Presynaptic HCN Channels Regulate Vesicular Glutamate Transport
The amount of neurotransmitter stored in synaptic vesicles determines postsynaptic quantal size and thus the strength of synaptic transmission. However, little is known about regulation of vesicular neurotransmitter uptake. In recordings from the calyx of Held, a giant mammalian glutamatergic synaps...
Gespeichert in:
| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2014-10, Vol.84 (2), p.340-346 |
|---|---|
| Hauptverfasser: | , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 346 |
|---|---|
| container_issue | 2 |
| container_start_page | 340 |
| container_title | Neuron (Cambridge, Mass.) |
| container_volume | 84 |
| creator | Huang, Hai Trussell, Laurence O. |
| description | The amount of neurotransmitter stored in synaptic vesicles determines postsynaptic quantal size and thus the strength of synaptic transmission. However, little is known about regulation of vesicular neurotransmitter uptake. In recordings from the calyx of Held, a giant mammalian glutamatergic synapse, we found that changes in presynaptic Na+ concentration above and below a resting value of 13 mM regulated vesicular glutamate uptake, consistent with activation of a vesicular monovalent cation Na+(K+)/H+ exchanger. Na+ flux through presynaptic plasma membrane hyperpolarization-activated cyclic nucleotide-gated (HCN) channels enhanced presynaptic Na+ concentration and thus controlled postsynaptic quantal size. Our results indicate that a plasma membrane ion channel controls synaptic strength by modulating vesicular neurotransmitter uptake through a Na+-dependent process.
•Sodium ions facilitate glutamate loading into synaptic vesicles•Plasma membrane HCN channel controls intraterminal sodium level•Change in HCN channel activity alters the content of synaptic vesicles
Loading synaptic vesicles with transmitter depends upon availability of intracellular cations. Here, Huang and Trussell show that glutamate loading into vesicles is regulated by Na+ levels set by Na+-permeable HCN channels in the presynaptic plasma membrane. |
| doi_str_mv | 10.1016/j.neuron.2014.08.046 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4254032</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0896627314007478</els_id><sourcerecordid>1629967326</sourcerecordid><originalsourceid>FETCH-LOGICAL-c524t-b2fa1192722388667b0fcc70fa1bb14ba81fd54a40ebda908eff526d1e985c683</originalsourceid><addsrcrecordid>eNqNkU9v1DAQxS0EosvCN0AoEhcuCWPHduwLqFpBi1QBQoWr5TiT1qusvdhJpX57vNpS_hwQJ1vjNzPP70fIcwoNBSpfb5uAS4qhYUB5A6oBLh-QFQXd1Zxq_ZCsQGlZS9a1J-RJzlsoQqHpY3LCBJNtJ9iKvP2cMN8Gu5-9q843H6vNtQ0Bp1x9watlsjNW3zB7V66pOpuW2e4OtctkQ97HND8lj0Y7ZXx2d67J1_fvLjfn9cWnsw-b04vaCcbnumejpVSzjrFWKSm7HkbnOijVvqe8t4qOg-CWA_aD1aBwHIvHgaJWwknVrsmb49z90u9wcBjmZCezT35n062J1ps_X4K_NlfxxnAmOLSsDHh1NyDF7wvm2ex8djhNNmBcsqGyFVAciu4_pExr2bUlwzV5-Zd0G5cUShIHFVDBQImi4keVSzHnhOO9bwrmANNszRGmOcA0oEyBWdpe_P7n-6af9H6FUnjhjcdksvMYHA4-oZvNEP2_N_wAybKyQw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1620152085</pqid></control><display><type>article</type><title>Presynaptic HCN Channels Regulate Vesicular Glutamate Transport</title><source>MEDLINE</source><source>Cell Press Free Archives</source><source>Access via ScienceDirect (Elsevier)</source><source>EZB-FREE-00999 freely available EZB journals</source><creator>Huang, Hai ; Trussell, Laurence O.</creator><creatorcontrib>Huang, Hai ; Trussell, Laurence O.</creatorcontrib><description>The amount of neurotransmitter stored in synaptic vesicles determines postsynaptic quantal size and thus the strength of synaptic transmission. However, little is known about regulation of vesicular neurotransmitter uptake. In recordings from the calyx of Held, a giant mammalian glutamatergic synapse, we found that changes in presynaptic Na+ concentration above and below a resting value of 13 mM regulated vesicular glutamate uptake, consistent with activation of a vesicular monovalent cation Na+(K+)/H+ exchanger. Na+ flux through presynaptic plasma membrane hyperpolarization-activated cyclic nucleotide-gated (HCN) channels enhanced presynaptic Na+ concentration and thus controlled postsynaptic quantal size. Our results indicate that a plasma membrane ion channel controls synaptic strength by modulating vesicular neurotransmitter uptake through a Na+-dependent process.
