Sperm-Storage Defects and Live Birth in Drosophila Females Lacking Spermathecal Secretory Cells

Schnakenberg, Sandra L.; Matias, Wilfredo R.; Siegal, Mark L.

doi:10.1371/journal.pbio.1001192

Cited by 111 publications

(138 citation statements)

References 56 publications

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“…For example, in the beetle, Drusilla canaliculata, sperm migrate into the spermathecae (41), whereas the spermathecal gland in the boll weevil, Anthonomus grandis, is required for sperm activation, storage, clearance, and fertility (42,43) In D. melanogaster, sperm swim backward upon entering the female reproductive tract, and genetic ablation of the spermatheca secretory cells (SSCs) before mating leads to sperm storage defects: sperm fail to migrate into spermathcae and become inactive within the seminal receptacle (44)(45)(46). Moreover, SSC-ablated females display reduced fertility over time and ovovivipary (47). These experiments suggest that substances in spermathecae, SSCs, or perhaps other tissues are involved in the activation and chemoattraction of insect sperm (48).…”

Section: Significancementioning

confidence: 99%

Odorant receptor-mediated sperm activation in disease vector mosquitoes

Pitts

Liu

Zhou

et al. 2014

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

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Insects, such as the malaria vector mosquito, Anopheles gambiae, depend upon chemoreceptors to respond to volatiles emitted from a range of environmental sources, most notably blood meal hosts and oviposition sites. A subset of peripheral signaling pathways involved in these insect chemosensory-dependent behaviors requires the activity of heteromeric odorant receptor (OR) ion channel complexes and ligands for numerous A. gambiae ORs (AgOrs) have been identified. Although AgOrs are expressed in nonhead appendages, studies characterizing potential AgOr function in nonolfactory tissues have not been conducted. In the present study, we explore the possibility that AgOrs mediate responses of spermatozoa to endogenous signaling molecules in A. gambiae. In addition to finding AgOr transcript expression in testes, we show that the OR coreceptor, AgOrco, is localized to the flagella of A. gambiae spermatozoa where Orco-specific agonists, antagonists, and other odorant ligands robustly activate flagella beating in an Orco-dependent process. We also demonstrate Orco expression and Orco-mediated activation of spermatozoa in the yellow fever mosquito, Aedes aegypti. Moreover, we find Orco localization in testes across distinct insect taxa and posit that OR-mediated responses in spermatozoa may represent a general characteristic of insect reproduction and an example of convergent evolution.transcriptomics | cell signaling | gamete | chemical ecology | Culicidae

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Section: Significancementioning

confidence: 99%

Odorant receptor-mediated sperm activation in disease vector mosquitoes

Pitts

Liu

Zhou

et al. 2014

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

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“…Both Nep1 and Nep2 are highly expressed in the CNS and the spermathecae, two tissues that are known to influence egg laying (Yang et al 2009;Schnakenberg et al 2011;Sun and Spradling 2013). Nep2 is also expressed in the border cells of the follicular epithelium, which are important for micropyle development and for anterior-posterior polarity in the egg (Furriols et al 2007).…”

