Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila

Persistent Link:
http://hdl.handle.net/10150/610224
Title:
Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila
Author:
Sinakevitch, Irina; Grau, Yves; Strausfeld, Nicholas; Birman, Serge
Affiliation:
Laboratoire de Neurobiologie, CNRS UMR 7637, ESPCI ParisTech, 10 rue Vauquelin, 75231 Paris cedex 5, France; Institut de Biologie du Développement de Marseille-Luminy, CNRS UMR 6216, Université de la Méditerranée, Campus de Luminy case 907, 13288 Marseille cedex 9, France; Institut de Génomique Fonctionnelle, CNRS UMR 5203, INSERM U661, Université de Montpellier I et II, 141 rue de la Cardonille, 34094 Montpellier cedex 5, France; Center for Insect Science and Department of Neuroscience, University of Arizona, Tucson, Arizona 85721, USA; Current address: Arizona State University, School of Life Sciences, Tempe, AZ 85287-4501, USA
Issue Date:
2010
Publisher:
BioMed Central
Citation:
Sinakevitch et al. Neural Development 2010, 5:10 http://www.neuraldevelopment.com/content/5/1/10
Journal:
Neural Development
Rights:
© 2010 Sinakevitch et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0)
Collection Information:
This item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.
Abstract:
BACKGROUND:The mushroom bodies (MBs) are paired brain centers located in the insect protocerebrum involved in olfactory learning and memory and other associative functions. Processes from the Kenyon cells (KCs), their intrinsic neurons, form the bulk of the MB's calyx, pedunculus and lobes. In young adult Drosophila, the last-born KCs extend their processes in the alpha/beta lobes as a thin core (alpha/beta cores) that is embedded in the surrounding matrix of other mature KC processes. A high level of L-glutamate (Glu) immunoreactivity is present in the alpha/beta cores (alpha/betac) of recently eclosed adult flies. In a Drosophila model of fragile X syndrome, the main cause of inherited mental retardation, treatment with metabotropic Glu receptor (mGluR) antagonists can rescue memory deficits and MB structural defects.RESULTS:To address the role of Glu signaling in the development and maturation of the MB, we have compared the time course of Glu immunoreactivity with the expression of various glutamatergic markers at various times, that is, 1 hour, 1 day and 10 days after adult eclosion. We observed that last-born alpha/betac KCs in young adult as well as developing KCs in late larva and at various pupal stages transiently express high level of Glu immunoreactivity in Drosophila. One day after eclosion, the Glu level was already markedly reduced in the alpha/betac neurons. Glial cell processes expressing glutamine synthetase and the Glu transporter dEAAT1 were found to surround the Glu-expressing KCs in very young adults, subsequently enwrapping the alpha/beta lobes to become distributed equally over the entire MB neuropil. The vesicular Glu transporter DVGluT was detected by immunostaining in processes that project within the MB lobes and pedunculus, but this transporter is apparently never expressed by the KCs themselves. The NMDA receptor subunit dNR1 is widely expressed in the MB neuropil just after eclosion, but was not detected in the alpha/betac neurons. In contrast, we provide evidence that DmGluRA, the only Drosophila mGluR, is specifically expressed in Glu-accumulating cells of the MB alpha/betac immediately and for a short time after eclosion.CONCLUSIONS:The distribution and dynamics of glutamatergic markers indicate that newborn KCs transiently accumulate Glu at a high level in late pupal and young eclosed Drosophila, and may locally release this amino acid by a mechanism that would not involve DVGluT. At this stage, Glu can bind to intrinsic mGluRs abundant in the alpha/betac KCs, and to NMDA receptors in the rest of the MB neuropil, before being captured and metabolized in surrounding glial cells. This suggests that Glu acts as an autocrine or paracrine agent that contributes to the structural and functional maturation of the MB during the first hours of Drosophila adult life.
EISSN:
1749-8104
DOI:
10.1186/1749-8104-5-10
Version:
Final published version
Additional Links:
http://www.neuraldevelopment.com/content/5/1/10

