Ovarian ecdysteroid biosynthesis and female germline stem cells

Ameku, Tomotsune; Yoshinari, Yuto; Fukuda, Ryūji; Niwa, Ryusuke

doi:10.1080/19336934.2017.1291472

Cited by 32 publications

(39 citation statements)

References 50 publications

(64 reference statements)

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“…SP is received by its specific receptor, sex peptide receptor (SPR), in a small subset of SPR-positive sensory neurons (SPSNs), which are located in the uterine lumen and send afferent axons into the tip of the abdominal ganglion ( Häsemeyer et al, 2009 ; Yapici et al, 2008 ). The SP-SPR signaling in the SPSNs stimulates the biosynthesis of the ovarian insect steroid hormones (ecdysteroids), which play an essential role in mating-induced GSC increase ( Ameku et al, 2017 ; Ameku and Niwa, 2016 ; Uryu et al, 2015 ). Because SPSNs do not directly innervate into the ovary, it is hypothesized that a signal and its signaling pathway are involved in bridging the gap between SPSNs and GSCs.…”

Section: Introductionmentioning

confidence: 99%

Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster

Yoshinari

Ameku

Kondo

et al. 2020

eLife

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Stem cells fuel the development and maintenance of tissues. Many studies have addressed how local signals from neighboring niche cells regulate stem cell identity and their proliferative potential. However, the regulation of stem cells by tissue-extrinsic signals in response to environmental cues remains poorly understood. Here we report that efferent octopaminergic neurons projecting to the ovary are essential for germline stem cell (GSC) increase in response to mating in female Drosophila. The neuronal activity of the octopaminergic neurons is required for mating-induced GSC increase as they relay the mating signal from sex peptide receptor-positive cholinergic neurons. Octopamine and its receptor Oamb are also required for mating-induced GSC increase via intracellular Ca2+ signaling. Moreover, we identified Matrix metalloproteinase-2 as a downstream component of the octopamine-Ca2+ signaling to induce GSC increase. Our study provides a mechanism describing how neuronal system couples stem cell behavior to environmental cues through stem cell niche signaling.

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Section: Introductionmentioning

confidence: 99%

Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster

Yoshinari

Ameku

Kondo

et al. 2020

eLife

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“…As we have previously reported, the RNAi of neverland (nvd), which encodes an 333 ecdysteroidogenic enzyme (Yoshiyama-Yanagawa et al, 2011;Yoshiyama et al, 2006) in the 334 escort cells, suppressed the mating-induced GSC increase ( Figure 3A) (Ameku et al, 2017;335 Ameku and Niwa, 2016). We also found a similar phenotype in the RNAi of ecdysone receptor 336 (EcR) in the escort cells ( Figure 3A).…”

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confidence: 60%

“…The biosynthesis and signaling of ecdysteroid in the ovary are required for the mating-induced 330 GSC increase (Ameku et al, 2017;Ameku and Niwa, 2016). Therefore, we next examined 331 whether ecdysteroid signaling has a pivotal role in the OA-Oamb-Ca 2+ -dependent GSC increase.…”

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confidence: 99%

Neuronal octopamine signaling regulates mating-induced germline stem cell proliferation in femaleDrosophila melanogaster

Yoshinari

Ameku

Kondo

et al. 2020

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27Stem cells fuel the development and maintenance of tissues. Many studies have addressed how 28 local signals from neighboring niche cells regulate stem cell identity and their proliferative 29 potential. However, the regulation of stem cells by tissue-extrinsic signals in response to external 30 cues remains poorly understood. Here we report that efferent octopaminergic neurons projecting 31 to the ovary are essential for germline stem cell (GSC) proliferation in response to mating in 32 female Drosophila. The neuronal activity of the octopaminergic neurons is required for mating-33 induced GSC proliferation as they relay the mating signal from Sex peptide receptor-positive 34 cholinergic neurons. Octopamine and its receptor Oamb are also required for mating-induced 35 GSC proliferation via intracellular Ca 2+ signaling. Moreover, we identified Matrix 36 metalloproteinase-2 as a downstream component of the octopamine-Ca 2+ signaling to induce 37 GSC proliferation. Our study provides a mechanism describing how neuronal system couples 38 stem cell behavior to external cues through stem cell niche signaling. 39 40 Kim et al., 2016; Nakada et al., 2014). Retinoic acid and thyroid hormone play essential roles in 52 the differentiation of testicular stem cells and neural stem cells, respectively (Gothié et al., 2017; 53 Ikami et al., 2015). In addition, mesenchymal stem cell proliferation is stimulated by adrenaline 54 (Wu et al., 2014). However, the when, how, and why these humoral factors are produced, 55 circulated, and received during stem cell regulation remain to be elucidated. 56The ovaries of the fruit fly Drosophila melanogaster are an excellent model system on 57how stem cell lineages are shaped by both local niche signals and tissue-extrinsic signals 58(Drummond-Barbosa, 2019). D. melanogaster ovary is composed of 16-20 chains of developing 59 egg chambers called ovarioles. The anterior-most region of which, known as the germarium, 60 contains germline stem cells (GSCs) that give rise to the eggs ( Figure 1A and B). GSCs are 61 adjacent to the somatic niche cells, which comprises cap cells, escort cells, and terminal filament 62 cells ( Figure 1A). After GSC divides, one daughter cell that remains attached to the niche cells 63 retains its GSC identity, whereas the remaining daughter cell is displaced away from the niche 64 cells and differentiates into cystoblast (CB). Each CB then undergoes differentiation into 15 65 nurse cells and 1 oocyte in each egg chamber, which is surrounded by somatic follicle cells. 66 GSC niche produces and secretes several local niche signals that regulate the balance 67 between GSC self-renewal and differentiation (Hayashi et al., 2020;Kirilly and Xie, 2007; 68 Spradling et al., 2011). For example, bone morphogenetic protein (BMP) ligands 69 Decapentaplegic (Dpp) and Glass bottom boat (Gbb) are produced from the niche cells and 70 directly activate BMP receptors in GSCs, leading to the repression of the differentiation inducer, 71 bag-of-marbles (bam) (Morrison and Spra...

