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Properties of ribbon and non-ribbon release from rod photoreceptors revealed by visualizing individual synaptic vesicles
Vesicle release from rod photoreceptors is regulated by Ca(2+) entry through L-type channels located near synaptic ribbons. We characterized sites and kinetics of vesicle release in salamander rods by using total internal reflection fluorescence microscopy to visualize fusion of individual synaptic...
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Published in: | The Journal of neuroscience 2013-01, Vol.33 (5), p.2071-2086 |
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description | Vesicle release from rod photoreceptors is regulated by Ca(2+) entry through L-type channels located near synaptic ribbons. We characterized sites and kinetics of vesicle release in salamander rods by using total internal reflection fluorescence microscopy to visualize fusion of individual synaptic vesicles. A small number of vesicles were loaded by brief incubation with FM1-43 or a dextran-conjugated, pH-sensitive form of rhodamine, pHrodo. Labeled organelles matched the diffraction-limited size of fluorescent microspheres and disappeared rapidly during stimulation. Consistent with fusion, depolarization-evoked vesicle disappearance paralleled electrophysiological release kinetics and was blocked by inhibiting Ca(2+) influx. Rods maintained tonic release at resting membrane potentials near those in darkness, causing depletion of membrane-associated vesicles unless Ca(2+) entry was inhibited. This depletion of release sites implies that sustained release may be rate limited by vesicle delivery. During depolarizing stimulation, newly appearing vesicles approached the membrane at ∼800 nm/s, where they paused for ∼60 ms before fusion. With fusion, vesicles advanced ∼18 nm closer to the membrane. Release events were concentrated near ribbons, but lengthy depolarization also triggered release from more distant non-ribbon sites. Consistent with greater contributions from non-ribbon sites during lengthier depolarization, damaging the ribbon by fluorophore-assisted laser inactivation (FALI) of Ribeye caused only weak inhibition of exocytotic capacitance increases evoked by 200-ms depolarizing test steps, whereas FALI more strongly inhibited capacitance increases evoked by 25 ms steps. Amplifying release by use of non-ribbon sites when rods are depolarized in darkness may improve detection of decrements in release when they hyperpolarize to light. |
doi_str_mv | 10.1523/jneurosci.3426-12.2013 |
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We characterized sites and kinetics of vesicle release in salamander rods by using total internal reflection fluorescence microscopy to visualize fusion of individual synaptic vesicles. A small number of vesicles were loaded by brief incubation with FM1-43 or a dextran-conjugated, pH-sensitive form of rhodamine, pHrodo. Labeled organelles matched the diffraction-limited size of fluorescent microspheres and disappeared rapidly during stimulation. Consistent with fusion, depolarization-evoked vesicle disappearance paralleled electrophysiological release kinetics and was blocked by inhibiting Ca(2+) influx. Rods maintained tonic release at resting membrane potentials near those in darkness, causing depletion of membrane-associated vesicles unless Ca(2+) entry was inhibited. This depletion of release sites implies that sustained release may be rate limited by vesicle delivery. During depolarizing stimulation, newly appearing vesicles approached the membrane at ∼800 nm/s, where they paused for ∼60 ms before fusion. With fusion, vesicles advanced ∼18 nm closer to the membrane. Release events were concentrated near ribbons, but lengthy depolarization also triggered release from more distant non-ribbon sites. Consistent with greater contributions from non-ribbon sites during lengthier depolarization, damaging the ribbon by fluorophore-assisted laser inactivation (FALI) of Ribeye caused only weak inhibition of exocytotic capacitance increases evoked by 200-ms depolarizing test steps, whereas FALI more strongly inhibited capacitance increases evoked by 25 ms steps. Amplifying release by use of non-ribbon sites when rods are depolarized in darkness may improve detection of decrements in release when they hyperpolarize to light.