Drosophila follicle cells: morphogenesis in an eggshell

Abstract

Epithelial morphogenesis is important for organogenesis and pivotal for carcinogenesis, but mechanisms that control it are poorly understood. The Drosophila follicular epithelium is a genetically tractable model to understand these mechanisms in vivo. This epithelium of follicle cells encases germline cells to create an egg. In this review, we summarize progress toward understanding mechanisms that maintain the epithelium or permit migrations essential for oogenesis. Cell-cell communication is important, but the same signals are used repeatedly to control distinct events. Understanding intrinsic mechanisms that alter responses to developmental signals will be important to understand regulation of cell shape and organization.

Figure 1

Cell outlines visualized by phalloidin staining of the actin cytoskeleton (white). Stages of egg chambers are indicated by the numbers; and G is for germarium. Anterior is to the left. Follicle cells form an epithelium to cover the underlying germline cells. As oogenesis proceeds, follicle cells undergo shape changes and morphogenetic movements and eventually give rise to the complex structure of the eggshell. CFC: columnar follicle cells; NC: nurse cells; Oo: oocyte; SFC: squamous follicle cells.

Figure 2

Scanning electron micrograph of an eggshell (dorso-lateral view). Image adapted from Ref. [5] copyright 2000 Wiley-Liss.

Figure 3

A. Diagram of a Drosophila germarium. This illustration is shows the location of germline stem cells (GSCs; red) and follicle cell stem cells (FCSCs; yellow) and their niche cells. Two GSCs cells are located close to their niche composed of cap cell (bright green) and terminal filament (turquoise). The GSCs and cap cells also contact the Escort stem cells (blue). The GSCs differentiating daughters cystoblasts (light orange) move away from the niche in close contact with escort cells (moon shape pale blue) until escort cells die (star shaped pale blue) or replaced by prefollicular cells (light yellow). The prefollicular cells are derived from follicle cell stem cells (yellow), located at the junction of regions 2a and 2b. FCSCs are in close contact with inner germarial sheath cells (pink) (This illustration is based on figures and date in [4, 5, 22, 25, 27, 185, 186]. B. Egg chambers stained with Fas3 (red) and counterstained with the nuclear dye Topro3 (white). Polar cells (arrow) stain strongly with Fas3. Epithelial follicle cells (arrowhead) down-regulate Fas3 as they mature. Anterior is to the left.

Figure 4

A-D. Follicle cell morphology visualized by α-spectrin staining. Anterior is to the left. A. At stage 8, epithelial follicle cells are morphologically uniform and have a cuboidal shape. B. At stage 9, follicle cells change their shapes as they migrate posteriorly (arrows). C. At stage 10A, follicle cells that are in contact with the oocyte (Oo) become columnar, while those covering the nurse cells (nc) become squamous. D. At stage 10B, a group of anterior columnar follicle cells elongate and migrate at the interface between the oocyte and the nurse cells (indicated by the arrows). These are centripetally migrating follicle cells. E. A stage 9 egg chamber stained with Fas3 (red) to label polar cells and counterstained with Topro3 (white) to visualize nuclei. Border cells (arrowhead) migrate posteriorly between the nurse cells. A pair of polar cells is located in the center of the border cell cluster. Image adapted from Ref. [5] copyright 2000 Wiley-Liss.