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A glial variant of the vesicular monoamine transporter is required to store histamine in the Drosophila visual system.

Romero-Calderón R, Uhlenbrock G, Borycz J, Simon AF, Grygoruk A, Yee SK, Shyer A, Ackerson LC, Maidment NT, Meinertzhagen IA, Hovemann BT, Krantz DE - PLoS Genet. (2008)

Bottom Line: In mammals, vesicular monoamine transporters (VMATs) are expressed exclusively in neurons and mediate the storage of histamine and other monoamines.We report here that a novel mRNA splice variant of Drosophila VMAT (DVMAT-B) is expressed not in neurons but rather in a small subset of glia in the lamina of the fly's optic lobe.Our results suggest a novel role for a monoamine transporter in glia that may be relevant to histamine homeostasis in other systems.

View Article: PubMed Central - PubMed

Affiliation: Gonda Goldschmied Center for Neuroscience and Genetics Research, David Geffen School of Medicine at University of California Los Angeles, Los Angeles, California, United States of America.

ABSTRACT
Unlike other monoamine neurotransmitters, the mechanism by which the brain's histamine content is regulated remains unclear. In mammals, vesicular monoamine transporters (VMATs) are expressed exclusively in neurons and mediate the storage of histamine and other monoamines. We have studied the visual system of Drosophila melanogaster in which histamine is the primary neurotransmitter released from photoreceptor cells. We report here that a novel mRNA splice variant of Drosophila VMAT (DVMAT-B) is expressed not in neurons but rather in a small subset of glia in the lamina of the fly's optic lobe. Histamine contents are reduced by mutation of dVMAT, but can be partially restored by specifically expressing DVMAT-B in glia. Our results suggest a novel role for a monoamine transporter in glia that may be relevant to histamine homeostasis in other systems.

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The location and possible function of the fenestrated glia.(A) Photoreceptor cells R1–R6 terminate in the lamina where they innervate lamina target neurons. Groups of six R1–R6 terminals and lamina target neurons are organized into cartridges, the component modules of the lamina. The diagram illustrates the relationship between the photoreceptor cell axons (red), the basement membrane (blue) separating the retina and lamina, and the lamina target neurons (silver). Identified glial subtypes in the fly's lamina include the fenestrated (dark green), pseudocartridge (orange), satellite (light green), epithelial (yellow), and marginal glia (brown). (B) Possible functions of DVMAT-B in the fenestrated glia include: recycling metabolized histamine back to the photoreceptors (“Recycling”); preventing spillover of histamine into nearby cartridges (“Spillover”); and releasing a reserve pool of histamine into the lamina to regulate its concentration during periods of heavy release (“Reserve”).
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pgen-1000245-g009: The location and possible function of the fenestrated glia.(A) Photoreceptor cells R1–R6 terminate in the lamina where they innervate lamina target neurons. Groups of six R1–R6 terminals and lamina target neurons are organized into cartridges, the component modules of the lamina. The diagram illustrates the relationship between the photoreceptor cell axons (red), the basement membrane (blue) separating the retina and lamina, and the lamina target neurons (silver). Identified glial subtypes in the fly's lamina include the fenestrated (dark green), pseudocartridge (orange), satellite (light green), epithelial (yellow), and marginal glia (brown). (B) Possible functions of DVMAT-B in the fenestrated glia include: recycling metabolized histamine back to the photoreceptors (“Recycling”); preventing spillover of histamine into nearby cartridges (“Spillover”); and releasing a reserve pool of histamine into the lamina to regulate its concentration during periods of heavy release (“Reserve”).

Mentions: Ultrastructural and immunohistochemical studies in the fly have identified several distinct glial populations in the lamina. Although detailed ultrastructural accounts are available only in the housefly [61],[62], it is clear that Drosophila has similar populations of glia, and that genetic markers exist for most [68],[69]. The epithelial glia have been assigned an important role in histamine recycling [36],[44],[45], but the remaining glial subtypes have not been functionally characterized. The fenestrated glia lie closest to the retina and surround the photoreceptor axons as they enter the distal face of lamina (see Figure 9A). Processes from the fenestrated glia also extend through the basement membrane and into the retina. Our data strongly suggest that DVMAT-B localizes to the Drosophila equivalent of the fenestrated glia, consistent with the previously described location of the dVMAT transcript [56].


