Development of gap junctions in normal and mutant ovaries of Drosophila melanogaster.

An ovarian follicle of Drosophila consists of an oocyte, 15 nurse cells, and hundreds of follicular epithelial cells. A freeze-fracture analysis of the surfaces between glutaraldehyde-fixed ovarian cells showed that all three cell types were interconnected by gap junctions. This is the first report of gap junctions between adjacent nurse cells, between nurse cells and oocytes, and between follicle cells and oocytes in Drosophila. Since we did not observe intramembranous particle clumping into crystalline patterns and since structurally different gap junctions occurred at different times in development and at different cell-cell interfaces, it is unlikely that fixation artifacts influenced particle distribution in our experiments. A computer-assisted morphometric analysis showed that the extent, size, and morphology of gap junctions varied with development and that these junctions can cover up to 9% of the cell surfaces. To test the role of gap junctions in follicular maturation, we studied ovaries from flies homozygous for the female sterile mutation fs(2)A17, in which follicles develop normally until yolk deposition commences. During the development of mutant follicles, gap junctions became abnormal before any other morphological aspect of the follicle. These studies show that gap junctions are available to play an important role in coordinating intercellular activities between all three cell types in ovarian follicles of Drosophila.