</description><identifier>ISSN: 0270-6474</identifier><identifier>ISSN: 1529-2401</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/jneurosci.3426-12.2013</identifier><identifier>PMID: 23365244</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Animals ; Caudata ; Electric Capacitance ; Female ; Male ; Presynaptic Terminals - physiology ; Retina - physiology ; Retinal Cone Photoreceptor Cells - physiology ; Retinal Rod Photoreceptor Cells - physiology ; Synapses - physiology ; Synaptic Vesicles - physiology ; Urodela</subject><ispartof>The Journal of neuroscience, 2013-01, Vol.33 (5), p.2071-2086</ispartof><rights>Copyright © 2013 the authors 0270-6474/13/332071-16$15.00/0 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c599t-67e1376bb7e44abe5643277e5ec19e371b0032d2c3bb7ec3c151d2bae9f1995b3</citedby><cites>FETCH-LOGICAL-c599t-67e1376bb7e44abe5643277e5ec19e371b0032d2c3bb7ec3c151d2bae9f1995b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3689321/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3689321/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,53827,53829</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23365244$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Minghui</creatorcontrib><creatorcontrib>Van Hook, Matthew J</creatorcontrib><creatorcontrib>Zenisek, David</creatorcontrib><creatorcontrib>Thoreson, Wallace B</creatorcontrib><title>Properties of ribbon and non-ribbon release from rod photoreceptors revealed by visualizing individual synaptic vesicles</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Vesicle release from rod photoreceptors is regulated by Ca(2+) entry through L-type channels located near synaptic ribbons. We characterized sites and kinetics of vesicle release in salamander rods by using total internal reflection fluorescence microscopy to visualize fusion of individual synaptic vesicles. A small number of vesicles were loaded by brief incubation with FM1-43 or a dextran-conjugated, pH-sensitive form of rhodamine, pHrodo. Labeled organelles matched the diffraction-limited size of fluorescent microspheres and disappeared rapidly during stimulation. Consistent with fusion, depolarization-evoked vesicle disappearance paralleled electrophysiological release kinetics and was blocked by inhibiting Ca(2+) influx. Rods maintained tonic release at resting membrane potentials near those in darkness, causing depletion of membrane-associated vesicles unless Ca(2+) entry was inhibited. This depletion of release sites implies that sustained release may be rate limited by vesicle delivery. During depolarizing stimulation, newly appearing vesicles approached the membrane at ∼800 nm/s, where they paused for ∼60 ms before fusion. With fusion, vesicles advanced ∼18 nm closer to the membrane. Release events were concentrated near ribbons, but lengthy depolarization also triggered release from more distant non-ribbon sites. Consistent with greater contributions from non-ribbon sites during lengthier depolarization, damaging the ribbon by fluorophore-assisted laser inactivation (FALI) of Ribeye caused only weak inhibition of exocytotic capacitance increases evoked by 200-ms depolarizing test steps, whereas FALI more strongly inhibited capacitance increases evoked by 25 ms steps. Amplifying release by use of non-ribbon sites when rods are depolarized in darkness may improve detection of decrements in release when they hyperpolarize to light.</description><subject>Animals</subject><subject>Caudata</subject><subject>Electric Capacitance</subject><subject>Female</subject><subject>Male</subject><subject>Presynaptic Terminals - physiology</subject><subject>Retina - physiology</subject><subject>Retinal Cone Photoreceptor Cells - physiology</subject><subject>Retinal Rod Photoreceptor Cells - physiology</subject><subject>Synapses - physiology</subject><subject>Synaptic Vesicles - physiology</subject><subject>Urodela</subject><issn>0270-6474</issn><issn>1529-2401</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqNUk1v1DAQtRAVXQp_ofKRSxZ_O7kgoVULRRWtWnq2bGfSusrawU4ill9PVl0quPU0Gr0Pzeg9hE4pWVPJ-MfHCFNOxYc1F0xVlK0ZofwVWi1oUzFB6Gu0IkyTSgktjtHbUh4JIZpQ_QYdM86VZEKs0K_rnAbIY4CCU4dzcC5FbGOLY4rVYc3Qgy2Au5y2OKcWDw9pTBk8DMsoCz6D7aHFbofnUCbbh98h3uMQ2zCHdtlx2UU7jMHjGUrwPZR36KizfYH3h3mC7s7Pfmy-VpdXXy42ny8rL5tmrJQGyrVyToMQ1oFUgjOtQYKnDXBNHSGctczzPcVzTyVtmbPQdLRppOMn6NOT7zC5LbQe4phtb4YctjbvTLLB_I_E8GDu02y4qhvO6GLw4WCQ088Jymi2oXjoexshTcVQKaliijUvoQpdS0Ze4spqrjmpSb1Q1RPVL4GXDN3z8ZSYfRnMt-9ndzdXt5sLsy_DojX7MizC039ff5b9TZ__AZPCtag</recordid><startdate>20130130</startdate><enddate>20130130</enddate><creator>Chen, Minghui</creator><creator>Van Hook, Matthew J</creator><creator>Zenisek, David</creator><creator>Thoreson, Wallace