Abstract
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.
Highlights
Regulated secretion of neurotransmitters, hormones and enzymes from neuronal, endocrine and exocrine cells typically involves fusion of specialised secretory compartments with the plasma membrane
Since release rate varies with the level of stimulation, it must be matched to dense-core granules (DCGs) biogenesis to replenish the DCG pool rapidly after secretion
To determine which Bone Morphogenetic Protein (BMP) receptors are expressed in secondary cell (SC), we first analysed a yellow fluorescent protein- (YFP-) tagged tkv gene trap line, tkvCPTI002487 [27]
Summary
Hormones and enzymes from neuronal, endocrine and exocrine cells typically involves fusion of specialised secretory compartments with the plasma membrane. Cargos are first clustered together at the trans-Golgi network, and bud off in membrane-bound compartments. They are sorted from non-DCG proteins by specific interactions with adaptor molecules [2] and condense together in a maturation process that requires intraluminal Ca2+ ions and acidification [3,4]. Cargo clustering at the trans-Golgi network involves cholesterol and lipid raft-like structures [7], and requires the activity of specific enzymes associated with lipid metabolism [8,1]
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