Development of the male germline stem cell niche in Drosophila

Abstract

Stem cells are found in specialized microenvironments, or "niches", which regulate stem cell identity and behavior. The adult testis and ovary in Drosophila contain germline stem cells (GSCs) with well-defined niches, and are excellent models for studying niche development. Here, we investigate the formation of the testis GSC niche, or "hub", during the late stages of embryogenesis. By morphological and molecular criteria, we identify and follow the development of an embryonic hub that forms from a subset of anterior somatic gonadal precursors (SGPs) in the male gonad. Embryonic hub cells form a discrete cluster apart from other SGPs, express several molecular markers in common with the adult hub and organize anterior-most germ cells in a rosette pattern characteristic of GSCs in the adult. The sex determination genes transformer and doublesex ensure that hub formation occurs only in males. Interestingly, hub formation occurs in both XX and XY gonads mutant for doublesex, indicating that doublesex is required to repress hub formation in females. This work establishes the Drosophila male GSC niche as a model for understanding the mechanisms controlling niche formation and initial stem cell recruitment, as well as the development of sexual dimorphism in the gonad.

Sexual Back Talk With Evolutionary Implications: Stimulation of the Drosophila Sex-Determination Gene Sex-lethal by Its Target transformer

“…We hypothesize that their disintegration soon after the onset of metamorphosis is a consequence of a sudden increase in the level of dsx F required to promote the rapid female differentiation and counteract any dsx M present, a level that cannot be reached by these mutant cells that have not fully engaged the Sxl f9 positive feedback loop. In this connection it may be relevant that Le Bras and Van Doren (2006) reported that the gonad's requirements for dsx F and dsx M are qualitatively different during embryonic development than at later stages. We can imagine that a sudden shift in sexual identity during a period of rapid differentiation might be more disruptive than an intersexual orientation held consistently throughout development, such as that imposed by a loss of the dsx or ix genes.…”

Somatic gonadal cells: The supporting cast for the germline

“…Finally, by the end of stage 17, a critical structure that regulates the germline stem cells (GSCs), called the hub, forms from a group of 10-12 anterior SGPs, and this structure persists through adulthood ( Fig. 1; Aboïm, 1945;Gonczy et al, 1992;Hardy et al, 1979;Le Bras and Van Doren, 2006). Within the hub, multiple adhesion proteins are expressed from this point forward, including Fasciclin 3 (Fas3), Drosophila E-cadherin (DEcad) and Drosophila N-cadherin (DN-cad) Le Bras and Van Doren, 2006;Yamashita et al, 2003).…”

“…1; Aboïm, 1945;Gonczy et al, 1992;Hardy et al, 1979;Le Bras and Van Doren, 2006). Within the hub, multiple adhesion proteins are expressed from this point forward, including Fasciclin 3 (Fas3), Drosophila E-cadherin (DEcad) and Drosophila N-cadherin (DN-cad) Le Bras and Van Doren, 2006;Yamashita et al, 2003). In addition, integrins are required to anchor the hub at the anterior end of the gonad (Tanentzapf et al, 2007).…”

“…In addition, integrins are required to anchor the hub at the anterior end of the gonad (Tanentzapf et al, 2007). Interestingly, hub formation can proceed in the absence of PGCs or if there are earlier defects in gonad compaction (Le Bras and Van Le Bras and Van Doren, 2006). Each GSC is ensheathed by two somatic stem cells, known as the cyst stem cells (CySCs), which are required for GSC maintenance and self-renewal (Gonczy and DiNardo, 1996;Dinardo, 2008, 2010).…”

“…Each GSC is ensheathed by two somatic stem cells, known as the cyst stem cells (CySCs), which are required for GSC maintenance and self-renewal (Gonczy and DiNardo, 1996;Dinardo, 2008, 2010). By the first larval instar (L1), spermatogenesis begins (Aboïm, 1945;Le Bras and Van Doren, 2006). Each GSC undergoes asymmetric division to give rise to one GSC and a daughter cell, called the gonialblast (reviewed in Fuller, 1993).…”