Myoinhibiting peptides are the ancestral ligands of the promiscuous Drosophila sex peptide receptor

Poels, Jeroen; Loy, Tom Van; Vandersmissen, Hans Peter; Hiel, Matthias B. Van; Soest, Sofie Van; Nachman, Ronald J.; Broeck, Jozef Vanden

doi:10.1007/s00018-010-0393-8

Cited by 101 publications

(109 citation statements)

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“…Despite the highly specific behavioural response, however, SPR is broadly expressed in the nervous system and the oviduct. SPR also binds myoinhibitory peptides (MIPs) with high affinity, which do not induce the SP-mediated postmating switch [17][18][19]. It therefore appears that SPR has additional functions.…”

Section: Introductionmentioning

confidence: 99%

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

et al. 2013

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Male-derived sex-peptide (SP) induces profound changes in the behaviour of Drosophila females, resulting in decreased receptivity to further mating and increased egg laying. SP can mediate the switch in female reproductive behaviours via a G protein-coupled receptor, SPR, in neurons expressing fruitless, doublesex and pickpocket. Whether SPR is the sole receptor and whether SP induces the postmating switch in a single pathway has not, to our knowledge been tested. Here we report that the SP response can be induced in the absence of SPR when SP is ectopically expressed in neurons or when SP, transferred by mating, can access neurons through a leaky blood brain barrier. Membrane-tethered SP can induce oviposition via doublesex, but not fruitless and pickpocket neurons in SPR mutant females. Although pickpocket and doublesex neurons rely on G(o) signalling to reduce receptivity and induce oviposition, G(o) signalling in fruitless neurons is required only to induce oviposition, but not to reduce receptivity. Our results show that SP's action in reducing receptivity and inducing oviposition can be separated in fruitless and doublesex neurons. Hence, the SP-induced postmating switch incorporates shared, but also distinct circuitry of fruitless, doublesex and pickpocket neurons and additional receptors.

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Section: Introductionmentioning

confidence: 99%

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

et al. 2013

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“…It has been demonstrated that SPR expression in a limited number of pickpocket-expressing neurons in the female common oviduct was sufficient to rescue the mutant phenotype, suggesting that these neurons are targeted by SP (Yang et al 2009;Hanin et al 2012). Interestingly, neuronally expressed SP reduced receptivity and increased oviposition in the absence of SPR, suggesting an additional pathway capable of inducing PMR (Haussmann et al 2013).Several studies have shown that myoinhibitory peptides (MIPs) are also potent ligands for SPR (Kim et al 2010;Poels et al 2010;Yamanaka et al 2010 Here, we developed a GFP-tagged SP (G-SP) derived from D. melanogaster and used it to visualize cross-species binding activity to female reproductive system of 11 species. G-SP binds to the oviducts of six species belonging to the D. melanogaster species group, but not to those outside the group.…”

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confidence: 99%

“…Several studies have shown that myoinhibitory peptides (MIPs) are also potent ligands for SPR (Kim et al 2010;Poels et al 2010;Yamanaka et al 2010 Here, we developed a GFP-tagged SP (G-SP) derived from D. melanogaster and used it to visualize cross-species binding activity to female reproductive system of 11 species. G-SP binds to the oviducts of six species belonging to the D. melanogaster species group, but not to those outside the group.…”

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confidence: 99%

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Visualizing Molecular Functions and Cross-Species Activity of Sex-Peptide in Drosophila

