Cracking open cell death in the Drosophila ovary

Abstract

The Drosophila melanogaster ovary is a powerful yet simple system with only a few cell types. Cell death in the ovary can be induced in response to multiple developmental and environmental signals. These cell deaths occur at distinct stages of oogenesis and involve unique mechanisms utilizing apoptotic, autophagic and perhaps necrotic processes. In this review, we summarize recent progress characterizing cell death mechanisms in the fly ovary.

Fig. 1

Stages of Drosophila Oogenesis. Egg chambers stained with 4',6 diamidino-2-phenylindole (DAPI) to label DNA. Anterior portion of ovariole (left) shows early stages starting at the germarium (G). Nurse cells (NC) and follicle cells (FC) are labeled in a stage 8 egg chamber. A stage 10 egg chamber (right) shows that the FC have migrated. The oocyte (O) increases in size as the egg chamber develops. In the most posterior stage 10 egg chamber the oocyte (O) is under the follicle cell layer. All egg chambers at the same magnification.

Fig. 2

Programmed cell death events in early and mid-oogenesis. (a–d) Egg chambers stained with DAPI (blue) to label DNA. (a) A germarium from a nutrient-deprived (Starved) wild-type fly stained with TUNEL (green) to label dying cells. Arrow indicates cells dying in region 2, the central portion of the germarium. (b) Stage 8 healthy egg chamber from a wild-type fly. (c) Abnormal egg chamber from a homozygous dcp-1^prev1 nutrient-deprived fly [49]. The follicle cells have died while the nurse cells remain intact. (d) Degenerating wild-type stage 8 egg chamber shows fragmented and condensed DNA. (e) Caspase activity (green) is noted in the same egg chamber, labeled with an anti-cleaved caspase-3 antibody (Cell Signaling). (f) An induction in autophagy is also shown in the same egg chamber by an increase in LysoTracker (red, Invitrogen). All images at the same magnification.

Fig. 3

Progression and disruption in developmental nurse cell death of late oogenesis. (a–f) Egg chambers stained with DAPI to visualize nurse cell nuclear morphology. (d'–f') DIC images of the same egg chambers in (d–f). (a) Wild-type stage 10 egg chamber prior to dumping. (b) Wild-type stage 11 egg chamber in the process of transferring nurse cell cytoplasm to the oocyte. (c) Wild-type stage 13 egg chamber in which the cytoplasmic transfer is complete, the dorsal appendages are clearly visible but not fully formed, and the nurse cells remnants are dying. (d–d') Wild-type stage 14 egg chamber with no remaining nurse cell remnants and dorsal appendages fully formed. (e–e') NGT/+;UASp-p35/nosGAL4 [50] stage 14 egg chamber with persisting nurse cell nuclei indicated by arrows. NGT and nosGAL4 are germline-specific GAL4 drivers [90]. (f–f') chickadee¹³²⁰ [53] dumpless egg chamber in which nurse cell dumping has not occurred but oocyte development is complete as indicated by fully formed dorsal appendages. All images at the same magnification.