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“…In fact, this latter may be mediated by Notch pathway. Ecdysone signalling induces Dl expression at the terminal filament in cell membranes, which activates N and determines the fate of these cells, which can become cap or escort cells (Ameku et al, 2017; Green et al, 2011; Hsu et al, 2019). Our results in B. germanica suggest that similar signalling networks occur in panoistic ovaries.…”

Section: Discussionmentioning

confidence: 99%

“…In insect ovaries, germ stem cells are located in niches in the germarium of each ovariole. The control of their proliferation and differentiation has been thoroughly studied, mainly in species with meroistic polytrophic ovaries such as the fruit fly Drosophila melanogaster (see Ameku et al, 2017; Belles and Piulachs, 2015; Dai et al, 2017). In contrast, the number of genes involved in regulating oogenesis so far identified in less modified panoistic ovaries such as those of the cockroaches including Blattella germanica is very limited.…”

Section: Introductionmentioning

confidence: 99%

eyes absentin the cockroach panoistic ovaries regulates proliferation and differentiation through ecdysone signalling

Ramos

Chelemen

Pagone

et al. 2019

Preprint

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21Eye absent (Eya) is a protein which has been structurally conserved from hydrozoans to 22 humans which has two functions: it is both a transcription cofactor and a protein 23 tyrosine phosphatase. Eya was first described in the fly Drosophila melanogaster for its 24 role in eye development, and the same functions were also later reported in less derived 25 insects. Studies on the involvement of Eya in insect oogenesis are limited to D. 26 melanogaster, which has meroistic ovaries. In this fly, Eya plays a fundamental role in 27 the first stages of ovarian development because Eya mutations abolish gonad formation. 28 In this present work we studied the function of Eya in the panoistic ovary of the 29 cockroach Blattella germanica. We demonstrated that Eya is essential for correct ovary 30 development also in this ovary type. In B. germanica ovaries, Eya affects both somatic 31 and germinal cells in the germarium and the vitellarium, acting differently in different 32 ovarian regions. Development of the basal ovarian follicles is arrested BgEya-depleted 33 females, while in the germaria, BgEya helps to the maintain the correct number of 34 somatic and germinal stem cells by regulating the expression of ecdysteroidogenic 35 genes in the ovary.36 37 38 39 40 41 42 43 44 45 46 KEYWORDS: panoistic ovary, ecdysone, Halloween genes, cell proliferation, insect 47 oogenesis, Notch 48 49 50 51Maintaining the stability of stem cells is crucial in every organism, and this is especially 52 important in the case of germ stem cells. Oogenesis describes the process of ovary 53 development from the time of germ stem cell differentiation until oocyte maturation. 54During oogenesis, oocytes must synthesize and accumulate all maternal factors needed 55 by embryos to complete their development, thus ensuring reproductive success. 56In insect ovaries, germ stem cells are located in niches in the germarium of each 57 ovariole. The control of their proliferation and differentiation has been thoroughly 58 studied, mainly in species with meroistic polytrophic ovaries such as the fruit fly 59 Drosophila melanogaster (see Ameku et al., 2017; Belles and Piulachs, 2015; Dai et al., 60 2017). In contrast, the number of genes involved in regulating oogenesis so far 61 identified in less modified panoistic ovaries such as those of the cockroaches including 62 Blattella germanica is very limited. This prevents study of the mechanisms that control 63 oocyte growth and maturation in these basal insects. B. germanica is emerging as a 64 choice model in which to study panoistic ovaries. In this cockroach, each ovary has 65 around 20 ovarioles and only the most basal ovarian follicle of each ovariole matures 66 during a given gonadotrophic cycle, a process that starts early in the last nymphal instar. 67The basal ovarian follicles are almost ready to mature in freshly ecdysed females, 68 whereas the development of the remaining ovarian follicles of each ovariole is arrested 69 until these basal ones are oviposited. 70In previous co...

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Ovarian ecdysteroid biosynthesis and female germline stem cells

Cited by 32 publications

References 50 publications

Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster

Neuronal octopamine signaling regulates mating-induced germline stem cell increase in female Drosophila melanogaster

Neuronal octopamine signaling regulates mating-induced germline stem cell proliferation in femaleDrosophila melanogaster

eyes absentin the cockroach panoistic ovaries regulates proliferation and differentiation through ecdysone signalling

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