Regulation of Dense-Core Granule Replenishment by Autocrine BMP Signalling in Drosophila Secondary Cells.

Regulated secretion by glands and neurons involves release of signalling molecules and enzymes selectively concentrated in dense-core granules (DCGs). Although we understand how many secretagogues stimulate DCG release, how DCG biogenesis is then accelerated to replenish the DCG pool remains poorly...

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Main Authors: Siamak Redhai, Josephine E E U Hellberg, Mark Wainwright, Sumeth W Perera, Felix Castellanos, Benjamin Kroeger, Carina Gandy, Aaron Leiblich, Laura Corrigan, Thomas Hilton, Benjamin Patel, Shih-Jung Fan, Freddie Hamdy, Deborah C I Goberdhan, Clive Wilson
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-10-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5065122?pdf=render
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spelling doaj-d77d8f6fd0594162acd3177dbbd6980c2020-11-25T02:49:25ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042016-10-011210e100636610.1371/journal.pgen.1006366Regulation of Dense-Core Granule Replenishment by Autocrine BMP Signalling in Drosophila Secondary Cells.Siamak RedhaiJosephine E E U HellbergMark WainwrightSumeth W PereraFelix CastellanosBenjamin KroegerCarina GandyAaron LeiblichLaura CorriganThomas HiltonBenjamin PatelShih-Jung FanFreddie HamdyDeborah C I GoberdhanClive WilsonRegulated secretion by glands and neurons involves release of signalling molecules and enzymes selectively concentrated in dense-core granules (DCGs). Although we understand how many secretagogues stimulate DCG release, how DCG biogenesis is then accelerated to replenish the DCG pool remains poorly characterised. Here we demonstrate that each prostate-like secondary cell (SC) in the paired adult Drosophila melanogaster male accessory glands contains approximately ten large DCGs, which are loaded with the Bone Morphogenetic Protein (BMP) ligand Decapentaplegic (Dpp). These DCGs can be marked in living tissue by a glycophosphatidylinositol (GPI) lipid-anchored form of GFP. In virgin males, BMP signalling is sporadically activated by constitutive DCG secretion. Upon mating, approximately four DCGs are typically released immediately, increasing BMP signalling, primarily via an autocrine mechanism. Using inducible knockdown specifically in adult SCs, we show that secretion requires the Soluble NSF Attachment Protein, SNAP24. Furthermore, mating-dependent BMP signalling not only promotes cell growth, but is also necessary to accelerate biogenesis of new DCGs, restoring DCG number within 24 h. Our analysis therefore reveals an autocrine BMP-mediated feedback mechanism for matching DCG release to replenishment as secretion rates fluctuate, and might explain why in other disease-relevant systems, like pancreatic β-cells, BMP signalling is also implicated in the control of secretion.http://europepmc.org/articles/PMC5065122?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Siamak Redhai
Josephine E E U Hellberg
Mark Wainwright
Sumeth W Perera
Felix Castellanos
Benjamin Kroeger
Carina Gandy
Aaron Leiblich
Laura Corrigan
Thomas Hilton
Benjamin Patel
Shih-Jung Fan
Freddie Hamdy
Deborah C I Goberdhan
Clive Wilson
spellingShingle Siamak Redhai
Josephine E E U Hellberg
Mark Wainwright
Sumeth W Perera
Felix Castellanos
Benjamin Kroeger
Carina Gandy
Aaron Leiblich
Laura Corrigan
Thomas Hilton
Benjamin Patel
Shih-Jung Fan
Freddie Hamdy
Deborah C I Goberdhan
Clive Wilson
Regulation of Dense-Core Granule Replenishment by Autocrine BMP Signalling in Drosophila Secondary Cells.
PLoS Genetics
author_facet Siamak Redhai
Josephine E E U Hellberg
Mark Wainwright
Sumeth W Perera
Felix Castellanos
Benjamin Kroeger
Carina Gandy
Aaron Leiblich
Laura Corrigan
Thomas Hilton
Benjamin Patel
Shih-Jung Fan
Freddie Hamdy
Deborah C I Goberdhan
Clive Wilson
author_sort Siamak Redhai
title Regulation of Dense-Core Granule Replenishment by Autocrine BMP Signalling in Drosophila Secondary Cells.
title_short Regulation of Dense-Core Granule Replenishment by Autocrine BMP Signalling in Drosophila Secondary Cells.
title_full Regulation of Dense-Core Granule Replenishment by Autocrine BMP Signalling in Drosophila Secondary Cells.
title_fullStr Regulation of Dense-Core Granule Replenishment by Autocrine BMP Signalling in Drosophila Secondary Cells.
title_full_unstemmed Regulation of Dense-Core Granule Replenishment by Autocrine BMP Signalling in Drosophila Secondary Cells.
title_sort regulation of dense-core granule replenishment by autocrine bmp signalling in drosophila secondary cells.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2016-10-01
description Regulated secretion by glands and neurons involves release of signalling molecules and enzymes selectively concentrated in dense-core granules (DCGs). Although we understand how many secretagogues stimulate DCG release, how DCG biogenesis is then accelerated to replenish the DCG pool remains poorly characterised. Here we demonstrate that each prostate-like secondary cell (SC) in the paired adult Drosophila melanogaster male accessory glands contains approximately ten large DCGs, which are loaded with the Bone Morphogenetic Protein (BMP) ligand Decapentaplegic (Dpp). These DCGs can be marked in living tissue by a glycophosphatidylinositol (GPI) lipid-anchored form of GFP. In virgin males, BMP signalling is sporadically activated by constitutive DCG secretion. Upon mating, approximately four DCGs are typically released immediately, increasing BMP signalling, primarily via an autocrine mechanism. Using inducible knockdown specifically in adult SCs, we show that secretion requires the Soluble NSF Attachment Protein, SNAP24. Furthermore, mating-dependent BMP signalling not only promotes cell growth, but is also necessary to accelerate biogenesis of new DCGs, restoring DCG number within 24 h. Our analysis therefore reveals an autocrine BMP-mediated feedback mechanism for matching DCG release to replenishment as secretion rates fluctuate, and might explain why in other disease-relevant systems, like pancreatic β-cells, BMP signalling is also implicated in the control of secretion.
url http://europepmc.org/articles/PMC5065122?pdf=render
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