Calcium and egg activation in Drosophila

Sartain, Caroline V.; Wolfner, Mariana F.

doi:10.1016/j.ceca.2012.11.008

Cited by 51 publications

(51 citation statements)

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“…We also found that stage 14 eggs were thinner, relatively translucent, and often did not activate (incomplete inflation) in PBS (21). Eggs were depleted or devoid of yolk (Fig.…”

Section: Disruption Of Eth Signaling Reduces Fecundity and Impairs VImentioning

confidence: 75%

Endocrine network essential for reproductive success in Drosophila melanogaster

Meiselman

Lee

Tran

et al. 2017

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

140

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Ecdysis-triggering hormone (ETH) was originally discovered and characterized as a molt termination signal in insects through its regulation of the ecdysis sequence. Here we report that ETH persists in adult Drosophila melanogaster, where it functions as an obligatory allatotropin to promote juvenile hormone (JH) production and reproduction. ETH signaling deficits lead to sharply reduced JH levels and consequent reductions of ovary size, egg production, and yolk deposition in mature oocytes. Expression of ETH and ETH receptor genes is in turn dependent on ecdysone (20E). Furthermore, 20E receptor knockdown specifically in Inka cells reduces fecundity. Our findings indicate that the canonical developmental roles of 20E, ETH, and JH during juvenile stages are repurposed to function as an endocrine network essential for reproductive success.ecdysis triggering hormone | ecdysone | juvenile hormone | fecundity | oogenesis T he life history of insects is characterized by radical morphogenetic transformations, whereby tissues are reorganized and hormones are repurposed for roles associated with stage-specific functions. During development, larvae complete each molt by shedding the cuticle under control of ecdysis triggering hormones (ETHs) targeting central peptidergic ensembles to orchestrate an innate behavioral sequence (1-3). Previous observations that Inka cells, the sole source of ETHs, persist into the adult stage (4) suggest possible reproductive functions for these peptides.We hypothesized that ETHs regulate juvenile hormone (JH) levels, based on the report of ETH receptor (ETHR) expression in the corpora allata (CA) of the silkworm, Bombyx mori (5). Evidence that ETH functions as an allatotropin in the yellow fever mosquito Aedes aegypti came from a recent study showing its activation of JH acid methyltransferase (6).JH is a sesquiterpenoid hormone with well-known morphogenetic and gonadotropic functions. In Drosophila, adult phenotypes resulting from reduction of JH levels have been characterized through induction of cell death in the CA or through enhancement of its degradation (7,8). Based on evidence from studies on Bombyx and Aedes, we investigated whether ETH functions as an allatotropin in adult Drosophila and the extent to which it may be necessary for reproductive functions.Previous studies showed that ecdysone (20E) regulates synthesis and release of ETH and expression of ETHR during larval stages of moths and mosquitoes (9-12). More recently, selftranscribing active regulatory region sequencing (STARR-Seq) data confirm that 20E induces 20E receptor (EcR) enhancer activity in promoters of both ETH and ETHR genes (13). Because circulating 20E levels are of major physiological and reproductive relevance (14), we also asked whether 20E influences ETH gene expression during the adult stage.Here we describe functional roles for 20E, ETH, and JH as a hormonal triad essential for reproductive success in Drosophila.In particular, we confirm persistence of ETH signaling throughout adulthood and demonstrate it...

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“…We also found that stage 14 eggs were thinner, relatively translucent, and often did not activate (incomplete inflation) in PBS (21). Eggs were depleted or devoid of yolk (Fig.…”

Section: Disruption Of Eth Signaling Reduces Fecundity and Impairs VImentioning

confidence: 75%

Endocrine network essential for reproductive success in Drosophila melanogaster

Meiselman

Lee

Tran

et al. 2017

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

140

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“…41). Three genes of the transient receptor potential (TRP) family encoding mechanosensitive ion channels are expressed in the ovary, but their role has not been assessed during Drosophila egg activation.…”

