Niche formation and function in developing tissue: studies from the Drosophila ovary

Abstract

Adult stem cells have a unique ability to self-renew and to generate differentiated daughter cells that are required in the body tissues. The identity of adult stem cells is maintained by extrinsic signals from other cell types, known as niche cells. Thus, the niche is required for appropriate tissue homeostasis. Niche is formed and recruits stem cells during tissue development; therefore, it is essential to establish niche cells and stem cells in proper numbers during development. A small niche may recruit too few stem cells and cause tissue degeneration, while a large niche may maintain too many stem cells and lead to tumorigenesis. Given that vertebrate tissues are not suitable for large-scale forward genetics studies, the Drosophila ovary stands out as an excellent model for studying how multiple niche cell types and germ cells (GCs) are coordinately regulated in vivo. Recent studies are beginning to reveal how various signaling molecules regulate niche formation and how niche cells non-autonomously influence GC number. In this review, we summarize the ovarian niche structure, the key signaling pathways for niche formation, and how niche cells generate extrinsic factors to control GC proliferation during ovarian development. Video abstract.

Keywords: Drosophila; Hippo; Insulin; Niche; Ovary.

Fig. 1

Schematic of ovarian development in Drosophila from the embryo to the larval–pupal (LP) transition stage. The embryonic gonad consists of primordial germ cells (PGCs: blue) and somatic gonadal precursors (SGPs: red). The L2 larval ovary is composed of germ cells (GCs: blue) surrounded by intermingled cells (ICs: red). By the mid-third instar larval (ML3), terminal filament cells (TFCs: yellow) first appear and somatic swarm cells (SwCs: purple) are located dorsolaterally. During the LP transition, SwCs form a new posterior domain and the ICs adjacent to basal TFCs differentiate into cap cells (CCs: green); the TFCs are organized into 16–20 TF stacks

Fig. 2

Schematic diagram of signaling crosstalk that regulates the formation of ovarian niche cells and germ cells. The Hippo, Insulin and Tor signaling pathways function in the soma to regulate proliferation both autonomously in TFCs and ICs and non-autonomously in GCs. The Notch signaling is required for TFC and CC formation. The EGFR pathway regulates homeostatic growth of both IC and GC numbers