Section: Characterization Of the Hatchability Defects In Nep2 Null Mumentioning

confidence: 99%

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

et al. 2014

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Members of the M13 class of metalloproteases have been implicated in diseases and in reproductive fitness. Nevertheless, their physiological role remains poorly understood. To obtain a tractable model with which to analyze this protein family's function, we characterized the gene family in Drosophila melanogaster and focused on reproductive phenotypes. The D. melanogaster genome contains 24 M13 class protease homologs, some of which are orthologs of human proteases, including neprilysin. Many are expressed in the reproductive tracts of either sex. Using RNAi we individually targeted the five Nep genes most closely related to vertebrate neprilysin, Nep1-5, to investigate their roles in reproduction. A reduction in Nep1, Nep2, or Nep4 expression in females reduced egg laying. Nep1 and Nep2 are required in the CNS and the spermathecae for wild-type fecundity. Females that are null for Nep2 also show defects as hosts of sperm competition as well as an increased rate of depletion for stored sperm. Furthermore, eggs laid by Nep2 mutant females are fertilized normally, but arrest early in embryonic development. In the male, only Nep1 was required to induce normal patterns of female egg laying. Reduction in the expression of Nep2-5 in the male did not cause any dramatic effects on reproductive fitness, which suggests that these genes are either nonessential for male fertility or perform redundant functions. Our results suggest that, consistent with the functions of neprilysins in mammals, these proteins are also required for reproduction in Drosophila, opening up this model system for further functional analysis of this protein class and their substrates. P ROTEASES play key roles in diverse physiological systems. One such family of metalloproteases, the M13 class of neutral endopeptidases, consists mainly of membranebound zinc proteases that are involved in the processing of neuropeptides and peptide hormones (reviewed in Turner et al. 2000;Turner et al. 2001;Bland et al. 2008). In mammals, seven members of this family have been identified, of which neprilysin (NEP) and endothelin converting enzyme (ECE) are the best studied. These proteins have been implicated in various diseases including cardiovascular disease (Segura and Ruilope 2011;Wick et al. 2011), Alzheimer's disease (Mulder et al. 2012;Klein et al. 2013), inflammation and inflammatory disorders (Wong et al. 2011), and cancer (Smollich et al. 2007;Maguer-Satta et al. 2011).In addition to their role in disease, NEPs are essential for development and reproduction in mammals. The mammalian Neprilysin-2, called NL1 in mice, is highly expressed in the testis. NL1-deficient males sire fewer pups, even though spermatogenesis appears to be unaffected (Carpentier et al. 2004). In females, NEP expression in the uterus is modulated by estrogen treatment in rats (Pinto et al. 1999) and during the estrogen/progesterone cycle in humans (Head et al. 1993). In female rats and mice, controlled degradation of tachykinins, particularly substance-P, by NEP in the uterus ...

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“…Studies in Drosophila have shown that the sperm storage organs act to nourish and protect sperm by creating an appropriate environment through secretion: genetic or targeted disruption of the secretory glandular cells or of the secretory pathway results in nonfunctional spermathecae and reduced fertility phenotypes (8)(9)(10)(11). Transcriptional and proteomic profiling of sperm storage organs and their secretions in Drosophila and Apis have identified pathways involved in carbohydrate and lipid metabolism, oxidative stress, and antimicrobial responses that are likely to play roles in nourishing and/or protecting sperm from damage caused by infection and reactive oxygen species (ROS) (9,(12)(13)(14)(15).…”

mentioning

confidence: 99%

Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae

Shaw

Teodori

Mitchell

et al. 2014

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

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Anopheles gambiae mosquitoes are major African vectors of malaria, a disease that kills more than 600,000 people every year. Given the spread of insecticide resistance in natural mosquito populations, alternative vector control strategies aimed at reducing the reproductive success of mosquitoes are being promoted. Unlike many other insects, An. gambiae females mate a single time in their lives and must use sperm stored in the sperm storage organ, the spermatheca, to fertilize a lifetime's supply of eggs. Maintenance of sperm viability during storage is therefore crucial to the reproductive capacity of these mosquitoes. However, to date, no information is available on the factors and mechanisms ensuring sperm functionality in the spermatheca. Here we identify cellular components and molecular mechanisms used by An. gambiae females to maximize their fertility. Pathways of energy metabolism, cellular transport, and oxidative stress are strongly regulated by mating in the spermatheca. We identify the mating-induced heme peroxidase (HPX) 15 as an important factor in long-term fertility, and demonstrate that its function is required during multiple gonotrophic cycles. We find that HPX15 induction is regulated by sexually transferred 20-hydroxy-ecdysone (20E), a steroid hormone that is produced by the male accessory glands and transferred during copulation, and that expression of this peroxidase is mediated via the 20E nuclear receptor. To our knowledge, our findings provide the first evidence of the mechanisms regulating fertility in Anopheles, and identify HPX15 as a target for vector control.

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Sperm-Storage Defects and Live Birth in Drosophila Females Lacking Spermathecal Secretory Cells

Abstract: Transgenic Drosophila are used to identify the functions of a small set of secretory cells that are typically associated with the sperm-storage organs of female insects.

Cited by 111 publications

References 56 publications

Odorant receptor-mediated sperm activation in disease vector mosquitoes

Odorant receptor-mediated sperm activation in disease vector mosquitoes

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae

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