Escort cells generate a dynamic compartment for germline stem cell differentiation via combined Stat and Erk signalling

Banisch, Torsten U.; Maimon, Iris; Dadosh, Tali; Gilboa, Lilach

doi:10.1242/dev.143727

Cited by 40 publications

(60 citation statements)

References 57 publications

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“…Multiple somatic cell types are significantly enriched for genes expressing proteins with roles in mediating cell-cell communication. These protein classes will expand previous observations which showed that, in addition to conventional signaling pathways, ovarian cells coordinate their behaviors through alternative modes of signaling (Banisch et al, 2017;Gilboa et al, 2003). For example, a gap junction protein zpg is highly enriched in germ cells, while other gap junction proteins, inx2, inx3, and ogre, are expressed in somatic cell types surrounding the germ cells.…”

Section: Cell Type Specific Transcriptional Signatures Reveal Functiosupporting

confidence: 51%

See 1 more Smart Citation

A single cell atlas of the developingDrosophilaovary identifies follicle stem cell progenitors

Slaidina¹,

Banisch²,

Gupta³

et al. 2019

Preprint

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Addressing the complexity of organogenesis at a system-wide level requires a complete understanding of adult cell types, their origin and precursor relationships. The Drosophila ovary has been a model to study how coordinated stem cell units, germline and somatic follicle stem cells, maintain and renew an organ. However, lack of cell-type specific tools have limited our ability to study the origin of individual cell types and stem cell units. Here, we use a single cell RNA sequencing approach to uncover all known cell types of the developing ovary, reveal transcriptional signatures, and identify cell type specific markers for lineage tracing. Our study identifies a novel cell type corresponding to the elusive follicle stem cell precursors and predicts sub-types of known cell types. Altogether, we reveal a previously unanticipated complexity of the developing ovary, and provide a comprehensive resource for the systematic analysis of ovary morphogenesis.

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Section: Cell Type Specific Transcriptional Signatures Reveal Functiosupporting

confidence: 51%

“…In addition to common developmental origins, an overlap in transcriptional signatures may also reflect shared functions. Consistently, ICs and FCs both intimately interact with germ cells and guide their differentiation (Banisch et al, 2017;Wu et al, 2008;Xie, 2013)…”

Section: Discussionmentioning

confidence: 99%

A single cell atlas of the developingDrosophilaovary identifies follicle stem cell progenitors

Slaidina¹,

Banisch²,

Gupta³

et al. 2019

Preprint

Self Cite

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“…A second signaling center, sometimes termed a "differentiation niche, " is formed by the somatic escort cells (also called inner germarial sheath cells) ( Figure 2D). Escort cells promote germ cell differentiation and guide the posterior movement of differentiated cysts (Decotto and Spradling, 2005;Morris and Spradling, 2011;Banisch et al, 2017). Escort cells line the outside of the anterior germarium (regions 1-2) and send long, thin cellular protrusions into the center of the germarium, around the dividing germ cells (Kirilly et al, 2011;Morris and Spradling, 2011;Banisch et al, 2017).…”

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

confidence: 99%

“…Escort cells promote germ cell differentiation and guide the posterior movement of differentiated cysts (Decotto and Spradling, 2005;Morris and Spradling, 2011;Banisch et al, 2017). Escort cells line the outside of the anterior germarium (regions 1-2) and send long, thin cellular protrusions into the center of the germarium, around the dividing germ cells (Kirilly et al, 2011;Morris and Spradling, 2011;Banisch et al, 2017). 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.…”

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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“…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). In future it will be interesting to investigate whether pupal or adult ECs have graded EC adhesive properties or send graded differentiation signals according to their AP position, instructed for example by the strength of Wnt signaling.…”

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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Escort cells generate a dynamic compartment for germline stem cell differentiation via combined Stat and Erk signalling

Cited by 40 publications

References 57 publications

A single cell atlas of the developingDrosophilaovary identifies follicle stem cell progenitors

A single cell atlas of the developingDrosophilaovary identifies follicle stem cell progenitors

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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