B</creator><general>Society for Neuroscience</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>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>7TK</scope><scope>5PM</scope></search><sort><creationdate>20130130</creationdate><title>Properties of ribbon and non-ribbon release from rod photoreceptors revealed by visualizing individual synaptic vesicles</title><author>Chen, Minghui ; Van Hook, Matthew J ; Zenisek, David ; Thoreson, Wallace B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c599t-67e1376bb7e44abe5643277e5ec19e371b0032d2c3bb7ec3c151d2bae9f1995b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Caudata</topic><topic>Electric Capacitance</topic><topic>Female</topic><topic>Male</topic><topic>Presynaptic Terminals - physiology</topic><topic>Retina - physiology</topic><topic>Retinal Cone Photoreceptor Cells - physiology</topic><topic>Retinal Rod Photoreceptor Cells - physiology</topic><topic>Synapses - physiology</topic><topic>Synaptic Vesicles - physiology</topic><topic>Urodela</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Minghui</creatorcontrib><creatorcontrib>Van Hook, Matthew J</creatorcontrib><creatorcontrib>Zenisek, David</creatorcontrib><creatorcontrib>Thoreson, Wallace B</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Minghui</au><au>Van Hook, Matthew J</au><au>Zenisek, David</au><au>Thoreson, Wallace B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Properties of ribbon and non-ribbon release from rod photoreceptors revealed by visualizing individual synaptic vesicles</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2013-01-30</date><risdate>2013</risdate><volume>33</volume><issue>5</issue><spage>2071</spage><epage>2086</epage><pages>2071-2086</pages><issn>0270-6474</issn><issn>1529-2401</issn><eissn>1529-2401</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Author contributions: M.C., D.Z., and W.B.T. designed research; M.C., M.J.V.H., and W.B.T. performed research; M.C., M.J.V.H., D.Z., and W.B.T. analyzed data; M.C. and W.B.T. wrote the paper.</notes><abstract>Vesicle release from rod photoreceptors is regulated by Ca(2+) entry through L-type channels located near synaptic ribbons. We characterized sites and kinetics of vesicle release in salamander rods by using total internal reflection fluorescence microscopy to visualize fusion of individual synaptic vesicles. A small number of vesicles were loaded by brief incubation with FM1-43 or a dextran-conjugated, pH-sensitive form of rhodamine, pHrodo. Labeled organelles matched the diffraction-limited size of fluorescent microspheres and disappeared rapidly during stimulation. Consistent with fusion, depolarization-evoked vesicle disappearance paralleled electrophysiological release kinetics and was blocked by inhibiting Ca(2+) influx. Rods maintained tonic release at resting membrane potentials near those in darkness, causing depletion of membrane-associated vesicles unless Ca(2+) entry was inhibited. This depletion of release sites implies that sustained release may be rate limited by vesicle delivery. During depolarizing stimulation, newly appearing vesicles approached the membrane at ∼800 nm/s, where they paused for ∼60 ms before fusion. With fusion, vesicles advanced ∼18 nm closer to the membrane. Release events were concentrated near ribbons, but lengthy depolarization also triggered release from more distant non-ribbon sites. Consistent with greater contributions from non-ribbon sites during lengthier depolarization, damaging the ribbon by fluorophore-assisted laser inactivation (FALI) of Ribeye caused only weak inhibition of exocytotic capacitance increases evoked by 200-ms depolarizing test steps, whereas FALI more strongly inhibited capacitance increases evoked by 25 ms steps. Amplifying release by use of non-ribbon sites when rods are depolarized in darkness may improve detection of decrements in release when they hyperpolarize to light.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>23365244</pmid><doi>10.1523/jneurosci.3426-12.2013</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Caudata Electric Capacitance Female Male Presynaptic Terminals - physiology Retina - physiology Retinal Cone Photoreceptor Cells - physiology Retinal Rod Photoreceptor Cells - physiology Synapses - physiology Synaptic Vesicles - physiology Urodela |
title | Properties of ribbon and non-ribbon release from rod photoreceptors revealed by visualizing individual synaptic vesicles |
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