Glycine enhances microglial intracellular calcium signaling. A role for sodium-coupled neutral amino acid transporters
The inhibitory neurotransmitter glycine is known to enhance microglial nitric oxide production. However, up to now, the mechanism is undocumented. Since calcium is an important second messenger in both immune and glial cells, we studied the effects of glycine on intracellular calcium signaling. We f...
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| Veröffentlicht in: | Pflügers Archiv 2011-04, Vol.461 (4), p.481-491 |
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| creator | Van den Eynden, Jimmy Notelaers, Kristof Brône, Bert Janssen, Daniel Nelissen, Katherine SahebAli, Sheen Smolders, Inge Hellings, Niels Steels, Paul Rigo, Jean-Michel |
| description | The inhibitory neurotransmitter glycine is known to enhance microglial nitric oxide production. However, up to now, the mechanism is undocumented. Since calcium is an important second messenger in both immune and glial cells, we studied the effects of glycine on intracellular calcium signaling. We found that millimolar concentrations of glycine enhance microglial intracellular calcium transients induced by 100 μM ATP or by 500 nM thapsigargin. This modulation was unaffected by the glycine receptor antagonist strychnine and could not be mimicked by glycine receptor agonists such as taurine or β-alanine, indicating glycine receptor independency. The modulation of calcium responses could be mimicked by several structurally related amino acids (e.g., serine, alanine, or glutamine) and was inhibited in the presence of the neutral amino acid transporter substrate α-aminoisobutyric acid (AIB). We correlated these findings to immunofluorescence glycine uptake experiments which showed a clear glycine uptake which was inhibited by AIB. Furthermore, all amino acids that were shown to modulate calcium responses also evoked AIB-sensitive inward currents, mainly carried by sodium, as demonstrated by patch clamp experiments. Based on these findings, we propose that sodium-coupled neutral amino acid transporters are responsible for the observed glycine modulation of intracellular calcium responses. |
| doi_str_mv | 10.1007/s00424-011-0939-0 |
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A role for sodium-coupled neutral amino acid transporters</title><source>MEDLINE</source><source>SpringerLink Journals - AutoHoldings</source><creator>Van den Eynden, Jimmy ; Notelaers, Kristof ; Brône, Bert ; Janssen, Daniel ; Nelissen, Katherine ; SahebAli, Sheen ; Smolders, Inge ; Hellings, Niels ; Steels, Paul ; Rigo, Jean-Michel</creator><creatorcontrib>Van den Eynden, Jimmy ; Notelaers, Kristof ; Brône, Bert ; Janssen, Daniel ; Nelissen, Katherine ; SahebAli, Sheen ; Smolders, Inge ; Hellings, Niels ; Steels, Paul ; Rigo, Jean-Michel</creatorcontrib><description>The inhibitory neurotransmitter glycine is known to enhance microglial nitric oxide production. However, up to now, the mechanism is undocumented. Since calcium is an important second messenger in both immune and glial cells, we studied the effects of glycine on intracellular calcium signaling. We found that millimolar concentrations of glycine enhance microglial intracellular calcium transients induced by 100 μM ATP or by 500 nM thapsigargin. This modulation was unaffected by the glycine receptor antagonist strychnine and could not be mimicked by glycine receptor agonists such as taurine or β-alanine, indicating glycine receptor independency. The modulation of calcium responses could be mimicked by several structurally related amino acids (e.g., serine, alanine, or glutamine) and was inhibited in the presence of the neutral amino acid transporter substrate α-aminoisobutyric acid (AIB). We correlated these findings to immunofluorescence glycine uptake experiments which showed a clear glycine uptake which was inhibited by AIB. Furthermore, all amino acids that were shown to modulate calcium responses also evoked AIB-sensitive inward currents, mainly carried by sodium, as demonstrated by patch clamp experiments. Based on these findings, we propose that sodium-coupled neutral amino acid transporters are responsible for the observed glycine modulation of intracellular calcium responses.