•Sodium ions facilitate glutamate loading into synaptic vesicles•Plasma membrane HCN channel controls intraterminal sodium level•Change in HCN channel activity alters the content of synaptic vesicles
Loading synaptic vesicles with transmitter depends upon availability of intracellular cations. Here, Huang and Trussell show that glutamate loading into vesicles is regulated by Na+ levels set by Na+-permeable HCN channels in the presynaptic plasma membrane.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2014.08.046</identifier><identifier>PMID: 25263752</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Biological Transport - physiology ; Calibration ; Cyclic Nucleotide-Gated Cation Channels - metabolism ; Excitatory Postsynaptic Potentials - physiology ; Experiments ; Glutamic Acid - metabolism ; Hemodialysis ; Neurotransmitter Agents - metabolism ; Patch-Clamp Techniques - methods ; Presynaptic Terminals - metabolism ; Rats, Wistar ; Rodents ; Synaptic Transmission - physiology ; Synaptic Vesicles - metabolism</subject><ispartof>Neuron (Cambridge, Mass.), 2014-10, Vol.84 (2), p.340-346</ispartof><rights>2014 Elsevier Inc.</rights><rights>Copyright © 2014 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Oct 22, 2014</rights><rights>2014 Elsevier Inc. All rights reserved 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c524t-b2fa1192722388667b0fcc70fa1bb14ba81fd54a40ebda908eff526d1e985c683</citedby><cites>FETCH-LOGICAL-c524t-b2fa1192722388667b0fcc70fa1bb14ba81fd54a40ebda908eff526d1e985c683</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuron.2014.08.046$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25263752$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Huang, Hai</creatorcontrib><creatorcontrib>Trussell, Laurence O.</creatorcontrib><title>Presynaptic HCN Channels Regulate Vesicular Glutamate Transport</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>The amount of neurotransmitter stored in synaptic vesicles determines postsynaptic quantal size and thus the strength of synaptic transmission. However, little is known about regulation of vesicular neurotransmitter uptake. In recordings from the calyx of Held, a giant mammalian glutamatergic synapse, we found that changes in presynaptic Na+ concentration above and below a resting value of 13 mM regulated vesicular glutamate uptake, consistent with activation of a vesicular monovalent cation Na+(K+)/H+ exchanger. Na+ flux through presynaptic plasma membrane hyperpolarization-activated cyclic nucleotide-gated (HCN) channels enhanced presynaptic Na+ concentration and thus controlled postsynaptic quantal size. Our results indicate that a plasma membrane ion channel controls synaptic strength by modulating vesicular neurotransmitter uptake through a Na+-dependent process.
•Sodium ions facilitate glutamate loading into synaptic vesicles•Plasma membrane HCN channel controls intraterminal sodium level•Change in HCN channel activity alters the content of synaptic vesicles
Loading synaptic vesicles with transmitter depends upon availability of intracellular cations. Here, Huang and Trussell show that glutamate loading into vesicles is regulated by Na+ levels set by Na+-permeable HCN channels in the presynaptic plasma membrane.</description><subject>Animals</subject><subject>Biological Transport - physiology</subject><subject>Calibration</subject><subject>Cyclic Nucleotide-Gated Cation Channels - metabolism</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>Experiments</subject><subject>Glutamic Acid - metabolism</subject><subject>Hemodialysis</subject><subject>Neurotransmitter Agents - metabolism</subject><subject>Patch-Clamp Techniques - methods</subject><subject>Presynaptic Terminals - metabolism</subject><subject>Rats, Wistar</subject><subject>Rodents</subject><subject>Synaptic Transmission - physiology</subject><subject>Synaptic Vesicles - metabolism</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU9v1DAQxS0EosvCN0AoEhcuCWPHduwLqFpBi1QBQoWr5TiT1qusvdhJpX57vNpS_hwQJ1vjNzPP70fIcwoNBSpfb5uAS4qhYUB5A6oBLh-QFQXd1Zxq_ZCsQGlZS9a1J-RJzlsoQqHpY3LCBJNtJ9iKvP2cMN8Gu5-9q843H6vNtQ0Bp1x9watlsjNW3zB7V66pOpuW2e4OtctkQ97HND8lj0Y7ZXx2d67J1_fvLjfn9cWnsw-b04vaCcbnumejpVSzjrFWKSm7HkbnOijVvqe8t4qOg-CWA_aD1aBwHIvHgaJWwknVrsmb49z90u9wcBjmZCezT35n062J1ps_X4K_NlfxxnAmOLSsDHh1NyDF7wvm2ex8djhNNmBcsqGyFVAciu4_pExr2bUlwzV5-Zd0G5cUShIHFVDBQImi4keVSzHnhOO9bwrmANNszRGmOcA0oEyBWdpe_P7n-6af9H6FUnjhjcdksvMYHA4-oZvNEP2_N_wAybKyQw</recordid><startdate>20141022</startdate><enddate>20141022</enddate><creator>Huang, Hai</creator><creator>Trussell, Laurence O.