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Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta
Glial cells have several critical roles in the developing and adult olfactory (antennal) lobe of the moth Manduca sexta. Early in development, glial cells occupy discrete regions of the developing olfactory pathway and processes of γ‐aminobutyric acid (GABA)ergic neurons extend into some of these re...
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Published in: | Journal of comparative neurology (1911) 2010-03, Vol.518 (6), p.815-838 |
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description | Glial cells have several critical roles in the developing and adult olfactory (antennal) lobe of the moth Manduca sexta. Early in development, glial cells occupy discrete regions of the developing olfactory pathway and processes of γ‐aminobutyric acid (GABA)ergic neurons extend into some of these regions. Because GABA is known to have developmental effects in a variety of systems, we explored the possibility that the glial cells express a GABA transporter that could regulate GABA levels to which olfactory neurons and glial cells are exposed. By using an antibody raised against a characterized high‐affinity M. sexta GABA transporter with high sequence homology to known mammalian GABA transporters (Mbungu et al. [1995] Arch. Biochem. Biophys. 318:489–497; Umesh and Gill [2002] J. Comp. Neurol. 448:388–398), we found that the GABA transporter is localized to subsets of centrally derived glial cells during metamorphic adult development. The transporter persists into adulthood in a subset of the neuropil‐associated glial cells, but its distribution pattern as determined by light‐and electron‐microscopic‐level immunocytochemistry indicates that it could not serve to regulate GABA concentration in the synaptic cleft. Instead, its role is more likely to regulate extracellular GABA levels within the glomerular neuropil. Expression in the sorting zone glial cells disappears after the period of olfactory receptor axon ingrowth, but may be important during ingrowth if GABA regulates axon growth. Glial cells take up GABA, and that uptake can be blocked by L‐2,4‐diaminobutyric acid (DABA). This is the first molecular evidence that the central glial cell population in this pathway is heterogeneous. J. Comp. Neurol. 518:815–838, 2010. © 2009 Wiley‐Liss, Inc. |
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Early in development, glial cells occupy discrete regions of the developing olfactory pathway and processes of γ‐aminobutyric acid (GABA)ergic neurons extend into some of these regions. Because GABA is known to have developmental effects in a variety of systems, we explored the possibility that the glial cells express a GABA transporter that could regulate GABA levels to which olfactory neurons and glial cells are exposed. By using an antibody raised against a characterized high‐affinity M. sexta GABA transporter with high sequence homology to known mammalian GABA transporters (Mbungu et al. [1995] Arch. Biochem. Biophys. 318:489–497; Umesh and Gill [2002] J. Comp. Neurol. 448:388–398), we found that the GABA transporter is localized to subsets of centrally derived glial cells during metamorphic adult development. The transporter persists into adulthood in a subset of the neuropil‐associated glial cells, but its distribution pattern as determined by light‐and electron‐microscopic‐level immunocytochemistry indicates that it could not serve to regulate GABA concentration in the synaptic cleft. Instead, its role is more likely to regulate extracellular GABA levels within the glomerular neuropil. Expression in the sorting zone glial cells disappears after the period of olfactory receptor axon ingrowth, but may be important during ingrowth if GABA regulates axon growth. Glial cells take up GABA, and that uptake can be blocked by L‐2,4‐diaminobutyric acid (DABA). This is the first molecular evidence that the central glial cell population in this pathway is heterogeneous. J. Comp. Neurol. 518:815–838, 2010. © 2009 Wiley‐Liss, Inc.</description><identifier>ISSN: 0021-9967</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.22244</identifier><identifier>PMID: 20058309</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc., A Wiley Company</publisher><subject>Animals ; antennal ; Axons - metabolism ; Axons - ultrastructure ; Brain - growth & development ; Brain - metabolism ; Brain - ultrastructure ; Dendrites - metabolism ; Dendrites - ultrastructure ; Female ; GABA Plasma Membrane Transport Proteins - metabolism ; gamma-Aminobutyric Acid - metabolism ; GAT ; glia ; insect ; Insect Proteins - metabolism ; invertebrate ; Male ; Manduca - growth & development ; Manduca - metabolism ; Manduca - ultrastructure ; Manduca sexta ; Metamorphosis, Biological ; Neuroglia - metabolism ; Neuroglia - ultrastructure ; Neurons - metabolism ; Neurons - ultrastructure ; Olfactory Pathways - growth & development ; Olfactory Pathways - metabolism ; Olfactory Pathways - ultrastructure ; Sensory Receptor Cells - metabolism ; Sensory Receptor Cells - ultrastructure</subject><ispartof>Journal of comparative neurology (1911), 2010-03, Vol.518 (6), p.815-838</ispartof><rights>Copyright © 2009 Wiley‐Liss, Inc.