Signal transduction in the early Drosophila follicle stem cell lineage

Rust, Katja; Nystul, Todd

doi:10.1016/j.cois.2019.11.005

Cited by 20 publications

(16 citation statements)

References 77 publications

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“…The finding that somatic cells on most germline cysts are replaced by an independent epithelial cell population at an analogous developmental stage in both Drosophila and mouse ovaries suggests that cellular succession is functionally important and has been conserved in evolution. The transcriptomes of mouse BPG cells (Dataset S2) will make it easier to compare the early stages of ovarian follicle formation in mammals and invertebrates (29,93,94).…”

Section: Two Pregranulosa Cell Pathways Support Two Different Folliclementioning

confidence: 99%

Two distinct pathways of pregranulosa cell differentiation support follicle formation in the mouse ovary

Niu

Spradling

2020

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

161

205

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We sequenced more than 52,500 single cells from embryonic day 11.5 (E11.5) postembryonic day 5 (P5) gonads and performed lineage tracing to analyze primordial follicles and wave 1 medullar follicles during mouse fetal and perinatal oogenesis. Germ cells clustered into six meiotic substages, as well as dying/nurse cells. Wnt-expressing bipotential precursors already present at E11.5 are followed at each developmental stage by two groups of ovarian pregranulosa (PG) cells. One PG group, bipotential pregranulosa (BPG) cells, derives directly from bipotential precursors, expresses Foxl2 early, and associates with cysts throughout the ovary by E12.5. A second PG group, epithelial pregranulosa (EPG) cells, arises in the ovarian surface epithelium, ingresses cortically by E12.5 or earlier, expresses Lgr5, but delays robust Foxl2 expression until after birth. By E19.5, EPG cells predominate in the cortex and differentiate into granulosa cells of quiescent primordial follicles. In contrast, medullar BPG cells differentiate along a distinct pathway to become wave 1 granulosa cells. Reflecting their separate somatic cellular lineages, second wave follicles were ablated by diptheria toxin treatment of Lgr5-DTR-EGFP mice at E16.5 while first wave follicles developed normally and supported fertility. These studies provide insights into ovarian somatic cells and a resource to study the development, physiology, and evolutionary conservation of mammalian ovarian follicles.

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Section: Two Pregranulosa Cell Pathways Support Two Different Folliclementioning

confidence: 99%

Two distinct pathways of pregranulosa cell differentiation support follicle formation in the mouse ovary

Niu

Spradling

2020

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

161

205

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“…The complex intersection of signalling pathways is involved in FSC differentiation and specification, and the increase in the number of anteriorly positioned msi mutant FSCs/FPCs within the germarium may predispose cells to receiving signals which direct cells toward an anterior fate. Although Notch, Hh, Wnt, Hippo and EGFR signalling all play roles in some aspect of FSC proliferation, FSC self-renewal or differentiation, FSC survival and competition (reviewed in (Rust & Nystul, 2020)), we specifically addressed whether msi mutations may affect Wnt signalling activity, since an increase in Wnt activity has recently been associated with an increase in the differentiation towards an anterior EC fate from the FSC niche (Reilein et al, 2017). A steep gradient of Wnt signalling activity has been reported in the germarium from regions 1 to 2b, with high levels of Wnt signalling activity present in FSCs and FPCs at the region 2a/2b border, while nearly undetectable levels of Wnt pathway activity have been reported in FPCs that have moved into Region 2b of the germarium (Dai et al, 2017; Kim-Yip & Nystul, 2018).…”

Section: Discussionmentioning

confidence: 99%

MiMIC analysis reveals an isoform specific role forDrosophilaMusashi in follicle stem cell maintenance and escort cell function

Siddall

Casagranda

Dominado

et al. 2020

Preprint

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The Musashi (Msi) family of RNA-binding proteins regulate maintenance and differentiation of stem cells in multiple tissues of different species. Here, we use the powerful system of the Drosophila ovary to uncover an intrinsic requirement for Msi in both the maintenance of the follicle stem cell population and regulation of the architecture of the follicle stem cell niche. Further, we demonstrate an associated G2 lag of cycling somatic cells within the niche when Msi function is abrogated. Additionally, we show that Msi interaction with the Wnt pathway influences differentiation of anterior germarial escort cells from cells within the follicle stem cell niche region. This provides further evidence that escort cells can be derived from follicle stem/precursor cells and that Msi regulates lineage differentiation of follicle stem cell daughters.

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“…Mitotically dividing germ cells are guided through the germaria by somatic escort cells ( Banisch et al 2017 ). Cessation of germ cell mitosis coincides with a transfer of 16-cell cysts from escort cells to pre-follicle cells, which originate from a second population of stem cells, the follicle stem cells ( Rust and Nystul 2020 ). Pre-follicle cells migrate around cysts and interdigitate to separate newly forming egg chambers ( Lovegrove et al 2019 ).…”

Section: Introductionmentioning

confidence: 99%

Orphan nuclear receptorftz-f1 (NR5A3)promotes egg chamber survival in theDrosophilaovary

Beachum

Whitehead

McDonald

et al. 2021

G3 Genes|Genomes|Genetics

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Gamete production in mammals and insects is controlled by cell signaling pathways that facilitate communication between germ cells and somatic cells. Nuclear receptor signaling is a key mediator of many aspects of reproduction, including gametogenesis. For example, the NR5A sub-family of nuclear receptors are essential for gonad development and sex steroid production in mammals. Despite the original identification of the NR5A sub-family in the model insect Drosophila melanogaster, it has been unclear whether Drosophila NR5A receptors directly control oocyte production. Ftz-f1 is expressed throughout the ovary, including in germline stem cells, germline cysts, and several populations of somatic cells. We demonstrate that ftz-f1 is required in follicle cells prior to stage 10 to promote egg chamber survival at the mid-oogenesis checkpoint. Our data suggest that egg chamber death in the absence of ftz-f1 is due, at least in part, to failure of follicle cells to exit the mitotic cell cycle or failure to accumulate oocyte-specific factors in the germline. Taken together, these results demonstrate that, as in mammals, the NR5A sub-family promotes maximal reproductive output in Drosophila. Our data underscore the importance of nuclear receptors in the control of reproduction and highlight the utility of Drosophila oogenesis as a key model for unraveling the complexity of nuclear receptor signaling in gametogenesis.

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Signal transduction in the early Drosophila follicle stem cell lineage

Cited by 20 publications

References 77 publications

Two distinct pathways of pregranulosa cell differentiation support follicle formation in the mouse ovary

Two distinct pathways of pregranulosa cell differentiation support follicle formation in the mouse ovary

MiMIC analysis reveals an isoform specific role forDrosophilaMusashi in follicle stem cell maintenance and escort cell function

Orphan nuclear receptorftz-f1 (NR5A3)promotes egg chamber survival in theDrosophilaovary

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