A glial variant of the vesicular monoamine transporter is required to store histamine in the Drosophila visual system.

Romero-Calderón R, Uhlenbrock G, Borycz J, Simon AF, Grygoruk A, Yee SK, Shyer A, Ackerson LC, Maidment NT, Meinertzhagen IA, Hovemann BT, Krantz DE - PLoS Genet. (2008)

The location and possible function of the fenestrated glia.(A) Photoreceptor cells R1–R6 terminate in the lamina where they innervate lamina target neurons. Groups of six R1–R6 terminals and lamina target neurons are organized into cartridges, the component modules of the lamina. The diagram illustrates the relationship between the photoreceptor cell axons (red), the basement membrane (blue) separating the retina and lamina, and the lamina target neurons (silver). Identified glial subtypes in the fly's lamina include the fenestrated (dark green), pseudocartridge (orange), satellite (light green), epithelial (yellow), and marginal glia (brown). (B) Possible functions of DVMAT-B in the fenestrated glia include: recycling metabolized histamine back to the photoreceptors (“Recycling”); preventing spillover of histamine into nearby cartridges (“Spillover”); and releasing a reserve pool of histamine into the lamina to regulate its concentration during periods of heavy release (“Reserve”).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2570955&req=5

pgen-1000245-g009: The location and possible function of the fenestrated glia.(A) Photoreceptor cells R1–R6 terminate in the lamina where they innervate lamina target neurons. Groups of six R1–R6 terminals and lamina target neurons are organized into cartridges, the component modules of the lamina. The diagram illustrates the relationship between the photoreceptor cell axons (red), the basement membrane (blue) separating the retina and lamina, and the lamina target neurons (silver). Identified glial subtypes in the fly's lamina include the fenestrated (dark green), pseudocartridge (orange), satellite (light green), epithelial (yellow), and marginal glia (brown). (B) Possible functions of DVMAT-B in the fenestrated glia include: recycling metabolized histamine back to the photoreceptors (“Recycling”); preventing spillover of histamine into nearby cartridges (“Spillover”); and releasing a reserve pool of histamine into the lamina to regulate its concentration during periods of heavy release (“Reserve”).
Mentions: Ultrastructural and immunohistochemical studies in the fly have identified several distinct glial populations in the lamina. Although detailed ultrastructural accounts are available only in the housefly [61],[62], it is clear that Drosophila has similar populations of glia, and that genetic markers exist for most [68],[69]. The epithelial glia have been assigned an important role in histamine recycling [36],[44],[45], but the remaining glial subtypes have not been functionally characterized. The fenestrated glia lie closest to the retina and surround the photoreceptor axons as they enter the distal face of lamina (see Figure 9A). Processes from the fenestrated glia also extend through the basement membrane and into the retina. Our data strongly suggest that DVMAT-B localizes to the Drosophila equivalent of the fenestrated glia, consistent with the previously described location of the dVMAT transcript [56].

Bottom Line: In mammals, vesicular monoamine transporters (VMATs) are expressed exclusively in neurons and mediate the storage of histamine and other monoamines.We report here that a novel mRNA splice variant of Drosophila VMAT (DVMAT-B) is expressed not in neurons but rather in a small subset of glia in the lamina of the fly's optic lobe.Our results suggest a novel role for a monoamine transporter in glia that may be relevant to histamine homeostasis in other systems.

View Article: PubMed Central - PubMed

Affiliation: Gonda Goldschmied Center for Neuroscience and Genetics Research, David Geffen School of Medicine at University of California Los Angeles, Los Angeles, California, United States of America.

ABSTRACT
Unlike other monoamine neurotransmitters, the mechanism by which the brain's histamine content is regulated remains unclear. In mammals, vesicular monoamine transporters (VMATs) are expressed exclusively in neurons and mediate the storage of histamine and other monoamines. We have studied the visual system of Drosophila melanogaster in which histamine is the primary neurotransmitter released from photoreceptor cells. We report here that a novel mRNA splice variant of Drosophila VMAT (DVMAT-B) is expressed not in neurons but rather in a small subset of glia in the lamina of the fly's optic lobe. Histamine contents are reduced by mutation of dVMAT, but can be partially restored by specifically expressing DVMAT-B in glia. Our results suggest a novel role for a monoamine transporter in glia that may be relevant to histamine homeostasis in other systems.

Show MeSH