Counting in oogenesis

Green, Delbert; Sarikaya, Didem P.; Extavour, Cassandra G.

doi:10.1007/s00441-011-1150-5

Cited by 9 publications

(9 citation statements)

References 26 publications

(28 reference statements)

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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%

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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Section: Discussionmentioning

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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“…Individualization of each TF is accomplished by the migration of apical somatic cells between TFs (Sheath Cells, Fig 1A) [28]. The number of TFs that form in the larval ovary (18)(19)(20) corresponds to the number of GSC niches at the adult stage [29][30][31]. At the prepupal stage, at the base of each newly formed TF, the anterior-most Intermingled Cells (ICs) differentiate into CCs adopting a cuboidal shape clearly distinguishable from that of TF cells ( Fig 1A-1B') [10,32].…”

Section: Plos Geneticsmentioning

confidence: 99%

The Bric-à-Brac BTB/POZ transcription factors are necessary in niche cells for germline stem cells establishment and homeostasis through control of BMP/DPP signaling in the Drosophila melanogaster ovary

et al. 2020

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Many studies have focused on the mechanisms of stem cell maintenance via their interaction with a particular niche or microenvironment in adult tissues, but how formation of a functional niche is initiated, including how stem cells within a niche are established, is less well understood. Adult Drosophila melanogaster ovary Germline Stem Cell (GSC) niches are comprised of somatic cells forming a stack called a Terminal Filament (TF) and associated Cap and Escort Cells (CCs and ECs, respectively), which are in direct contact with GSCs. In the adult ovary, the transcription factor Engrailed is specifically expressed in niche cells where it directly controls expression of the decapentaplegic (dpp) gene encoding a member of the Bone Morphogenetic Protein (BMP) family of secreted signaling molecules, which are key factors for GSC maintenance. In larval ovaries, in response to BMP signaling from newly formed niches, adjacent primordial germ cells become GSCs. The bric-à-brac paralogs (bab1 and bab2) encode BTB/POZ domain-containing transcription factors that are expressed in developing niches of larval ovaries. We show here that their functions are necessary specifically within precursor cells for TF formation during these stages. We also identify a new function for Bab1 and Bab2 within developing niches for GSC establishment in the larval ovary and for robust GSC maintenance in the adult. Moreover, we show that the presence of Bab proteins in niche cells is necessary for activation of transgenes reporting dpp expression as of larval stages in otherwise correctly specified Cap Cells, independently of Engrailed and its paralog Invected (En/Inv). Moreover, strong reduction of engrailed/invected expression during larval stages does not impair TF formation and only partially reduces GSC numbers. In the adult ovary, Bab proteins are also required for dpp reporter expression in CCs. Finally, when bab2 was overexpressed at this stage in somatic cells outside of the niche, there were no detectable levels of ectopic En/Inv, but ectopic expression of a dpp transgene was found in these cells and BMP signaling activation was induced in adjacent germ cells, which produced GSC-like tumors. Together, these results indicate that Bab transcription factors are positive regulators of BMP signaling in niche cells for establishment and homeostasis of GSCs in the Drosophila ovary.

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“…Morphogenesis begins with TF formation which involves flattening, sorting, intercalation and stacking of somatic TF cell precursors, initiating at the medial side of the ovary and progressing as a wave laterally ( Fig 1A) Sahut-Barnola et al, 1996). Individualization of each TF is accomplished by the migration of apical somatic cells (Inner Sheath Cells) between TFs ( Fig 1A) (Cohen et al, 2002).The number of TFs that form in the larval ovary determines the number of GSC niches at the adult stage (Bartoletti et al, 2012;Green et al, 2011;Sarikaya et al, 2012). At the base of each newlyformed TF, the anterior-most Intermingled Cells (ICs-somatic cells intermingled with Primordial Germ Cells, PGCs) differentiate into CCs adopting a cuboidal shape clearly distinguishable from that of the flat TF cells (Fig 1A and Fig 1B and B', yellow and green brackets, respectively) (Panchal et al, 2017;Zhu and Xie, 2003).…”

Section: Introductionmentioning

confidence: 99%

The Bric-à-Brac transcription factors are necessary for formation of functional germline stem cell niches through control ofdppexpression in theDrosophila melanogasterovary

Saler

Bartoletti

Hauser

et al. 2019

Preprint

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Many studies have focused on the mechanisms of stem cell maintenance via their interaction with a particular niche or microenvironment in adult tissues, but how formation of a functional niche is initiated, including how stem cells within a niche are established, is less well understood. Adult Drosophila melanogaster ovary Germline Stem Cell (GSC) niches are comprised of somatic cells forming a stack called a Terminal Filament (TF) and underlying Cap Cells (CCs) and Escort Cells (ECs), which are in direct contact with GSCs. In the adult, the Engrailed (En) transcription factor is specifically expressed in niche cells where it directly controls expression of the decapentaplegic gene (dpp) encoding a member of the Bone Morphogenetic Protein (BMP) family of secreted signaling molecules, which are key factors for GSC maintenance. In late third instar larval ovaries, in response to BMP signaling from newly-formed niches, adjacent primordial germ cells become GSCs. The bric-àbrac paralogs (bab1 and bab2) encode BTB/POZ-domain containing transcription factors, that are also expressed in developing GSCs niches where they are required for TF formation. Here, we demonstrate that Bab1 and Bab2 display redundant cell autonomous function for TF morphogenesis and we identify a new function for these genes in GSC establishment. Moreover, we show that Bab proteins control dpp expression in otherwise correctly specified CCs, independently of En and its paralog Invected (Inv). In fact, our results also indicate that en/inv function in larval stages are neither essential for TF formation, nor GSC establishment. Finally, when bab2 was overexpressed in ovarian somatic cells outside of the niche, where en/inv were not expressed, ectopic BMP signaling activation was induced in adjacent germ cells of adult ovaries, which formed GSC-like tumors.Together, these results indicate that Bab transcription factors are positive regulators of BMP signaling for acquisition of GSC status.

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Counting in oogenesis

Cited by 9 publications

References 26 publications

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

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

The Bric-à-Brac BTB/POZ transcription factors are necessary in niche cells for germline stem cells establishment and homeostasis through control of BMP/DPP signaling in the Drosophila melanogaster ovary

The Bric-à-Brac transcription factors are necessary for formation of functional germline stem cell niches through control ofdppexpression in theDrosophila melanogasterovary

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