A Pair of Oviduct-Born Pickpocket Neurons Important for Egg-Laying in Drosophila melanogaster

Lee, Hyunjin; Choi, Hyun Woo; Zhang, Chen; Park, Chul–Seung; Kim, Young-Joon

doi:10.14348/molcells.2016.0121

Cited by 14 publications

(16 citation statements)

References 37 publications

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“…To identify the type of neuron involved, we tested the consequence of NF-κB inactivation in two categories of cells previously implicated in controlling egg-laying behavior that are the ILP7 and ppk-positive neurons (Castellanos et al, 2013; Rezával et al, 2012; Lee et al, 2016). However, as shown Figure 5—figure supplement 1A, Fadd RNAi overexpression in these neurons did not prevent egg-laying drop post-infection.…”

Section: Resultsmentioning

confidence: 99%

Peptidoglycan sensing by octopaminergic neurons modulates Drosophila oviposition

Kurz

Charroux

Chaduli

et al. 2017

eLife

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As infectious diseases pose a threat to host integrity, eukaryotes have evolved mechanisms to eliminate pathogens. In addition to develop strategies reducing infection, animals can engage in behaviors that lower the impact of the infection. The molecular mechanisms by which microbes impact host behavior are not well understood. We demonstrate that bacterial infection of Drosophila females reduces oviposition and that peptidoglycan, the component that activates Drosophila antibacterial response, is also the elicitor of this behavioral change. We show that peptidoglycan regulates egg-laying rate by activating NF-κB signaling pathway in octopaminergic neurons and that, a dedicated peptidoglycan degrading enzyme acts in these neurons to buffer this behavioral response. This study shows that a unique ligand and signaling cascade are used in immune cells to mount an immune response and in neurons to control fly behavior following infection. This may represent a case of behavioral immunity.DOI: http://dx.doi.org/10.7554/eLife.21937.001

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Section: Resultsmentioning

confidence: 99%

Peptidoglycan sensing by octopaminergic neurons modulates Drosophila oviposition

Kurz

Charroux

Chaduli

et al. 2017

eLife

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“…To further investigate the subset of NPFR expressing cell-types involved in egg-lay depression, we tested the consequence of NPFR removal in previously identified neuronal subsets implicated in egg-laying behavior [ 53 , 56 , 57 ]. Female flies with NPFR knockdown in Tdc2 -marked octopaminergic neurons ( Tdc2-GAL4 ) [ 58 ] or a pair of oviduct-born pickpocket neurons ( ppk-GAL4 ) [ 56 , 59 ] or in pLB1 cells that mediate egg-lay decrease after bacterial infection ( pLB1-GAL4 ) [ 57 ] did not affect the egg-lay reduction observed after 24 hrs of wasp exposure ( Fig 7B ). Later, NPFR knockdown using GAL4 drivers that mark different regions of the fan-shaped body, a substructure of Drosophila central complex, whose function is implicated in inter-species communication [ 60 ] failed to suppress Lb17-induced behavioral modifications ( Fig 7C ).…”

Section: Resultsmentioning

confidence: 99%

“…UAS-NPF RNAi (KK 108772), UAS-NPFR RNAi (KK 107663 and GD 9605) [ 45 ] and UAS-Orco RNAi (KK 100825) were from the Vienna Drosophila Resource Center (VDRC). Or83b-GAL4 [ 28 ], MB247-GAL4 [ 39 ], Tdc2-GAL4 [ 58 ], and UAS-mCD8 :: GFP from Mani Ramaswami, ey-GAL4 from Yashi Ahmed, nos-GAL4-VP16 and mat ∝-GAL4-VP16 from Sharon E. Bickel, ppk-GAL4 [ 56 , 59 ] and pLB1-GAL4 [ 57 ] from Julien Royet and Tk-gut-GAL4 [ 51 , 52 ] from Irene Miguel-Aliaga. As previously described, the mutants NPF SK1 , NPF SK2 , and NPFR SK8 were generated in an yw background using CRISPR/Cas9 method [ 45 , 46 ].…”

