The actin-binding protein profilin is required for germline stem cell maintenance and germ cell enclosure by somatic cyst cells

Shields, Alicia; Spence, Allyson C.; Yamashita, Yukiko; Fuller, Margaret T.

doi:10.1242/dev.101931

Cited by 52 publications

(54 citation statements)

References 40 publications

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“…2D). Our results differ somewhat from those in a recent analysis of Chic by Shields et al (2014), who found that Chic knockdown resulted in fewer Tj-positive cells. This difference is likely to be due to our use of a different UAS driver and RNAi line to obtain a weaker knockdown of Chic.…”

Section: Chic Is Required In the Soma For Fertilitycontrasting

confidence: 99%

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A somatic permeability barrier around the germline is essential forDrosophilaspermatogenesis

2015

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Interactions between the soma and germline are essential for gametogenesis. In the Drosophila testis, differentiating germ cells are encapsulated by two somatic cells that surround the germline throughout spermatogenesis. chickadee (chic), the fly ortholog of Profilin, mediates soma-germline interactions. Knockdown of Chic in the soma results in sterility and severely disrupted spermatogenesis due to defective encapsulation. To study this defect further, we developed a permeability assay to analyze whether the germline is isolated from the surrounding environment by the soma. We find that germline encapsulation by the soma is, by itself, insufficient for the formation of a permeability barrier, but that such a barrier gradually develops during early spermatogenesis. Thus, germline stem cells, gonialblasts and early spermatogonia are not isolated from the outside environment. By late spermatocyte stages, however, a permeability barrier is formed by the soma. Furthermore, we find that, concomitant with formation of the permeability barrier, septate junction markers are expressed in the soma and localize to junctional sites connecting the two somatic cells that surround the germline. Importantly, knockdown of septate junction components also disrupts the permeability barrier. Finally, we show that germline differentiation is delayed when the permeability barrier is compromised. We propose that the permeability barrier around the germline serves an important regulatory function during spermatogenesis by shaping the signaling events that take place between the soma and the germline.

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Section: Chic Is Required In the Soma For Fertilitycontrasting

confidence: 99%

“…2L,M). In a recent study, Shields et al (2014) obtained results consistent with those that we describe here, supporting our findings that somatic Chic knockdown leads to defects in somatic differentiation and germline proliferation.…”

Section: Chic Is Required In the Soma For Fertilitysupporting

confidence: 92%

A somatic permeability barrier around the germline is essential forDrosophilaspermatogenesis

2015

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“…Physical association between ECs and germ cells is crucial for GSC differentiation (Jin et al, 2013;Kirilly et al, 2011;Schulz et al, 2002;Shields et al, 2014). Thus, loss of extensive physical contact with ECs per se could account for the downregulation phenotypes of stat, woc and zfh1.…”

Section: Soma-germline Association and Germ Cell Differentiationmentioning

confidence: 99%

Without children is required for Stat-mediatedzfh1transcription and for germline stem cell differentiation

2014

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Tissue homeostasis is maintained by balancing stem cell self-renewal and differentiation. How surrounding cells support this process has not been entirely resolved. Here we show that the chromatin and telomerebinding factor Without children (Woc) is required for maintaining the association of escort cells (ECs) with germ cells in adult ovaries. This tight association is essential for germline stem cell (GSC) differentiation into cysts. Woc is also required in larval ovaries for the association of intermingled cells (ICs) with primordial germ cells. Reduction in the levels of two other proteins, Stat92E and its target Zfh1, produce phenotypes similar to woc in both larval and adult ovaries, suggesting a molecular connection between these three proteins. Antibody staining and RT-qPCR demonstrate that Zfh1 levels are increased in somatic cells that contact germ cells, and that Woc is required for a Stat92E-mediated upregulation of zfh1 transcription. Our results further demonstrate that overexpression of Zfh1 in ECs can rescue GSC differentiation in woc-deficient ovaries. Thus, Zfh1 is a major Woc target in ECs. Stat signalling in niche cells has been previously shown to maintain GSCs non-autonomously. We now show that Stat92E also promotes GSC differentiation. Our results highlight the Woc-Stat-Zfh1 module as promoting somatic encapsulation of germ cells throughout their development. Each somatic cell type can then provide the germline with the support it requires at that particular stage. Stat is thus a permissive factor, which explains its apparently opposite roles in GSC maintenance and differentiation.

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“…dom is essential for stem cell maintenance in the testis (Morillo Prado et al, 2013). chic, the Drosophila gene that encodes profilin, is required to maintain GSCs in a cell-autonomous manner, possibly by regulating the GSC-hub cell interface (Shields et al, 2014). In our screen, knockdown of dom or chic (Fig.…”

Section: Gsc Self-renewal Screen In Fly Testesmentioning

confidence: 99%

“…In addition to the key molecules in the signaling pathways mentioned above, many other factors also regulate the self-renewal and differentiation of stem cells in the testis. Epigenetic factors, microRNAs, actin-binding proteins, nuclear lamins and RNA-binding proteins have all been shown to affect the activity of stem cells in the testis (Chen et al, 2014Cherry and Matunis, 2010;Eun et al, 2013;Pek et al, 2009;Shields et al, 2014). Traditional studies of genes that regulate stem cell activity in testes have relied on mosaic analysis or genetic screens for male sterility in homozygous mutant animals.…”

Section: Introductionmentioning

confidence: 99%

Protein synthesis and degradation are essential to regulate germline stem cell homeostasis in Drosophila testes

Xiang

Chen

et al. 2016

Development

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The homeostasis of self-renewal and differentiation in stem cells is controlled by intrinsic signals and their niche. We conducted a large-scale RNA interference (RNAi) screen in Drosophila testes and identified 221 genes required for germline stem cell (GSC) maintenance or differentiation. Knockdown of these genes in transit-amplifying spermatogonia and cyst cells further revealed various phenotypes. Complex analysis uncovered that many of the identified genes are involved in key steps of protein synthesis and degradation. A group of genes that are required for mRNA splicing and protein translation contributes to both GSC selfrenewal and early germ cell differentiation. Loss of genes in the protein degradation pathway in cyst cells leads to testis tumors consisting of overproliferated germ cells. Importantly, in the Cullin 4-RING E3 ubiquitin ligase (CRL4) complex, we identified multiple proteins that are crucial to GSC self-renewal: pic/DDB1, a CRL4 linker protein, is not only required for GSC self-renewal in flies but also for maintenance of spermatogonial stem cells (SSCs) in mice.

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The actin-binding protein profilin is required for germline stem cell maintenance and germ cell enclosure by somatic cyst cells

Cited by 52 publications

References 40 publications

A somatic permeability barrier around the germline is essential forDrosophilaspermatogenesis

A somatic permeability barrier around the germline is essential forDrosophilaspermatogenesis

Without children is required for Stat-mediatedzfh1transcription and for germline stem cell differentiation

Protein synthesis and degradation are essential to regulate germline stem cell homeostasis in Drosophila testes

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