The Drosophila cyst stem cell lineage: Partners behind the scenes?

Abstract

In all animals, germline cells differentiate in intimate contact with somatic cells and interactions between germline and soma are particularly important for germline development and function. In the male gonad of Drosophila melanogaster, the developing germline cells are enclosed by somatic cyst cells. The cyst cells are derived from cyst stem cells (CySCs) of somatic origin and codifferentiate with the germline cells. The fast generation cycle and the genetic tractability of Drosophila has made the Drosophila testis an excellent model for studying both the roles of somatic cells in guiding germline development and the interdependence of two separate stem cell lineages. This review focuses on our current understanding of CySC specification, CySC self-renewing divisions, cyst cell differentiation, and soma-germline interactions. Many of the mechanisms guiding these processes in Drosophila testes are similarly essential for the development and function of tissues in other organisms, most importantly for gametogenesis in mammals.

Figure 1. The organization of somatic cells and germline cells in wildtype testes. (A) Graphic depicting the organization and development of the cysts along the apical (left) to basal (right) axes of the testis. CySC, cyst stem cell; GSC, germline stem cell; GB, gonialblast; SG, spermatogonia; SC, spermatocytes; CC, cyst cells; HCC, head cyst cells; TCC, tail cyst cells. (B–D) Immunofluorescent labeling of wildtype testes as indicated. (B) Visualization of cyst cells enclosing the germline cells in a whole testis. (C) The apical tip of a testis showing colocalization of Zfh-1 and Tj. (D) The apical region and the testis coil. Tj is expressed in early stage cyst cells near the tip, and Eya is expressed strongly in late stage cyst cells. *hub cells; scale bars, 50 µm.

Figure 2. Regulation of cyst development.⁶² Graphics depicting specific steps of germline and cyst cell interactions. Molecules and Interactions as indicated. See main text for details. (A) Signaling events at the tip of the testes regulating CySC and GSC fate. (B) Signaling events regulating CySC and GSC division frequency (black round arrows). (C) The regulation of germline enclosure by EGF signaling. (D) The regulation of germline proliferation by EGF signaling. (E) Signaling events regulating the transition of the spermatogonia into the spermatocyte stage. (E) Sperm maturation depends on the cap proteins in the head cyst cells.