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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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DVMAT-B is not detected in photoreceptor cells and co-localizes with a marker for Drosophila glia.A primary antibody to the protein Tan (A) (green) labels the photoreceptor cell bodies and their axons that extend into the lamina (La) and medulla (Me), seen in horizontal cryostat sections of the head. Co-labeling with anti-B2 (B) (magenta) shows no overlap with Tan in merged images (C). Glia were labeled using repo-Gal4 to drive expression of the plasma membrane marker mCD8-GFP (D,G) (green). Some glial processes extend into the medulla (D,G) (small arrowheads). DVMAT-B was co-labeled using anti-B2 (E,H) (magenta). The merged images (F,I) show robust co-localization of DVMAT-B to profiles enclosed by glial cell membranes in the distal lamina, and additional, faint co-labeling of processes that extend distally into the retina (F,I) (large arrowheads). (G–I) Enlarged views of (D–F), to show the co-localization of the two signals. Bars: (A–F) 50 microns, (G–I) 10 microns.
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pgen-1000245-g004: DVMAT-B is not detected in photoreceptor cells and co-localizes with a marker for Drosophila glia.A primary antibody to the protein Tan (A) (green) labels the photoreceptor cell bodies and their axons that extend into the lamina (La) and medulla (Me), seen in horizontal cryostat sections of the head. Co-labeling with anti-B2 (B) (magenta) shows no overlap with Tan in merged images (C). Glia were labeled using repo-Gal4 to drive expression of the plasma membrane marker mCD8-GFP (D,G) (green). Some glial processes extend into the medulla (D,G) (small arrowheads). DVMAT-B was co-labeled using anti-B2 (E,H) (magenta). The merged images (F,I) show robust co-localization of DVMAT-B to profiles enclosed by glial cell membranes in the distal lamina, and additional, faint co-labeling of processes that extend distally into the retina (F,I) (large arrowheads). (G–I) Enlarged views of (D–F), to show the co-localization of the two signals. Bars: (A–F) 50 microns, (G–I) 10 microns.

Mentions: To further examine the localization of DVMAT-B, we performed co-labeling experiments using the antibodies specific for DVMAT-B: anti-B1 and anti-B2. To establish the relationship of DVMAT-B labeling to photoreceptors, we first performed co-labelings using an antibody to the gene product of tan. Although originally identified as a mutation affecting pigmentation in the cuticle [43], Tan protein also localizes to photoreceptors, where it converts recycled carcinine to histamine [36],[37],[44]. Labeling with anti-B2 (red) and anti-Tan (green) revealed a mutually exclusive pattern of expression, indicating that DVMAT-B was not expressed in photoreceptor cells (Figure 4A–4C). Rather, it appeared to bracket the photoreceptor cell axons where they extended beneath the retina, in a position beneath the basement membrane. Co-labeling with anti-B1 and the photoreceptor specific antibody MAb24B10 [65],[66] confirmed this relationship (data not shown).


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)

DVMAT-B is not detected in photoreceptor cells and co-localizes with a marker for Drosophila glia.A primary antibody to the protein Tan (A) (green) labels the photoreceptor cell bodies and their axons that extend into the lamina (La) and medulla (Me), seen in horizontal cryostat sections of the head. Co-labeling with anti-B2 (B) (magenta) shows no overlap with Tan in merged images (C). Glia were labeled using repo-Gal4 to drive expression of the plasma membrane marker mCD8-GFP (D,G) (green). Some glial processes extend into the medulla (D,G) (small arrowheads). DVMAT-B was co-labeled using anti-B2 (E,H) (magenta). The merged images (F,I) show robust co-localization of DVMAT-B to profiles enclosed by glial cell membranes in the distal lamina, and additional, faint co-labeling of processes that extend distally into the retina (F,I) (large arrowheads). (G–I) Enlarged views of (D–F), to show the co-localization of the two signals. Bars: (A–F) 50 microns, (G–I) 10 microns.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000245-g004: DVMAT-B is not detected in photoreceptor cells and co-localizes with a marker for Drosophila glia.A primary antibody to the protein Tan (A) (green) labels the photoreceptor cell bodies and their axons that extend into the lamina (La) and medulla (Me), seen in horizontal cryostat sections of the head. Co-labeling with anti-B2 (B) (magenta) shows no overlap with Tan in merged images (C). Glia were labeled using repo-Gal4 to drive expression of the plasma membrane marker mCD8-GFP (D,G) (green). Some glial processes extend into the medulla (D,G) (small arrowheads). DVMAT-B was co-labeled using anti-B2 (E,H) (magenta). The merged images (F,I) show robust co-localization of DVMAT-B to profiles enclosed by glial cell membranes in the distal lamina, and additional, faint co-labeling of processes that extend distally into the retina (F,I) (large arrowheads). (G–I) Enlarged views of (D–F), to show the co-localization of the two signals. Bars: (A–F) 50 microns, (G–I) 10 microns.
Mentions: To further examine the localization of DVMAT-B, we performed co-labeling experiments using the antibodies specific for DVMAT-B: anti-B1 and anti-B2. To establish the relationship of DVMAT-B labeling to photoreceptors, we first performed co-labelings using an antibody to the gene product of tan. Although originally identified as a mutation affecting pigmentation in the cuticle [43], Tan protein also localizes to photoreceptors, where it converts recycled carcinine to histamine [36],[37],[44]. Labeling with anti-B2 (red) and anti-Tan (green) revealed a mutually exclusive pattern of expression, indicating that DVMAT-B was not expressed in photoreceptor cells (Figure 4A–4C). Rather, it appeared to bracket the photoreceptor cell axons where they extended beneath the retina, in a position beneath the basement membrane. Co-labeling with anti-B1 and the photoreceptor specific antibody MAb24B10 [65],[66] confirmed this relationship (data not shown).

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