.adp5577</doi><tpages>7</tpages><orcidid>https://orcid.org/0000-0003-2300-4824</orcidid><orcidid>https://orcid.org/0009-0000-3726-7014</orcidid><orcidid>https://orcid.org/0000-0002-5399-944X</orcidid><orcidid>https://orcid.org/0009-0009-7292-3780</orcidid><orcidid>https://orcid.org/0000-0002-6041-7532</orcidid><orcidid>https://orcid.org/0000-0001-6799-5709</orcidid><orcidid>https://orcid.org/0000-0001-6628-9087</orcidid><orcidid>https://orcid.org/0000-0001-6247-8294</orcidid><orcidid>https://orcid.org/0000-0003-0566-2209</orcidid></addata></record> |
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| subjects | Adenosine triphosphatase Chemical communication Cytosol H+-transporting ATPase High resolution Membrane proteins Membrane vesicles Neurotransmitters Protons Synaptic vesicles Synaptophysin Vesicles |
| title | High-resolution electron cryomicroscopy of V-ATPase in native synaptic vesicles |
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