Phagocytosis genes nonautonomously promote developmental cell death in the Drosophila ovary

Programmed cell death (PCD) is usually considered a cell-autonomous suicide program, synonymous with apoptosis. Recent research has revealed that PCD is complex, with at least a dozen cell death modalities. Here, we demonstrate that the large-scale nonapoptotic developmental PCD in the Drosophila ov...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 9; pp. E1246 - E1255
Main Authors Timmons, Allison K., Mondragon, Albert A., Schenkel, Claire E., Yalonetskaya, Alla, Taylor, Jeffrey D., Moynihan, Katherine E., Etchegaray, Jon Iker, Meehan, Tracy L., McCall, Kimberly
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 01.03.2016
National Acad Sciences
SeriesPNAS Plus
Subjects
Animals
Apoptosis
Biological Sciences
Cell Death - genetics
Cellular biology
Drosophila
Drosophila - genetics
Female
Insects
Ovary - cytology
Phagocytosis - genetics
PNAS Plus
Reproductive system
engulfment
phagocytosis
ovary
cell death
Drosophila
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Summary:Programmed cell death (PCD) is usually considered a cell-autonomous suicide program, synonymous with apoptosis. Recent research has revealed that PCD is complex, with at least a dozen cell death modalities. Here, we demonstrate that the large-scale nonapoptotic developmental PCD in the Drosophila ovary occurs by an alternative cell death program where the surrounding follicle cells nonautonomously promote death of the germ line. The phagocytic machinery of the follicle cells, including Draper, cell death abnormality (Ced)-12, and c-Jun N-terminal kinase (JNK), is essential for the death and removal of germ-line–derived nurse cells during late oogenesis. Cell death events including acidification, nuclear envelope permeabilization, and DNA fragmentation of the nurse cells are impaired when phagocytosis is inhibited. Moreover, elimination of a small subset of follicle cells prevents nurse cell death and cytoplasmic dumping. Developmental PCD in the Drosophila ovary is an intriguing example of nonapoptotic, nonautonomous PCD, providing insight on the diversity of cell death mechanisms.
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Edited by Terry L. Orr-Weaver, Whitehead Institute, Cambridge, MA, and approved January 15, 2016 (received for review November 24, 2015)
Author contributions: A.K.T., A.A.M., C.E.S., A.Y., J.D.T., K.E.M., J.I.E., T.L.M., and K.M. designed research; A.K.T., A.A.M., C.E.S., A.Y., J.D.T., K.E.M., J.I.E., and T.L.M. performed research; A.K.T., A.A.M., C.E.S., A.Y., J.D.T., K.E.M., J.I.E., T.L.M., and K.M. analyzed data; and A.K.T., A.A.M., and K.M. wrote the paper.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1522830113