et al. 2015

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The Drosophila melanogaster sex-peptide (melSP) is a seminal fluid component that induces postmating responses (PMR) of females via the sex-peptide receptor (SPR) . Although SP orthologs are found in many Drosophila species, their functions remain poorly characterized. It is unknown whether SP functions are conserved across species or rather specific to each species. Here, we developed a GFP-tagged melSP (G-SP) and used it to visualize cross-species binding activity to the female reproductive system of various species. First we demonstrated that ectopically expressed G-SP induced PMR in D. melanogaster females and bound to the female reproductive system, most notably to the common oviduct. No binding occurred in the females lacking SPR, indicating that G-SP binding was dependent on SPR. Next we tested whether G-SP binds to the common oviducts from 11 Drosophila species using dissected reproductive tracts. The binding was observed in six species belonging to the D. melanogaster species group, but not to those outside the group. Injection of melSP reduced the receptivity of females belonging to the D. melanogaster species group, but not of those outside the group, being consistent with the ability to bind G-SP. Thus the SP-mediated PMR appears to be limited to this species group. SPR was expressed in the oviducts at high levels in this group; therefore, we speculate that an enhanced expression of SPR in the oviduct was critical to establish the SP-mediated PMR during evolution.KEYWORDS sex-peptide; SP receptor; GFP-tag; postmating response T HE mating behavior and physiology of Drosophila melanogaster females are dramatically modified after copulation: they reject courting males by extruding their ovipositor, a behavior not seen in virgin females and start to lay many eggs (Kubli 1992). Sex-peptide (SP), a seminal fluid peptide, has been shown to play a major role in eliciting postmating response (PMR). Injection of SP into the abdominal cavity of virgin females reduces receptivity and stimulates oviposition (Chen et al. 1988) and these phenotypes can be induced by ectopic expression of SP in virgin females (Aigaki et al. 1991). Furthermore, experiments involving an SP null mutant generated by gene targeting and dsRNAi-mediated gene knockdown unambiguously demonstrated that SP is a major component in inducing changes in receptivity, ovulation, and oviposition in mated females (Liu and Kubli 2003;Chapman et al. 2003). In addition, SP stimulates food intake (Hanin et al. 2011) and activates immune response genes (Peng et al. 2005b).An extensive transgenic RNAi screen identified a receptor for sex-peptide (SPR), a G-protein-coupled receptor broadly expressed in the female reproductive tracts and in some neural tissues (Yapici et al. 2008). Mutant females deleted for SPR do not respond to mating, accept repeated mating, and maintain a low level of oviposition (Yapici et al. 2008). It has been demonstrated that SPR expression in a limited number of pickpocket-expressing neurons in the female common oviduct was...

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“…MIP neuropeptides are characterized by a W-X 6-8 -Wamide motif (11). In Platynereis, the last but not the first tryptophan (W) residue is crucial for MIP receptor activation and hence induction of larval settlement.…”

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confidence: 99%

Neuropeptides control life-phase transitions

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Beets

2013

Proc. Natl. Acad. Sci. U.S.A.

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The growth toward adulthood occurs mainly through one or several intermediate stages or larval forms. Driven by environmental and internal state cues, all animals undergo one or more transitions during their life, which are accompanied by changes in morphology, physiology, and behavior. Larval settlement in the annelid Platynereis dumerilii is a prime example of such a life-phase transition. In PNAS, Conzelmann et al. (1) show that larval settlement is under the control of a myoinhibitory neuropeptide (MIP) produced by neurosecretory cells in the animal's brain.Platynereis is an emerging model organism for the study of animal development and behavior. This marine annelid worm belongs to the Lophotrochozoa, the third major branch of bilaterian animals next to Ecdysozoa (insects and nematode worms) and Chordata (lancelets, tunicates, and vertebrates). Genome investigation revealed that the genes of Platynereis are more closely related to those of vertebrates than to those of insects or nematodes. The urbilaterian ancestor of protostomes and deuterostomes likely had complex, intron-rich genes that are still present in Platynereis and human, but have been lost in insect and nematode genomes (2). The CNS of Platynereis shares a complex molecular architecture with that of vertebrates, implying that the urbilaterian ancestor also possessed a well-developed CNS (3). Platynereis has retained ancient sensorymotor circuits with low levels of integration, as well as combined sensory-neurosecretory cell types that are also found in the vertebrate forebrain (4, 5). In addition, the sensory-associative centers in the annelid brain, known as the mushroom bodies, show deep homology with the vertebrate cortex, which indicates that the origin of higher brain centers also dates back to prebilaterian times (6).Platynereis larvae swim for several days as plankton, change shape twice, and then turn into large segmented worms. Larval settlement is the process by which the planktonic larva stops swimming, explores, attaches to a substrate, and begins its benthic life (7). The transition to a next life-cycle stage is a dynamic event. Larvae can reject one site and select another for settlement. Such active site selection is often mediated by environmental cues. Although a variety of chemicals, including proteins, free fatty acids, polysaccharides, inorganic ions, and neurotransmitters, have been proposed as inducers of larval settlement in marine annelid worms, no internal regulator had so far been identified.The most diverse class of signaling molecules in the CNS are neuropeptides, short sequences of amino acids that act through binding and activation of G protein-coupled receptors (8). By operating as hormones, neurotransmitters, or neuromodulators, neuropeptides are involved in many biological processes, such as reproduction, metabolism, feeding, circadian rhythms, sensorimotor integration, adaptive behaviors, and cognition. It has become clear that many neuropeptidergic systems have been conserved throughout the animal kingdom (9)....

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Myoinhibiting peptides are the ancestral ligands of the promiscuous Drosophila sex peptide receptor

Cited by 101 publications

References 58 publications

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

Visualizing Molecular Functions and Cross-Species Activity of Sex-Peptide in Drosophila

Neuropeptides control life-phase transitions

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