Section: Methodsmentioning

confidence: 99%

Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila

et al. 2021

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Drosophila larvae and pupae are at high risk of parasitoid infection in nature. To circumvent parasitic stress, fruit flies have developed various survival strategies, including cellular and behavioral defenses. We show that adult Drosophila females exposed to the parasitic wasps, Leptopilina boulardi, decrease their total egg-lay by deploying at least two strategies: Retention of fully developed follicles reduces the number of eggs laid, while induction of caspase-mediated apoptosis eliminates the vitellogenic follicles. These reproductive defense strategies require both visual and olfactory cues, but not the MB247-positive mushroom body neuronal function, suggesting a novel mode of sensory integration mediates reduced egg-laying in the presence of a parasitoid. We further show that neuropeptide F (NPF) signaling is necessary for both retaining matured follicles and activating apoptosis in vitellogenic follicles. Whereas previous studies have found that gut-derived NPF controls germ stem cell proliferation, we show that sensory-induced changes in germ cell development specifically require brain-derived NPF signaling, which recruits a subset of NPFR-expressing cell-types that control follicle development and retention. Importantly, we found that reduced egg-lay behavior is specific to parasitic wasps that infect the developing Drosophila larvae, but not the pupae. Our findings demonstrate that female fruit flies use multimodal sensory integration and neuroendocrine signaling via NPF to engage in parasite-specific cellular and behavioral survival strategies.

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“…In addition, sensory ppk + neurons are also crucial for the female PMR (Häsemeyer et al 2009;Yang et al 2009). The male seminal fluid protein SP binds to the SPR expressed in female ppk + neurons to silence these neurons and elicit the PMR (Yapici et al 2008;Häsemeyer et al 2009;Yang et al 2009;Rezával et al 2012;Lee et al 2016). Both SP and SPR are known to influence sperm competition outcome (Chow et al 2010;Castillo and Moyle 2014).…”

Section: Discussionmentioning

confidence: 99%

Female Genetic Contributions to Sperm Competition in Drosophila melanogaster

et al. 2019

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In many species, sperm can remain viable in the reproductive tract of a female well beyond the typical interval to remating. This creates an opportunity for sperm from different males to compete for oocyte fertilization inside the female’s reproductive tract. In Drosophila melanogaster, sperm characteristics and seminal fluid content affect male success in sperm competition. On the other hand, although genome-wide association studies (GWAS) have demonstrated that female genotype plays a role in sperm competition outcome as well, the biochemical, sensory, and physiological processes by which females detect and selectively use sperm from different males remain elusive. Here, we functionally tested 26 candidate genes implicated via a GWAS for their contribution to the female’s role in sperm competition, measured as changes in the relative success of the first male to mate (P1). Of these 26 candidates, we identified eight genes that affect P1 when knocked down in females, and showed that five of them do so when knocked down in the female nervous system. In particular, Rim knockdown in sensory pickpocket (ppk)+ neurons lowered P1, confirming previously published results, and a novel candidate, caup, lowered P1 when knocked down in octopaminergic Tdc2+ neurons. These results demonstrate that specific neurons in the female’s nervous system play a functional role in sperm competition and expand our understanding of the genetic, neuronal, and mechanistic basis of female responses to multiple matings. We propose that these neurons in females are used to sense, and integrate, signals from courtship or ejaculates, to modulate sperm competition outcome accordingly.

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A Pair of Oviduct-Born Pickpocket Neurons Important for Egg-Laying in Drosophila melanogaster

Cited by 14 publications

References 37 publications

Peptidoglycan sensing by octopaminergic neurons modulates Drosophila oviposition

Peptidoglycan sensing by octopaminergic neurons modulates Drosophila oviposition

Neuropeptide F signaling regulates parasitoid-specific germline development and egg-laying in Drosophila

Female Genetic Contributions to Sperm Competition in Drosophila melanogaster

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