The Wnt pathway limits BMP signaling outside of the germline stem cell niche in Drosophila ovaries

Mottier-Pavie, Violaine; Palacios, Víctor; Eliazer, Susan; Scoggin, Shane; Buszczak, Michael

doi:10.1016/j.ydbio.2016.06.038

Cited by 48 publications

(59 citation statements)

References 48 publications

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“…Several constituents of ECs are known to be involved in silencing BMP ligands and facilitators. These include molecules necessary for regulating the cellular processes that contact germline cells (as exemplified by Rho; Kirilly et al, 2011), EGFR (Liu et al, 2010), Wnt pathway components (Hamada-Kawaguchi et al, 2014;Luo et al, 2015;Wang et al, 2015;Mottier-Pavie et al, 2016), Piwi (Ma et al, 2014) and multiple regulators of chromatin modifications (Eliazer et al, 2011;Wang et al, 2011;Xuan et al, 2013;Maimon et al, 2014). Here, we report that the Hh and Hpo/Yki pathways also serve to suppress BMP ligand production in ECs.…”

Section: Discussionmentioning

confidence: 65%

Yorkie and Hedgehog independently restrict BMP production in escort cells to permit germline differentiation in the Drosophila ovary

2017

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Multiple signaling pathways guide the behavior and differentiation of both germline stem cells (GSCs) and somatic follicle stem cells (FSCs) in the Drosophila germarium, necessitating careful control of signal generation, range and responses. Signal integration involves escort cells (ECs), which promote differentiation of the GSC derivatives they envelop, provide niche signals for FSCs and derive directly from FSCs in adults. Hedgehog (Hh) signaling induces the Hippo pathway effector Yorkie (Yki) to promote proliferation and maintenance of FSCs, but Hh also signals to ECs, which are quiescent. Here, we show that in ECs both Hh and Yki limit production of BMP ligands to allow germline differentiation. Loss of Yki produced a more severe germarial phenotype than loss of Hh signaling and principally induced a different BMP ligand. Moreover, Yki activity reporters and epistasis tests showed that Yki does not mediate the key actions of Hh signaling in ECs. Thus, both the coupling and output of the Hh and Yki signaling pathways differ between FSCs and ECs despite their proximity and the fact that FSCs give rise directly to ECs.

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Section: Discussionmentioning

confidence: 65%

Yorkie and Hedgehog independently restrict BMP production in escort cells to permit germline differentiation in the Drosophila ovary

2017

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“…Escort cell protrusions dynamically wrap the dividing cystoblasts and are essential for mitotic division of the cysts, as well as the association of follicle cells with the germline at encapsulation. Like cap cells, escort cells also produce and secrete signaling molecules; Hedgehog, Wnt/Wg, Epidermal Growth Factor (EGF), insulin, and ecdysone signaling all function non-autonomously in escort cells to control germ cell differentiation (Morris and Spradling, 2012;Xuan et al, 2013;Eliazer et al, 2014;König and Shcherbata, 2015;Liu et al, 2015;Lu et al, 2015;Luo et al, 2015;Mottier-Pavie et al, 2016;Huang et al, 2017;Su et al, 2018;Wang and Page-McCaw, 2018;Mao et al, 2019). In general, many of these signals act to sustain the cytoskeletal structure and/or dynamics of escort cell protrusions.…”

Section: Paracrine Signaling Promotes Gsc Self-renewal and Daughter Cmentioning

confidence: 99%

Coordinating Proliferation, Polarity, and Cell Fate in the Drosophila Female Germline

Hinnant

Merkle

Ables

2020

Front. Cell Dev. Biol.

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Gametes are highly specialized cell types produced by a complex differentiation process. Production of viable oocytes requires a series of precise and coordinated molecular events. Early in their development, germ cells are an interconnected group of mitotically dividing cells. Key regulatory events lead to the specification of mature oocytes and initiate a switch to the meiotic cell cycle program. Though the chromosomal events of meiosis have been extensively studied, it is unclear how other aspects of oocyte specification are temporally coordinated. The fruit fly, Drosophila melanogaster, has long been at the forefront as a model system for genetics and cell biology research. The adult Drosophila ovary continuously produces germ cells throughout the organism's lifetime, and many of the cellular processes that occur to establish oocyte fate are conserved with mammalian gamete development. Here, we review recent discoveries from Drosophila that advance our understanding of how early germ cells balance mitotic exit with meiotic initiation. We discuss cell cycle control and establishment of cell polarity as major themes in oocyte specification. We also highlight a germline-specific organelle, the fusome, as integral to the coordination of cell division, cell polarity, and cell fate in ovarian germ cells. Finally, we discuss how the molecular controls of the cell cycle might be integrated with cell polarity and cell fate to maintain oocyte production.