</description><identifier>ISSN: 0031-6768</identifier><identifier>EISSN: 1432-2013</identifier><identifier>DOI: 10.1007/s00424-011-0939-0</identifier><identifier>PMID: 21350800</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer-Verlag</publisher><subject>Alanine ; Amino Acid Transport System A - physiology ; Amino acids ; Aminoisobutyric Acids - pharmacology ; Animals ; ATP ; beta-Alanine - pharmacology ; Biomedical and Life Sciences ; Biomedicine ; Calcium (intracellular) ; Calcium Signaling - drug effects ; Calcium Signaling - physiology ; Cell Biology ; Cell Line ; Glial cells ; Glutamine ; Glycine - metabolism ; Glycine - pharmacology ; Glycine Agents - pharmacology ; Glycine receptors ; Human Physiology ; Immunofluorescence ; Intracellular signalling ; Mice ; Microglia - drug effects ; Microglia - physiology ; Models, Animal ; Molecular Medicine ; Neurosciences ; Neurotransmitters ; Nitric oxide ; Patch-Clamp Techniques ; Receptors ; Receptors, Glycine - agonists ; Receptors, Glycine - antagonists & inhibitors ; Receptors, Glycine - physiology ; Second messengers ; Serine ; Signaling and Cell Physiology ; Sodium ; strychnine ; Strychnine - pharmacology ; Taurine ; Taurine - pharmacology ; thapsigargin</subject><ispartof>Pflügers Archiv, 2011-04, Vol.461 (4), p.481-491</ispartof><rights>Springer-Verlag 2011</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c402t-d4d853589c8a1510755aa834f4661c546b5cc58b4643bb9567ad1d35f72de5ae3</citedby><cites>FETCH-LOGICAL-c402t-d4d853589c8a1510755aa834f4661c546b5cc58b4643bb9567ad1d35f72de5ae3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00424-011-0939-0$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00424-011-0939-0$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21350800$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Van den Eynden, Jimmy</creatorcontrib><creatorcontrib>Notelaers, Kristof</creatorcontrib><creatorcontrib>Brône, Bert</creatorcontrib><creatorcontrib>Janssen, Daniel</creatorcontrib><creatorcontrib>Nelissen, Katherine</creatorcontrib><creatorcontrib>SahebAli, Sheen</creatorcontrib><creatorcontrib>Smolders, Inge</creatorcontrib><creatorcontrib>Hellings, Niels</creatorcontrib><creatorcontrib>Steels, Paul</creatorcontrib><creatorcontrib>Rigo, Jean-Michel</creatorcontrib><title>Glycine enhances microglial intracellular calcium signaling. A role for sodium-coupled neutral amino acid transporters</title><title>Pflügers Archiv</title><addtitle>Pflugers Arch - Eur J Physiol</addtitle><addtitle>Pflugers Arch</addtitle><description>The inhibitory neurotransmitter glycine is known to enhance microglial nitric oxide production. However, up to now, the mechanism is undocumented. Since calcium is an important second messenger in both immune and glial cells, we studied the effects of glycine on intracellular calcium signaling. We found that millimolar concentrations of glycine enhance microglial intracellular calcium transients induced by 100 μM ATP or by 500 nM thapsigargin. This modulation was unaffected by the glycine receptor antagonist strychnine and could not be mimicked by glycine receptor agonists such as taurine or β-alanine, indicating glycine receptor independency. The modulation of calcium responses could be mimicked by several structurally related amino acids (e.g., serine, alanine, or glutamine) and was inhibited in the presence of the neutral amino acid transporter substrate α-aminoisobutyric acid (AIB). We correlated these findings to immunofluorescence glycine uptake experiments which showed a clear glycine uptake which was inhibited by AIB. Furthermore, all amino acids that were shown to modulate calcium responses also evoked AIB-sensitive inward currents, mainly carried by sodium, as demonstrated by patch clamp experiments. Based on these findings, we propose that sodium-coupled neutral amino acid transporters are responsible for the observed glycine modulation of intracellular calcium responses.