</rights><rights>Copyright © 2009 Wiley-Liss, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5454-c8d72f239d16e2932fdf2e0ed939d6abc063054bcdca712874c40abaceae58453</citedby><cites>FETCH-LOGICAL-c5454-c8d72f239d16e2932fdf2e0ed939d6abc063054bcdca712874c40abaceae58453</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20058309$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Oland, Lynne A.</creatorcontrib><creatorcontrib>Gibson, Nicholas J.</creatorcontrib><creatorcontrib>Tolbert, Leslie P.</creatorcontrib><title>Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta</title><title>Journal of comparative neurology (1911)</title><addtitle>J. Comp. Neurol</addtitle><description>Glial cells have several critical roles in the developing and adult olfactory (antennal) lobe of the moth Manduca sexta. Early in development, glial cells occupy discrete regions of the developing olfactory pathway and processes of γ‐aminobutyric acid (GABA)ergic neurons extend into some of these regions. Because GABA is known to have developmental effects in a variety of systems, we explored the possibility that the glial cells express a GABA transporter that could regulate GABA levels to which olfactory neurons and glial cells are exposed. By using an antibody raised against a characterized high‐affinity M. sexta GABA transporter with high sequence homology to known mammalian GABA transporters (Mbungu et al. [1995] Arch. Biochem. Biophys. 318:489–497; Umesh and Gill [2002] J. Comp. Neurol. 448:388–398), we found that the GABA transporter is localized to subsets of centrally derived glial cells during metamorphic adult development. The transporter persists into adulthood in a subset of the neuropil‐associated glial cells, but its distribution pattern as determined by light‐and electron‐microscopic‐level immunocytochemistry indicates that it could not serve to regulate GABA concentration in the synaptic cleft. Instead, its role is more likely to regulate extracellular GABA levels within the glomerular neuropil. Expression in the sorting zone glial cells disappears after the period of olfactory receptor axon ingrowth, but may be important during ingrowth if GABA regulates axon growth. Glial cells take up GABA, and that uptake can be blocked by L‐2,4‐diaminobutyric acid (DABA). This is the first molecular evidence that the central glial cell population in this pathway is heterogeneous. J. Comp. Neurol. 518:815–838, 2010. © 2009 Wiley‐Liss, Inc.</description><subject>Animals</subject><subject>antennal</subject><subject>Axons - metabolism</subject><subject>Axons - ultrastructure</subject><subject>Brain - growth & development</subject><subject>Brain - metabolism</subject><subject>Brain - ultrastructure</subject><subject>Dendrites - metabolism</subject><subject>Dendrites - ultrastructure</subject><subject>Female</subject><subject>GABA Plasma Membrane Transport Proteins - metabolism</subject><subject>gamma-Aminobutyric Acid - metabolism</subject><subject>GAT</subject><subject>glia</subject><subject>insect</subject><subject>Insect Proteins - metabolism</subject><subject>invertebrate</subject><subject>Male</subject><subject>Manduca - growth & development</subject><subject>Manduca - metabolism</subject><subject>Manduca - ultrastructure</subject><subject>Manduca sexta</subject><subject>Metamorphosis, Biological</subject><subject>Neuroglia - metabolism</subject><subject>Neuroglia - ultrastructure</subject><subject>Neurons - metabolism</subject><subject>Neurons - ultrastructure</subject><subject>Olfactory Pathways - growth & development</subject><subject>Olfactory Pathways - metabolism</subject><subject>Olfactory Pathways - ultrastructure</subject><subject>Sensory Receptor Cells - metabolism</subject><subject>Sensory Receptor Cells - ultrastructure</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><recordid>eNqFkk9vEzEQxVcIREPhwBdAljgAh2299tprXyqFqA1IoYj_R2vi9SYuzjrY3rbh0-OQNgIk4DSS5zdvPE-vKB5X-KjCmBzr3hwRQur6TjGqsOSlFLy6W4xyryql5M1B8SDGC4yxlFTcLw4IxkxQLEfFZuY1OPsdkvU98h0CNB2_HKMUoI9rH5IJKHm0cBYc0sa5iGyP0tKg1lwa59e2XyDoWwTt4BLyrgOdfNigNaTlFWy2klt65dMSvcngoAFFc53gYXGvAxfNo5t6WHw6O_04eVXO3k5fT8azUrOa1aUWbUM6QmVbcUMkJV3bEYNNK_MTh7nGnGJWz3WroamIaGpdY5iDNmCYqBk9LE52uuthvjKtNn2-zal1sCsIG-XBqt87vV2qhb9URJLsH8kCz24Egv82mJjUysatFdAbP0TV5H8ywln9f5JSwYkQPJPP_0lWoiGCSsKajD79A73wQ-izZZninHCCq-3qFztKBx9jMN3-wAqrbUhUDon6GZLMPvnVkT15m4oMHO-AK-vM5u9KanJ-eitZ7iZsTOZ6PwHhq-INbZj6cj5V7xt-9uHzO6Ym9AcfltYg</recordid><startdate>20100315</startdate><enddate>20100315</enddate><creator>Oland, Lynne A.</creator><creator>Gibson, Nicholas J.</creator><creator>Tolbert, Leslie P.</creator><general>Wiley Subscription Services, Inc., A Wiley Company</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</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>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>7SS</scope><scope>5PM</scope></search><sort><creationdate>20100315</creationdate><title>Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta</title><author>Oland, Lynne A. ; Gibson, Nicholas J. ; Tolbert, Leslie P.