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“…The differentiation of germline cysts in the adult germarium depends on interactions with ECs and this has also been seen in some cases during pupal development even though many EC precursors are still dividing during early pupation. Normal Wnt pathway activity is among those shown to be important for this function in ECs and pre-ECs (Hamada-Kawaguchi et al, 2014;Luo et al, 2015;Mottier-Pavie et al, 2016;Upadhyay et al, 2018;Waghmare and Page-McCaw, 2018;Wang et al, 2015;Wang and Page-McCaw, 2018). It is not known what drives ordered posterior movement of germline cysts in adult germaria but this also may depend on EC interactions (Banisch et al, 2017).…”

Section: Coordination Between Germline and Somatic Ovarian Cell Develmentioning

confidence: 99%

Adult Stem Cells and Niche Cells segregate gradually from common precursors that build the adult Drosophila ovary during pupal development

Reilein¹,

Kogan²,

Misner³

et al. 2020

Preprint

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Adult stem cell function relies on the prior specification and organization of appropriate numbers of stem cells and supportive niche cells during development. Insights into those developmental processes could facilitate the synthesis of organoid mimics. Drosophila Follicle Stem Cells (FSCs) present an amenable paradigm with many similarities to mammalian gut stem cells. In an adult germarium a central domain of about 16 FSCs produces a posterior stream of transit-amplifying Follicle Cells (FCs), which encapsulate mature germline cysts to support egg development and, from their anterior face, quiescent Escort Cells (EC), which support the maturation of germline cysts. The behavior of FSCs is guided in part by niche signals produced by ECs and by a specialized polar cell FC derivative. Thus, ECs and FCs are both adult stem cell products and niche cells. Here we show by lineage analyses that adult ECs, FSCs and FCs derive from common precursors during pupal development. We infer that disparities in initial anterior-posterior (AP) precursor location followed by limited dispersal of progeny leads to a gradual acquisition of distinct fates determined by final AP location, with progeny of a single precursor commonly straddling EC and FSC, FSC and FC, or all three territories through most of pupal development. Direct visualization of pupal ovaries, including live imaging revealed a transient population of FC precursors posterior to the developing germarium awaiting emergence of the most mature germline cyst. The consequent budding process was quite different from the budding of egg chambers in adults. An anterior to posterior gradient of Wnt signaling develops shortly after pupariation. Loss of pathway activity cell autonomously resulted in more posterior adult progeny fates, while increased pathway activity elicited the opposite response, suggesting that stronger Wnt signaling favors anterior migration. Clearly detectable JAK-STAT pathway activity emerges only halfway through pupation after polar cells form, and spreads from posterior to anterior.Loss of JAK-STAT activity had similar consequences to increased Wnt pathway activity, drastically reducing FSC and FC production cell autonomously, while increased JAK-STAT activity promoted excessive precursor proliferation. We conclude that FSCs develop in co-ordination with their niche and product cells, that specification of stem cell identity is gradual, subject to stochastic influences and guided by graded extracellular signals, presaging similar regulation of adult stem cell behavior by the same pathways. cytokinesis to yield a progression of 2-, 4-, 8-and 16-cell germline cysts. Their maturation is accompanied by posterior movement and depends on interactions with neighboring quiescent, somatic

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The Wnt pathway limits BMP signaling outside of the germline stem cell niche in Drosophila ovaries

Cited by 48 publications

References 48 publications

Yorkie and Hedgehog independently restrict BMP production in escort cells to permit germline differentiation in the Drosophila ovary

Yorkie and Hedgehog independently restrict BMP production in escort cells to permit germline differentiation in the Drosophila ovary

Coordinating Proliferation, Polarity, and Cell Fate in the Drosophila Female Germline

Adult Stem Cells and Niche Cells segregate gradually from common precursors that build the adult Drosophila ovary during pupal development

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