</description><subject>Alanine</subject><subject>Amino Acid Transport System A - physiology</subject><subject>Amino acids</subject><subject>Aminoisobutyric Acids - pharmacology</subject><subject>Animals</subject><subject>ATP</subject><subject>beta-Alanine - pharmacology</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Calcium (intracellular)</subject><subject>Calcium Signaling - drug effects</subject><subject>Calcium Signaling - physiology</subject><subject>Cell Biology</subject><subject>Cell Line</subject><subject>Glial cells</subject><subject>Glutamine</subject><subject>Glycine - metabolism</subject><subject>Glycine - pharmacology</subject><subject>Glycine Agents - pharmacology</subject><subject>Glycine receptors</subject><subject>Human Physiology</subject><subject>Immunofluorescence</subject><subject>Intracellular signalling</subject><subject>Mice</subject><subject>Microglia - drug effects</subject><subject>Microglia - physiology</subject><subject>Models, Animal</subject><subject>Molecular Medicine</subject><subject>Neurosciences</subject><subject>Neurotransmitters</subject><subject>Nitric oxide</subject><subject>Patch-Clamp Techniques</subject><subject>Receptors</subject><subject>Receptors, Glycine - agonists</subject><subject>Receptors, Glycine - antagonists & inhibitors</subject><subject>Receptors, Glycine - physiology</subject><subject>Second messengers</subject><subject>Serine</subject><subject>Signaling and Cell Physiology</subject><subject>Sodium</subject><subject>strychnine</subject><subject>Strychnine - pharmacology</subject><subject>Taurine</subject><subject>Taurine - pharmacology</subject><subject>thapsigargin</subject><issn>0031-6768</issn><issn>1432-2013</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kU1rVDEUhoModqz-ADcS3LhKPfnOXZaiVSi40XXITXLHlNxkTOYK_fdmmKoguArhPO8bTh6EXlO4ogD6fQcQTBCglMDEJwJP0I4KzggDyp-iHQCnRGllLtCL3u8BgAnDnqMLRrkEA7BDP2_zg08l4li-u-Jjx2vyre5zchmncmzOx5y37Br2Lvu0rbinfXE5lf0Vvsat5oiX2nCvYQyJr9shx4BL3EY2Y7emUrHzKeBxL_1Q2zG2_hI9W1zu8dXjeYm-ffzw9eYTufty-_nm-o54AexIgghGcmkmbxyVFLSUzhkuFqEU9VKoWXovzSyU4PM8SaVdoIHLRbMQpYv8Er079x5a_bHFfrRr6qeNXIl163YCTRXXehrk23_I-7q1sWi3RhqhmZZqQPQMjS_qvcXFHlpaXXuwFOxJiT0rsUOJPSmxMDJvHou3eY3hT-K3gwGwM9DHqOxj-_vy_1t_AWV7l4o</recordid><startdate>20110401</startdate><enddate>20110401</enddate><creator>Van den Eynden, Jimmy</creator><creator>Notelaers, Kristof</creator><creator>Brône, Bert</creator><creator>Janssen, Daniel</creator><creator>Nelissen, Katherine</creator><creator>SahebAli, Sheen</creator><creator>Smolders, Inge</creator><creator>Hellings, Niels</creator><creator>Steels, Paul</creator><creator>Rigo, Jean-Michel</creator><general>Springer-Verlag</general><general>Springer Nature B.V</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>7QP</scope><scope>7TK</scope><scope>7TS</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope></search><sort><creationdate>20110401</creationdate><title>Glycine enhances microglial intracellular calcium signaling. A role for sodium-coupled neutral amino acid transporters</title><author>Van den Eynden, Jimmy ; Notelaers, Kristof ; Brône, Bert ; Janssen, Daniel ; Nelissen, Katherine ; SahebAli, Sheen ; Smolders, Inge ; Hellings, Niels ; Steels, Paul ; Rigo, Jean-Michel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c402t-d4d853589c8a1510755aa834f4661c546b5cc58b4643bb9567ad1d35f72de5ae3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Alanine</topic><topic>Amino Acid Transport System A - physiology</topic><topic>Amino acids</topic><topic>Aminoisobutyric Acids - pharmacology</topic><topic>Animals</topic><topic>ATP</topic><topic>beta-Alanine - pharmacology</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Calcium (intracellular)</topic><topic>Calcium Signaling - drug effects</topic><topic>Calcium Signaling - physiology</topic><topic>Cell Biology</topic><topic>Cell Line</topic><topic>Glial cells</topic><topic>Glutamine</topic><topic>Glycine - metabolism</topic><topic>Glycine - pharmacology</topic><topic>Glycine Agents - pharmacology</topic><topic>Glycine receptors</topic><topic>Human Physiology</topic><topic>Immunofluorescence</topic><topic>Intracellular signalling</topic><topic>Mice</topic><topic>Microglia - drug effects</topic><topic>Microglia - physiology</topic><topic>Models, Animal</topic><topic>Molecular Medicine</topic><topic>Neurosciences</topic><topic>Neurotransmitters</topic><topic>Nitric oxide</topic><topic>Patch-Clamp Techniques</topic><topic>Receptors</topic><topic>Receptors, Glycine - agonists</topic><topic>Receptors, Glycine - antagonists & inhibitors</topic><topic>Receptors, Glycine - physiology</topic><topic>Second messengers</topic><topic>Serine</topic><topic>Signaling and Cell Physiology</topic><topic>Sodium</topic><topic>strychnine</topic><topic>Strychnine - pharmacology</topic><topic>Taurine</topic><topic>Taurine - pharmacology</topic><topic>thapsigargin</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Van den Eynden, Jimmy</creatorcontrib><creatorcontrib>Notelaers, Kristof</creatorcontrib><creatorcontrib>Brône, Bert</creatorcontrib><creatorcontrib>Janssen, Daniel</creatorcontrib><creatorcontrib>Nelissen, Katherine</creatorcontrib><creatorcontrib>SahebAli, Sheen</creatorcontrib><creatorcontrib>Smolders, Inge</creatorcontrib><creatorcontrib>Hellings, Niels</creatorcontrib><creatorcontrib>Steels, Paul</creatorcontrib><creatorcontrib>Rigo, Jean-Michel</creatorcontrib><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>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Physical Education Index</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>ProQuest Pharma Collection</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><jtitle>Pflügers Archiv</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Van den Eynden, Jimmy</au><au>Notelaers, Kristof</au><au>Brône, Bert</au><au>Janssen, Daniel</au><au>Nelissen, Katherine</au><au>SahebAli, Sheen</au><au>Smolders, Inge</au><au>Hellings, Niels</au><au>Steels, Paul</au><au>Rigo, Jean-Michel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Glycine enhances microglial intracellular calcium signaling. A role for sodium-coupled neutral amino acid transporters</atitle><jtitle>Pflügers Archiv</jtitle><stitle>Pflugers Arch - Eur J Physiol</stitle><addtitle>Pflugers Arch</addtitle><date>2011-04-01</date><risdate>2011</risdate><volume>461</volume><issue>4</issue><spage>481</spage><epage>491</epage><pages>481-491</pages><issn>0031-6768</issn><eissn>1432-2013</eissn><abstract>The inhibitory neurotransmitter glycine is known to enhance microglial nitric oxide production. However, up to now, the mechanism is undocumented. Since calcium is an important second messenger in both immune and glial cells, we studied the effects of glycine on intracellular calcium signaling. We found that millimolar concentrations of glycine enhance microglial intracellular calcium transients induced by 100 μM ATP or by 500 nM thapsigargin. This modulation was unaffected by the glycine receptor antagonist strychnine and could not be mimicked by glycine receptor agonists such as taurine or β-alanine, indicating glycine receptor independency. The modulation of calcium responses could be mimicked by several structurally related amino acids (e.g., serine, alanine, or glutamine) and was inhibited in the presence of the neutral amino acid transporter substrate α-aminoisobutyric acid (AIB). We correlated these findings to immunofluorescence glycine uptake experiments which showed a clear glycine uptake which was inhibited by AIB. Furthermore, all amino acids that were shown to modulate calcium responses also evoked AIB-sensitive inward currents, mainly carried by sodium, as demonstrated by patch clamp experiments. Based on these findings, we propose that sodium-coupled neutral amino acid transporters are responsible for the observed glycine modulation of intracellular calcium responses.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer-Verlag</pub><pmid>21350800</pmid><doi>10.1007/s00424-011-0939-0</doi><tpages>11</tpages></addata></record> |
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| subjects | Alanine Amino Acid Transport System A - physiology Amino acids Aminoisobutyric Acids - pharmacology Animals ATP beta-Alanine - pharmacology Biomedical and Life Sciences Biomedicine Calcium (intracellular) Calcium Signaling - drug effects Calcium Signaling - physiology Cell Biology Cell Line Glial cells Glutamine Glycine - metabolism Glycine - pharmacology Glycine Agents - pharmacology Glycine receptors Human Physiology Immunofluorescence Intracellular signalling Mice Microglia - drug effects Microglia - physiology Models, Animal Molecular Medicine Neurosciences Neurotransmitters Nitric oxide Patch-Clamp Techniques Receptors Receptors, Glycine - agonists Receptors, Glycine - antagonists & inhibitors Receptors, Glycine - physiology Second messengers Serine Signaling and Cell Physiology Sodium strychnine Strychnine - pharmacology Taurine Taurine - pharmacology thapsigargin |
| title | Glycine enhances microglial intracellular calcium signaling. A role for sodium-coupled neutral amino acid transporters |
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