Full metadata record

DC FieldValue Language
dc.contributor.authorSinakevitch, Irinaen
dc.contributor.authorGrau, Yvesen
dc.contributor.authorStrausfeld, Nicholasen
dc.contributor.authorBirman, Sergeen
dc.date.accessioned2016-05-20T09:01:31Z-
dc.date.available2016-05-20T09:01:31Z-
dc.date.issued2010en
dc.identifier.citationSinakevitch et al. Neural Development 2010, 5:10 http://www.neuraldevelopment.com/content/5/1/10en
dc.identifier.doi10.1186/1749-8104-5-10en
dc.identifier.urihttp://hdl.handle.net/10150/610224-
dc.description.abstractBACKGROUND:The mushroom bodies (MBs) are paired brain centers located in the insect protocerebrum involved in olfactory learning and memory and other associative functions. Processes from the Kenyon cells (KCs), their intrinsic neurons, form the bulk of the MB's calyx, pedunculus and lobes. In young adult Drosophila, the last-born KCs extend their processes in the alpha/beta lobes as a thin core (alpha/beta cores) that is embedded in the surrounding matrix of other mature KC processes. A high level of L-glutamate (Glu) immunoreactivity is present in the alpha/beta cores (alpha/betac) of recently eclosed adult flies. In a Drosophila model of fragile X syndrome, the main cause of inherited mental retardation, treatment with metabotropic Glu receptor (mGluR) antagonists can rescue memory deficits and MB structural defects.RESULTS:To address the role of Glu signaling in the development and maturation of the MB, we have compared the time course of Glu immunoreactivity with the expression of various glutamatergic markers at various times, that is, 1 hour, 1 day and 10 days after adult eclosion. We observed that last-born alpha/betac KCs in young adult as well as developing KCs in late larva and at various pupal stages transiently express high level of Glu immunoreactivity in Drosophila. One day after eclosion, the Glu level was already markedly reduced in the alpha/betac neurons. Glial cell processes expressing glutamine synthetase and the Glu transporter dEAAT1 were found to surround the Glu-expressing KCs in very young adults, subsequently enwrapping the alpha/beta lobes to become distributed equally over the entire MB neuropil. The vesicular Glu transporter DVGluT was detected by immunostaining in processes that project within the MB lobes and pedunculus, but this transporter is apparently never expressed by the KCs themselves. The NMDA receptor subunit dNR1 is widely expressed in the MB neuropil just after eclosion, but was not detected in the alpha/betac neurons. In contrast, we provide evidence that DmGluRA, the only Drosophila mGluR, is specifically expressed in Glu-accumulating cells of the MB alpha/betac immediately and for a short time after eclosion.CONCLUSIONS:The distribution and dynamics of glutamatergic markers indicate that newborn KCs transiently accumulate Glu at a high level in late pupal and young eclosed Drosophila, and may locally release this amino acid by a mechanism that would not involve DVGluT. At this stage, Glu can bind to intrinsic mGluRs abundant in the alpha/betac KCs, and to NMDA receptors in the rest of the MB neuropil, before being captured and metabolized in surrounding glial cells. This suggests that Glu acts as an autocrine or paracrine agent that contributes to the structural and functional maturation of the MB during the first hours of Drosophila adult life.en
dc.language.isoenen
dc.publisherBioMed Centralen
dc.relation.urlhttp://www.neuraldevelopment.com/content/5/1/10en
dc.rights© 2010 Sinakevitch et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0)en
dc.titleDynamics of glutamatergic signaling in the mushroom body of young adult Drosophilaen
dc.typeArticleen
dc.identifier.eissn1749-8104en
dc.contributor.departmentLaboratoire de Neurobiologie, CNRS UMR 7637, ESPCI ParisTech, 10 rue Vauquelin, 75231 Paris cedex 5, Franceen
dc.contributor.departmentInstitut de Biologie du Développement de Marseille-Luminy, CNRS UMR 6216, Université de la Méditerranée, Campus de Luminy case 907, 13288 Marseille cedex 9, Franceen
dc.contributor.departmentInstitut de Génomique Fonctionnelle, CNRS UMR 5203, INSERM U661, Université de Montpellier I et II, 141 rue de la Cardonille, 34094 Montpellier cedex 5, Franceen
dc.contributor.departmentCenter for Insect Science and Department of Neuroscience, University of Arizona, Tucson, Arizona 85721, USAen
dc.contributor.departmentCurrent address: Arizona State University, School of Life Sciences, Tempe, AZ 85287-4501, USAen
dc.identifier.journalNeural Developmenten
dc.description.collectioninformationThis item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.en
dc.eprint.versionFinal published versionen
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