A genetic survey of fluoxetine action on synaptic transmission in Caenorhabditis elegans
Fluoxetine is one of the most commonly prescribed medications for many behavioral and neurological disorders. Fluoxetine acts primarily as an inhibitor of the serotonin reuptake transporter (SERT) to block the removal of serotonin from the synaptic cleft, thereby enhancing serotonin signals. While t...
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| Veröffentlicht in: | Genetics (Austin) 2010-11, Vol.186 (3), p.929-941 |
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| creator | Kullyev, Andrey Dempsey, Catherine M Miller, Sarah Kuan, Chih-Jen Hapiak, Vera M Komuniecki, Richard W Griffin, Christine T Sze, Ji Ying |
| description | Fluoxetine is one of the most commonly prescribed medications for many behavioral and neurological disorders. Fluoxetine acts primarily as an inhibitor of the serotonin reuptake transporter (SERT) to block the removal of serotonin from the synaptic cleft, thereby enhancing serotonin signals. While the effects of fluoxetine on behavior are firmly established, debate is ongoing whether inhibition of serotonin reuptake is a sufficient explanation for its therapeutic action. Here, we provide evidence of two additional aspects of fluoxetine action through genetic analyses in Caenorhabditis elegans. We show that fluoxetine treatment and null mutation in the sole SERT gene mod-5 eliminate serotonin in specific neurons. These neurons do not synthesize serotonin but import extracellular serotonin via MOD-5/SERT. Furthermore, we show that fluoxetine acts independently of MOD-5/SERT to regulate discrete properties of acetylcholine (Ach), gamma-aminobutyric acid (GABA), and glutamate neurotransmission in the locomotory circuit. We identified that two G-protein-coupled 5-HT receptors, SER-7 and SER-5, antagonistically regulate the effects of fluoxetine and that fluoxetine binds to SER-7. Epistatic analyses suggest that SER-7 and SER-5 act upstream of AMPA receptor GLR-1 signaling. Our work provides genetic evidence that fluoxetine may influence neuronal functions and behavior by directly targeting serotonin receptors. |
| doi_str_mv | 10.1534/genetics.110.118877 |
| format | Article |
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Fluoxetine acts primarily as an inhibitor of the serotonin reuptake transporter (SERT) to block the removal of serotonin from the synaptic cleft, thereby enhancing serotonin signals. While the effects of fluoxetine on behavior are firmly established, debate is ongoing whether inhibition of serotonin reuptake is a sufficient explanation for its therapeutic action. Here, we provide evidence of two additional aspects of fluoxetine action through genetic analyses in Caenorhabditis elegans. We show that fluoxetine treatment and null mutation in the sole SERT gene mod-5 eliminate serotonin in specific neurons. These neurons do not synthesize serotonin but import extracellular serotonin via MOD-5/SERT. Furthermore, we show that fluoxetine acts independently of MOD-5/SERT to regulate discrete properties of acetylcholine (Ach), gamma-aminobutyric acid (GABA), and glutamate neurotransmission in the locomotory circuit. We identified that two G-protein-coupled 5-HT receptors, SER-7 and SER-5, antagonistically regulate the effects of fluoxetine and that fluoxetine binds to SER-7. Epistatic analyses suggest that SER-7 and SER-5 act upstream of AMPA receptor GLR-1 signaling. Our work provides genetic evidence that fluoxetine may influence neuronal functions and behavior by directly targeting serotonin receptors.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1534/genetics.110.118877</identifier><identifier>PMID: 20739712</identifier><identifier>CODEN: GENTAE</identifier><language>eng</language><publisher>United States: Genetics Society of America</publisher><subject>Acetylcholine - metabolism ; Animals ; Antidepressants ; Behavior, Animal - drug effects ; Biological Assay ; Caenorhabditis elegans - drug effects ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; E coli ; Fluoxetine - metabolism ; Fluoxetine - pharmacology ; gamma-Aminobutyric Acid - metabolism ; Genes ; Genetics ; Glutamic Acid - metabolism ; Investigations ; Muscle Relaxation - drug effects ; Mutation - genetics ; Nematodes ; Neurons - drug effects ; Neurons - metabolism ; Receptors, Serotonin - genetics ; Receptors, Serotonin - metabolism ; Selective Serotonin Reuptake Inhibitors - pharmacology ; Serotonin - metabolism ; Serotonin - pharmacology ; Signal Transduction - drug effects ; Synaptic Transmission - drug effects</subject><ispartof>Genetics (Austin), 2010-11, Vol.186 (3), p.929-941</ispartof><rights>Copyright Genetics Society of America Nov 2010</rights><rights>Copyright © 2010 by the Genetics Society of America 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c497t-17f9404b0952b7e2c53df495f558e4abbb1ba31462e0d00604519a989c35202c3</citedby><cites>FETCH-LOGICAL-c497t-17f9404b0952b7e2c53df495f558e4abbb1ba31462e0d00604519a989c35202c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20739712$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kullyev, Andrey</creatorcontrib><creatorcontrib>Dempsey, Catherine M</creatorcontrib><creatorcontrib>Miller, Sarah</creatorcontrib><creatorcontrib>Kuan, Chih-Jen</creatorcontrib><creatorcontrib>Hapiak, Vera M</creatorcontrib><creatorcontrib>Komuniecki, Richard W</creatorcontrib><creatorcontrib>Griffin, Christine T</creatorcontrib><creatorcontrib>Sze, Ji Ying</creatorcontrib><title>A genetic survey of fluoxetine action on synaptic transmission in Caenorhabditis elegans</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>Fluoxetine is one of the most commonly prescribed medications for many behavioral and neurological disorders. Fluoxetine acts primarily as an inhibitor of the serotonin reuptake transporter (SERT) to block the removal of serotonin from the synaptic cleft, thereby enhancing serotonin signals. While the effects of fluoxetine on behavior are firmly established, debate is ongoing whether inhibition of serotonin reuptake is a sufficient explanation for its therapeutic action. Here, we provide evidence of two additional aspects of fluoxetine action through genetic analyses in Caenorhabditis elegans. We show that fluoxetine treatment and null mutation in the sole SERT gene mod-5 eliminate serotonin in specific neurons. These neurons do not synthesize serotonin but import extracellular serotonin via MOD-5/SERT. Furthermore, we show that fluoxetine acts independently of MOD-5/SERT to regulate discrete properties of acetylcholine (Ach), gamma-aminobutyric acid (GABA), and glutamate neurotransmission in the locomotory circuit. We identified that two G-protein-coupled 5-HT receptors, SER-7 and SER-5, antagonistically regulate the effects of fluoxetine and that fluoxetine binds to SER-7. Epistatic analyses suggest that SER-7 and SER-5 act upstream of AMPA receptor GLR-1 signaling. Our work provides genetic evidence that fluoxetine may influence neuronal functions and behavior by directly targeting serotonin receptors.</description><subject>Acetylcholine - metabolism</subject><subject>Animals</subject><subject>Antidepressants</subject><subject>Behavior, Animal - drug effects</subject><subject>Biological Assay</subject><subject>Caenorhabditis elegans - drug effects</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>E coli</subject><subject>Fluoxetine - metabolism</subject><subject>Fluoxetine - pharmacology</subject><subject>gamma-Aminobutyric Acid - metabolism</subject><subject>Genes</subject><subject>Genetics</subject><subject>Glutamic Acid - metabolism</subject><subject>Investigations</subject><subject>Muscle Relaxation - drug effects</subject><subject>Mutation - genetics</subject><subject>Nematodes</subject><subject>Neurons - drug effects</subject><subject>Neurons - metabolism</subject><subject>Receptors, Serotonin - genetics</subject><subject>Receptors, Serotonin - metabolism</subject><subject>Selective Serotonin Reuptake Inhibitors - pharmacology</subject><subject>Serotonin - metabolism</subject><subject>Serotonin - pharmacology</subject><subject>Signal Transduction - drug effects</subject><subject>Synaptic Transmission - drug effects</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpdUdtKAzEUDKJ4qX6BIIsvPlVz3WxeBCneQPBFwbeQTc_WyDapya7YvzdrW1EhkDBnzjCTQeiY4HMiGL-YgYfO2XROBoRUlZRbaJ8ozsa0ZGT713sPHaT0hjEulah20R7FkilJ6D56uSrWOkXq4wcsi9AUTduHz4x5KIztXPBFPmnpzWLgddH4NHcpDQPni4kBH-Krqaeuc6mAFmaZcIh2GtMmOFrfI_R8c_00uRs_PN7eT64expYr2Y2JbBTHvMZK0FoCtYJNG65EI0QF3NR1TWrDCC8p4Gn2j7kgyqhKWSYoppaN0OVKd9HXc5ha8NlfqxfRzU1c6mCc_jvx7lXPwoemSgpakSxwthaI4b2H1OmczULbGg-hT1qWjEtS5h8bodN_zLfQR5_T6YrkArBUZSaxFcnGkFKE5scKwXroTW9602RAvnvLWye_U_zsbIpiX097l04</recordid><startdate>201011</startdate><enddate>201011</enddate><creator>Kullyev, Andrey</creator><creator>Dempsey, Catherine M</creator><creator>Miller, Sarah</creator><creator>Kuan, Chih-Jen</creator><creator>Hapiak, Vera M</creator><creator>Komuniecki, Richard W</creator><creator>Griffin, Christine T</creator><creator>Sze, Ji Ying</creator><general>Genetics Society of America</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>3V.