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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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Immuno-EM shows that DVMAT in the distal lamina labels glia.(A) Electron micrograph of a tangential section through the proximal retina (Re) with seven rhabdomeres (arrowheads) visible in two complete cross-sections of ommatidia. The basement membrane, bm arrows in (A,B), separates the retina from the underlying lamina. Electron-dense gold particles lie just beneath the basement membrane. Beneath this band of labeling, an additional small profile quite distinct in appearance (double arrowhead) also expresses label, and may represent the profile of a serotonin-containing nerve terminal. (B) Higher magnification views of the labeled fenestrated glia and photoreceptor axons in the distal lamina. Gold particles (arrowhead) overlie the fenestrated glia. bm, basement membrane; pa, photoreceptor axons; t, tracheae; lc, glial nuclei. Bars: (A) 5 microns, (B) 2 microns.
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pgen-1000245-g005: Immuno-EM shows that DVMAT in the distal lamina labels glia.(A) Electron micrograph of a tangential section through the proximal retina (Re) with seven rhabdomeres (arrowheads) visible in two complete cross-sections of ommatidia. The basement membrane, bm arrows in (A,B), separates the retina from the underlying lamina. Electron-dense gold particles lie just beneath the basement membrane. Beneath this band of labeling, an additional small profile quite distinct in appearance (double arrowhead) also expresses label, and may represent the profile of a serotonin-containing nerve terminal. (B) Higher magnification views of the labeled fenestrated glia and photoreceptor axons in the distal lamina. Gold particles (arrowhead) overlie the fenestrated glia. bm, basement membrane; pa, photoreceptor axons; t, tracheae; lc, glial nuclei. Bars: (A) 5 microns, (B) 2 microns.

Mentions: Even though it has been suggested that dVMAT mRNA is expressed in the fenestrated glia [56], the localization of a vesicular monoamine transporter to glial cells had not been conclusively demonstrated. Both because of the heterodox nature of our observation and the difficulty inherent in interpreting co-localization from light micrographs, we performed additional immunolabelings at higher resolution, using electron microscopy (EM). For these experiments we used the anti-N antibody to visualize DVMAT-A+B; anti-N but not anti-B1 gave a good EM signal using the pre-embedding method. A high concentration of silver-enhanced gold particles was readily detected in the lamina, proximal to the basement membrane (Figure 5A), with some additional labeling seen in the retina itself. In addition, small profiles in the lamina cortex were also labeled. These may be profiles of serotonin-containing nerve terminals that express DVMAT-A [40], and are consistent with the punctate lamina labeling seen in light micrographs with anti-N (see Figure 3). The labeled glia were penetrated by ommatidial bundles of photoreceptor axons and also had extensive convolutions of their proximal cell surface (Figure 5B), consistent with the morphology of the fenestrated glia [62]. The convoluted morphology of the glia membranes made it difficult to determine the precise subcellular localization of DVMAT in material prepared by the pre-embedding method.


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)

Immuno-EM shows that DVMAT in the distal lamina labels glia.(A) Electron micrograph of a tangential section through the proximal retina (Re) with seven rhabdomeres (arrowheads) visible in two complete cross-sections of ommatidia. The basement membrane, bm arrows in (A,B), separates the retina from the underlying lamina. Electron-dense gold particles lie just beneath the basement membrane. Beneath this band of labeling, an additional small profile quite distinct in appearance (double arrowhead) also expresses label, and may represent the profile of a serotonin-containing nerve terminal. (B) Higher magnification views of the labeled fenestrated glia and photoreceptor axons in the distal lamina. Gold particles (arrowhead) overlie the fenestrated glia. bm, basement membrane; pa, photoreceptor axons; t, tracheae; lc, glial nuclei. Bars: (A) 5 microns, (B) 2 microns.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000245-g005: Immuno-EM shows that DVMAT in the distal lamina labels glia.(A) Electron micrograph of a tangential section through the proximal retina (Re) with seven rhabdomeres (arrowheads) visible in two complete cross-sections of ommatidia. The basement membrane, bm arrows in (A,B), separates the retina from the underlying lamina. Electron-dense gold particles lie just beneath the basement membrane. Beneath this band of labeling, an additional small profile quite distinct in appearance (double arrowhead) also expresses label, and may represent the profile of a serotonin-containing nerve terminal. (B) Higher magnification views of the labeled fenestrated glia and photoreceptor axons in the distal lamina. Gold particles (arrowhead) overlie the fenestrated glia. bm, basement membrane; pa, photoreceptor axons; t, tracheae; lc, glial nuclei. Bars: (A) 5 microns, (B) 2 microns.
Mentions: Even though it has been suggested that dVMAT mRNA is expressed in the fenestrated glia [56], the localization of a vesicular monoamine transporter to glial cells had not been conclusively demonstrated. Both because of the heterodox nature of our observation and the difficulty inherent in interpreting co-localization from light micrographs, we performed additional immunolabelings at higher resolution, using electron microscopy (EM). For these experiments we used the anti-N antibody to visualize DVMAT-A+B; anti-N but not anti-B1 gave a good EM signal using the pre-embedding method. A high concentration of silver-enhanced gold particles was readily detected in the lamina, proximal to the basement membrane (Figure 5A), with some additional labeling seen in the retina itself. In addition, small profiles in the lamina cortex were also labeled. These may be profiles of serotonin-containing nerve terminals that express DVMAT-A [40], and are consistent with the punctate lamina labeling seen in light micrographs with anti-N (see Figure 3). The labeled glia were penetrated by ommatidial bundles of photoreceptor axons and also had extensive convolutions of their proximal cell surface (Figure 5B), consistent with the morphology of the fenestrated glia [62]. The convoluted morphology of the glia membranes made it difficult to determine the precise subcellular localization of DVMAT in material prepared by the pre-embedding method.

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
Related in: MedlinePlus