Section: Extracellular Ca 2+ Enters the Oocyte Through Mechanosensitivementioning

confidence: 99%

Calcium waves occur as Drosophila oocytes activate

Kaneuchi

Sartain

Takeo

et al. 2015

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

Self Cite

114

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Egg activation is the process by which a mature oocyte becomes capable of supporting embryo development. In vertebrates and echinoderms, activation is induced by fertilization. Molecules introduced into the egg by the sperm trigger progressive release of intracellular calcium stores in the oocyte. Calcium wave(s) spread through the oocyte and induce completion of meiosis, new macromolecular synthesis, and modification of the vitelline envelope to prevent polyspermy. However, arthropod eggs activate without fertilization: in the insects examined, eggs activate as they move through the female’s reproductive tract. Here, we show that a calcium wave is, nevertheless, characteristic of egg activation in Drosophila. This calcium rise requires influx of calcium from the external environment and is induced as the egg is ovulated. Pressure on the oocyte (or swelling by the oocyte) can induce a calcium rise through the action of mechanosensitive ion channels. Visualization of calcium fluxes in activating eggs in oviducts shows a wave of increased calcium initiating at one or both oocyte poles and spreading across the oocyte. In vitro, waves also spread inward from oocyte pole(s). Wave propagation requires the IP3 system. Thus, although a fertilizing sperm is not necessary for egg activation in Drosophila, the characteristic of increased cytosolic calcium levels spreading through the egg is conserved. Because many downstream signaling effectors are conserved in Drosophila, this system offers the unique perspective of egg activation events due solely to maternal components.

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“…Therefore, we conclude that Tsl accumulates at the plasma membrane between late oogenesis and fertilisation. In this period, the most prominent changes are related to egg activation, the conversion of the oocyte into an egg capable of supporting embryogenesis (Sartain and Wolfner, 2013). Although in higher organisms fertilisation is coupled to egg activation (Sartain and Wolfner, 2013), in Drosophila, as in many insects, these two events are independent, and egg activation takes place as the oocytes pass through the oviducts before becoming fertilised (Heifetz et al, 2001).…”

Section: Resultsmentioning

confidence: 99%

“…In this period, the most prominent changes are related to egg activation, the conversion of the oocyte into an egg capable of supporting embryogenesis (Sartain and Wolfner, 2013). Although in higher organisms fertilisation is coupled to egg activation (Sartain and Wolfner, 2013), in Drosophila, as in many insects, these two events are independent, and egg activation takes place as the oocytes pass through the oviducts before becoming fertilised (Heifetz et al, 2001). While passing through the oviduct, eggs swell, causing an increase in their Ca 2+ concentration, which in turn triggers many physiological events including resumption of meiosis of the female pronucleus, translation of maternal mRNAs and crosslinking of the vitelline membrane (Sartain and Wolfner, 2013).…”

Section: Resultsmentioning

confidence: 99%

“…Whether there is an as yet unidentified proteolytic step that is indeed tsl-dependent or whether Tsl is involved in a different process, the fact remains that a cleaved form of Trk produced in the oocyte does not require tsl function to activate the Tor receptor, whereas the full-length Trk protein does (Furriols et al, 1998;Casali and Casanova, 2001). It is also worth noting that anchorage of MACPF proteins depends on Ca 2+ (Voskoboinik et al, 2005), which is also required for egg activation (Sartain and Wolfner, 2013). Thus a change in Ca concentration might act to trigger Tsl translocation, linking it to egg activation and eggshell crosslinking (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Accumulation of the Drosophila Torso-like protein at the blastoderm plasma membrane suggests that it translocates from the eggshell

2015

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The eggshell serves as a depository for proteins that play an important role in early embryonic development. In particular, the Drosophila eggshell is responsible for transferring asymmetries from the egg chamber to specify the regions at both ends of the embryo through the uneven activation of the Torso (Tor) receptor in its membrane. This process relies on the restricted expression of the gene torso-like (tsl) in subpopulations of follicle cells during oogenesis and its protein accumulation at both poles of the eggshell, but it is not known how this signal is transmitted to the embryo. Here, we show that Tsl accumulates at the embryonic plasma membrane, even in the absence of the Tor receptor. However, during oogenesis, we detected Tsl accumulation only at the eggshell. These results suggest that there is a two-step mechanism to transfer the asymmetric positional cues from the egg chamber into the early embryo: initial anchoring of Tsl at the eggshell as it is secreted, followed by its later translocation to the egg plasma membrane, where it enables Tor receptor activation. Translocation of anchored determinants from the eggshell might then regulate the spatial and temporal control of early embryonic developmental processes.

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Calcium and egg activation in Drosophila

Cited by 51 publications

References 50 publications

Endocrine network essential for reproductive success in Drosophila melanogaster

Endocrine network essential for reproductive success in Drosophila melanogaster

Calcium waves occur as Drosophila oocytes activate

Accumulation of the Drosophila Torso-like protein at the blastoderm plasma membrane suggests that it translocates from the eggshell

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