</scope><scope>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0R</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201011</creationdate><title>A genetic survey of fluoxetine action on synaptic transmission in Caenorhabditis elegans</title><author>Kullyev, Andrey ; Dempsey, Catherine M ; Miller, Sarah ; Kuan, Chih-Jen ; Hapiak, Vera M ; Komuniecki, Richard W ; Griffin, Christine T ; Sze, Ji Ying</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c497t-17f9404b0952b7e2c53df495f558e4abbb1ba31462e0d00604519a989c35202c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Acetylcholine - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genetics (Austin)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kullyev, Andrey</au><au>Dempsey, Catherine M</au><au>Miller, Sarah</au><au>Kuan, Chih-Jen</au><au>Hapiak, Vera M</au><au>Komuniecki, Richard W</au><au>Griffin, Christine T</au><au>Sze, Ji Ying</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A genetic survey of fluoxetine action on synaptic transmission in Caenorhabditis elegans</atitle><jtitle>Genetics (Austin)</jtitle><addtitle>Genetics</addtitle><date>2010-11</date><risdate>2010</risdate><volume>186</volume><issue>3</issue><spage>929</spage><epage>941</epage><pages>929-941</pages><issn>1943-2631</issn><issn>0016-6731</issn><eissn>1943-2631</eissn><coden>GENTAE</coden><abstract>Fluoxetine is one of the most commonly prescribed medications for many behavioral and neurological disorders. Fluoxetine acts primarily as an inhibitor of the serotonin reuptake transporter (SERT) to block the removal of serotonin from the synaptic cleft, thereby enhancing serotonin signals. While the effects of fluoxetine on behavior are firmly established, debate is ongoing whether inhibition of serotonin reuptake is a sufficient explanation for its therapeutic action. Here, we provide evidence of two additional aspects of fluoxetine action through genetic analyses in Caenorhabditis elegans. We show that fluoxetine treatment and null mutation in the sole SERT gene mod-5 eliminate serotonin in specific neurons. These neurons do not synthesize serotonin but import extracellular serotonin via MOD-5/SERT. Furthermore, we show that fluoxetine acts independently of MOD-5/SERT to regulate discrete properties of acetylcholine (Ach), gamma-aminobutyric acid (GABA), and glutamate neurotransmission in the locomotory circuit. We identified that two G-protein-coupled 5-HT receptors, SER-7 and SER-5, antagonistically regulate the effects of fluoxetine and that fluoxetine binds to SER-7. Epistatic analyses suggest that SER-7 and SER-5 act upstream of AMPA receptor GLR-1 signaling. Our work provides genetic evidence that fluoxetine may influence neuronal functions and behavior by directly targeting serotonin receptors.</abstract><cop>United States</cop><pub>Genetics Society of America</pub><pmid>20739712</pmid><doi>10.1534/genetics.110.118877</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Genetics (Austin), 2010-11, Vol.186 (3), p.929-941 |
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
| subjects | Acetylcholine - metabolism Animals Antidepressants Behavior, Animal - drug effects Biological Assay Caenorhabditis elegans - drug effects Caenorhabditis elegans - genetics Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism E coli Fluoxetine - metabolism Fluoxetine - pharmacology gamma-Aminobutyric Acid - metabolism Genes Genetics Glutamic Acid - metabolism Investigations Muscle Relaxation - drug effects Mutation - genetics Nematodes Neurons - drug effects Neurons - metabolism Receptors, Serotonin - genetics Receptors, Serotonin - metabolism Selective Serotonin Reuptake Inhibitors - pharmacology Serotonin - metabolism Serotonin - pharmacology Signal Transduction - drug effects Synaptic Transmission - drug effects |
| title | A genetic survey of fluoxetine action on synaptic transmission in Caenorhabditis elegans |
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