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20141022</creationdate><title>Presynaptic HCN Channels Regulate Vesicular Glutamate Transport</title><author>Huang, Hai ; Trussell, Laurence O.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c524t-b2fa1192722388667b0fcc70fa1bb14ba81fd54a40ebda908eff526d1e985c683</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Biological Transport - physiology</topic><topic>Calibration</topic><topic>Cyclic Nucleotide-Gated Cation Channels - metabolism</topic><topic>Excitatory Postsynaptic Potentials - physiology</topic><topic>Experiments</topic><topic>Glutamic Acid - metabolism</topic><topic>Hemodialysis</topic><topic>Neurotransmitter Agents - metabolism</topic><topic>Patch-Clamp Techniques - methods</topic><topic>Presynaptic Terminals - metabolism</topic><topic>Rats, Wistar</topic><topic>Rodents</topic><topic>Synaptic Transmission - physiology</topic><topic>Synaptic Vesicles - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Huang, Hai</creatorcontrib><creatorcontrib>Trussell, Laurence O.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Huang, Hai</au><au>Trussell, Laurence O.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Presynaptic HCN Channels Regulate Vesicular Glutamate Transport</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2014-10-22</date><risdate>2014</risdate><volume>84</volume><issue>2</issue><spage>340</spage><epage>346</epage><pages>340-346</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>The amount of neurotransmitter stored in synaptic vesicles determines postsynaptic quantal size and thus the strength of synaptic transmission. However, little is known about regulation of vesicular neurotransmitter uptake. In recordings from the calyx of Held, a giant mammalian glutamatergic synapse, we found that changes in presynaptic Na+ concentration above and below a resting value of 13 mM regulated vesicular glutamate uptake, consistent with activation of a vesicular monovalent cation Na+(K+)/H+ exchanger. Na+ flux through presynaptic plasma membrane hyperpolarization-activated cyclic nucleotide-gated (HCN) channels enhanced presynaptic Na+ concentration and thus controlled postsynaptic quantal size. Our results indicate that a plasma membrane ion channel controls synaptic strength by modulating vesicular neurotransmitter uptake through a Na+-dependent process.
•Sodium ions facilitate glutamate loading into synaptic vesicles•Plasma membrane HCN channel controls intraterminal sodium level•Change in HCN channel activity alters the content of synaptic vesicles
Loading synaptic vesicles with transmitter depends upon availability of intracellular cations. Here, Huang and Trussell show that glutamate loading into vesicles is regulated by Na+ levels set by Na+-permeable HCN channels in the presynaptic plasma membrane.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25263752</pmid><doi>10.1016/j.neuron.2014.08.046</doi><tpages>7</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0896-6273 |
| ispartof | Neuron (Cambridge, Mass.), 2014-10, Vol.84 (2), p.340-346 |
| issn | 0896-6273 1097-4199 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4254032 |
| source | MEDLINE; Cell Press Free Archives; Access via ScienceDirect (Elsevier); EZB-FREE-00999 freely available EZB journals |
| subjects | Animals Biological Transport - physiology Calibration Cyclic Nucleotide-Gated Cation Channels - metabolism Excitatory Postsynaptic Potentials - physiology Experiments Glutamic Acid - metabolism Hemodialysis Neurotransmitter Agents - metabolism Patch-Clamp Techniques - methods Presynaptic Terminals - metabolism Rats, Wistar Rodents Synaptic Transmission - physiology Synaptic Vesicles - metabolism |
| title | Presynaptic HCN Channels Regulate Vesicular Glutamate Transport |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-22T20%3A26%3A26IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Presynaptic%20HCN%20Channels%20Regulate%20Vesicular%20Glutamate%20Transport&rft.jtitle=Neuron%20(Cambridge,%20Mass.)&rft.au=Huang,%20Hai&rft.date=2014-10-22&rft.volume=84&rft.issue=2&rft.spage=340&rft.epage=346&rft.pages=340-346&rft.issn=0896-6273&rft.eissn=1097-4199&rft_id=info:doi/10.1016/j.neuron.2014.08.046&rft_dat=%3Cproquest_pubme%3E1629967326%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1620152085&rft_id=info:pmid/25263752&rft_els_id=S0896627314007478&rfr_iscdi=true |