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Somatic ERK activation during transit amplification is essential for maintaining the synchrony of germline divisions in Drosophila testis.

ABSTRACT: Transit amplification (TA) of progenitor cells maintains tissue homeostasis by balancing proliferation and differentiation. In Drosophila testis, the germline proliferation is tightly regulated by factors present in both the germline and the neighbouring somatic cyst cells (SCCs). Although the exact mechanism is unclear, the epidermal growth factor receptor (EGFR) activation in SCCs has been reported to control spermatogonial divisions within a cyst, through downstream activations of Rac1-dependent pathways. Here, we report that somatic activation of the mitogen-activated protein kinase (Rolled/ERK) downstream of EGFR is required to synchronize the mitotic divisions and regulate the transition to meiosis. The process operates independently of the Bag-of-marble activity in the germline. Also, the integrity of the somatic cyst enclosure is inessential for this purpose. Together, these results suggest that synchronization of germ-cell divisions through somatic activation of distinct ERK-downstream targets independently regulates TA and subsequent differentiation of neighbouring germline cells.

SUBMITTER: Gupta S

PROVIDER: S-EPMC6070716 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Somatic ERK activation during transit amplification is essential for maintaining the synchrony of germline divisions in <i>Drosophila</i> testis.

Gupta Samir S Varshney Bhavana B Chatterjee Shambhabi S Ray Krishanu K

Open biology 20180701 7

Transit amplification (TA) of progenitor cells maintains tissue homeostasis by balancing proliferation and differentiation. In <i>Drosophila</i> testis, the germline proliferation is tightly regulated by factors present in both the germline and the neighbouring somatic cyst cells (SCCs). Although the exact mechanism is unclear, the epidermal growth factor receptor (EGFR) activation in SCCs has been reported to control spermatogonial divisions within a cyst, through downstream activations of Rac1 ...[more]

PMID: 30045884

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Project description:BackgroundDisrupted germline differentiation or compromised testis development can lead to subfertility or infertility and are strongly associated with testis cancer in humans. In mice, SRY and SOX9 induce expression of Fgf9, which promotes Sertoli cell differentiation and testis development. FGF9 is also thought to promote male germline differentiation but the mechanism is unknown. FGFs typically signal through mitogen-activated protein kinases (MAPKs) to phosphorylate ERK1/2 (pERK1/2). We explored whether FGF9 regulates male germline development through MAPK by inhibiting either FGF or MEK1/2 signalling in the foetal testis immediately after gonadal sex determination and testis cord formation, but prior to male germline commitment.ResultspERK1/2 was detected in Sertoli cells and inhibition of MEK1/2 reduced Sertoli cell proliferation and organisation and resulted in some germ cells localised outside of the testis cords. While pERK1/2 was not detected in germ cells, inhibition of MEK1/2 after somatic sex determination profoundly disrupted germ cell mitotic arrest, dysregulated a broad range of male germline development genes and prevented the upregulation of key male germline markers, DPPA4 and DNMT3L. In contrast, while FGF inhibition reduced Sertoli cell proliferation, expression of male germline markers was unaffected and germ cells entered mitotic arrest normally. While male germline differentiation was not disrupted by FGF inhibition, a range of stem cell and cancer-associated genes were commonly altered after 24 h of FGF or MEK1/2 inhibition, including genes involved in the maintenance of germline stem cells, Nodal signalling, proliferation, and germline cancer.ConclusionsTogether, these data demonstrate a novel role for MEK1/2 signalling during testis development that is essential for male germline differentiation, but indicate a more limited role for FGF signalling. Our data indicate that additional ligands are likely to act through MEK1/2 to promote male germline differentiation and highlight a need for further mechanistic understanding of male germline development.

Dataset Information

Somatic ERK activation during transit amplification is essential for maintaining the synchrony of germline divisions in Drosophila testis.

Publications

Somatic ERK activation during transit amplification is essential for maintaining the synchrony of germline divisions in <i>Drosophila</i> testis.

Similar Datasets

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