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5454-c8d72f239d16e2932fdf2e0ed939d6abc063054bcdca712874c40abaceae58453</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Animals</topic><topic>antennal</topic><topic>Axons - metabolism</topic><topic>Axons - ultrastructure</topic><topic>Brain - growth & development</topic><topic>Brain - metabolism</topic><topic>Brain - ultrastructure</topic><topic>Dendrites - metabolism</topic><topic>Dendrites - ultrastructure</topic><topic>Female</topic><topic>GABA Plasma Membrane Transport Proteins - metabolism</topic><topic>gamma-Aminobutyric Acid - metabolism</topic><topic>GAT</topic><topic>glia</topic><topic>insect</topic><topic>Insect Proteins - metabolism</topic><topic>invertebrate</topic><topic>Male</topic><topic>Manduca - growth & development</topic><topic>Manduca - metabolism</topic><topic>Manduca - ultrastructure</topic><topic>Manduca sexta</topic><topic>Metamorphosis, Biological</topic><topic>Neuroglia - metabolism</topic><topic>Neuroglia - ultrastructure</topic><topic>Neurons - metabolism</topic><topic>Neurons - ultrastructure</topic><topic>Olfactory Pathways - growth & development</topic><topic>Olfactory Pathways - metabolism</topic><topic>Olfactory Pathways - ultrastructure</topic><topic>Sensory Receptor Cells - metabolism</topic><topic>Sensory Receptor Cells - ultrastructure</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Oland, Lynne A.</creatorcontrib><creatorcontrib>Gibson, Nicholas J.</creatorcontrib><creatorcontrib>Tolbert, Leslie P.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</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>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Entomology Abstracts (Full archive)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of comparative neurology (1911)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Oland, Lynne A.</au><au>Gibson, Nicholas J.</au><au>Tolbert, Leslie P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta</atitle><jtitle>Journal of comparative neurology (1911)</jtitle><addtitle>J. Comp. Neurol</addtitle><date>2010-03-15</date><risdate>2010</risdate><volume>518</volume><issue>6</issue><spage>815</spage><epage>838</epage><pages>815-838</pages><issn>0021-9967</issn><eissn>1096-9861</eissn><abstract>Glial cells have several critical roles in the developing and adult olfactory (antennal) lobe of the moth Manduca sexta. Early in development, glial cells occupy discrete regions of the developing olfactory pathway and processes of γ‐aminobutyric acid (GABA)ergic neurons extend into some of these regions. Because GABA is known to have developmental effects in a variety of systems, we explored the possibility that the glial cells express a GABA transporter that could regulate GABA levels to which olfactory neurons and glial cells are exposed. By using an antibody raised against a characterized high‐affinity M. sexta GABA transporter with high sequence homology to known mammalian GABA transporters (Mbungu et al. [1995] Arch. Biochem. Biophys. 318:489–497; Umesh and Gill [2002] J. Comp. Neurol. 448:388–398), we found that the GABA transporter is localized to subsets of centrally derived glial cells during metamorphic adult development. The transporter persists into adulthood in a subset of the neuropil‐associated glial cells, but its distribution pattern as determined by light‐and electron‐microscopic‐level immunocytochemistry indicates that it could not serve to regulate GABA concentration in the synaptic cleft. Instead, its role is more likely to regulate extracellular GABA levels within the glomerular neuropil. Expression in the sorting zone glial cells disappears after the period of olfactory receptor axon ingrowth, but may be important during ingrowth if GABA regulates axon growth. Glial cells take up GABA, and that uptake can be blocked by L‐2,4‐diaminobutyric acid (DABA). This is the first molecular evidence that the central glial cell population in this pathway is heterogeneous. J. Comp. Neurol. 518:815–838, 2010. © 2009 Wiley‐Liss, Inc.</abstract><cop>Hoboken</cop><pub>Wiley Subscription Services, Inc., A Wiley Company</pub><pmid>20058309</pmid><doi>10.1002/cne.22244</doi><tpages>24</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals antennal Axons - metabolism Axons - ultrastructure Brain - growth & development Brain - metabolism Brain - ultrastructure Dendrites - metabolism Dendrites - ultrastructure Female GABA Plasma Membrane Transport Proteins - metabolism gamma-Aminobutyric Acid - metabolism GAT glia insect Insect Proteins - metabolism invertebrate Male Manduca - growth & development Manduca - metabolism Manduca - ultrastructure Manduca sexta Metamorphosis, Biological Neuroglia - metabolism Neuroglia - ultrastructure Neurons - metabolism Neurons - ultrastructure Olfactory Pathways - growth & development Olfactory Pathways - metabolism Olfactory Pathways - ultrastructure Sensory Receptor Cells - metabolism Sensory Receptor Cells - ultrastructure |
title | Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta |
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