Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta

Lynne A Oland, Nicholas J. Gibson, Leslie P Tolbert

Research output: Contribution to journalArticle

10 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)815-838
Number of pages24
JournalJournal of Comparative Neurology
Volume518
Issue number6
DOIs
StatePublished - Mar 15 2010

Fingerprint

GABA Plasma Membrane Transport Proteins
Manduca
Olfactory Pathways
Moths
Neuroglia
gamma-Aminobutyric Acid
Neuropil
Axons
Odorant Receptors
Aminobutyrates
GABAergic Neurons
Sequence Homology
Immunohistochemistry
Electrons

Keywords

  • Antennal
  • GAT
  • Glia
  • Insect
  • Invertebrate

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Localization of a GABA transporter to glial cells in the developing and adult olfactory pathway of the moth Manduca sexta",
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.",
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AU - Gibson, Nicholas J.

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