Multiple signaling pathways establish both the individuation and the polarity of the oocyte follicle in Drosophila

The development of the Drosophila oocyte depends upon a sequential series of interactions between the germline cells and the somatically derived follicle cells to produce individual follicles with appropriate polarities. In the germarium the control of germline cell division depends upon a proper interaction with somatic cells adjacent to the germline stem cells. Both gurken and brainiac are required in the germline, and the Egfr, daughterless, Notch , and Delta genes are required in the somatic cells to produce individual egg chambers with a continuous follicular epithelium. After a follicle forms, components in these same signaling pathways, plus additional genes, are then required for the establishment of the anterior‐posterior polarity, followed by the dorsal‐ventral polarity of the developing follicle. Initially, gurken mRNA is localized to the posterior edge of the oocyte, where it signals the posterior polar follicle cells to differentiate as posterior. The anterior‐posterior assymmetry of the oocyte is then established by a reorganization of the microtubule network, which requires a Notch‐Delta ‐dependent signal sent from the posterior polar follicle cells to the oocyte and the activity of protein kinase A in the germ line. This reorganization leads to the localization of the maternal anterior‐posterior determinants bicoid and oskar to opposite poles of the oocyte and the repositioning of the oocyte nucleus to the anterior‐dorsal surface of the oocyte, gurken mRNA and protein are now concentrated between the oocyte nucleus and the adjacent anterior‐dorsal follicle cells, where, in combination with Rhomboid, it locally activates the EGF receptor and its downstream cascade to direct the adjoining cells to adopt a dorsal fate. This process is thought to restrict the action of three follicle cell gene functions, encoded by windbeutel, nudal , and, pipe , to the ventral follicle cells, where they lead to the localized activation of a serine protease cascade required to produce the active Spätzle ligand to activate the Toll receptor. Finally, the termini of the embryo are dependent upon the activation of the Torso receptor, and this requires the localized expression of torso‐like in a subset of follicle cells at the anterior and posterior poles of the follicle, which leads to the activation of Trunk, the putative ligand for Torso. In summary, the normal development of the oocyte requires a continuous sequence of germline‐follicle cell interactions to provide the polarities responsible for normal development. © 1996 Wiley‐Liss, Inc.