Noncanonical cell death pathways act during <i>Drosophila</i> oogenesis

Peterson, Jeanne S.; Bass, B. Paige; Jue, Deborah; Rodriguez, Antony; Abrams, John; McCall, Kimberly

doi:10.1002/dvg.20306

Cited by 34 publications

(42 citation statements)

References 51 publications

(85 reference statements)

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“…GLCs were generated with these FRT recombinants as well as Tor DP FRT40 18 using the FLP/ FRT/ovo D system as described. 9 To induce clones, larvae were heat shocked for 2 days at 37 1C for 1 h. Under these conditions, o20% of egg chambers have large FC clones (data not shown).…”

Section: Methodsmentioning

confidence: 93%

“…5 Levels of the caspase inhibitor Drosophila inhibitor of apoptosis protein 1 (DIAP1) decline during mid oogenesis, 5 which may be the mechanism that makes this stage of oogenesis more susceptible to PCD. However, mid oogenesis PCD is not regulated by the IAP-binding proteins Rpr, Hid, Grim and Skl, 9 so the mechanism controlling DIAP1 levels is unknown. Recently, we have determined that mitochondrial events and the Bcl-2 family partially control PCD in mid oogenesis.…”

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confidence: 99%

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Role of the insulin/Tor signaling network in starvation-induced programmed cell death in Drosophila oogenesis

Pritchett

McCall

2012

Cell Death Differ

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Amino-acid starvation leads to an inhibition of cellular proliferation and the induction of programmed cell death (PCD) in the Drosophila ovary. Disruption of insulin signaling has been shown to inhibit the progression of oogenesis, but it is unclear whether this phenotype mimics starvation. Here, we investigate whether the insulin-mediated phosphoinositide kinase-3 pathway regulates PCD in mid oogenesis. We reasoned that under well-fed conditions, disruption of positive components of the insulin signaling pathway within the germline would mimic starvation and produce degenerating egg chambers. Surprisingly, mutants did not mimic starvation but instead produced many abnormal egg chambers in which the somatic follicle cells disappeared and the germline persisted. These abnormal egg chambers did not show an induction of caspases and lysosomes like that observed in wild-type (WT) degenerating egg chambers. Egg chambers from insulin signaling mutants were resistant to starvation-induced PCD, indicating that a complete block in insulin-signaling prevents the proper response to starvation. However, target of rapamycin (Tor) mutants did show a phenotype that mimicked WT starvation-induced PCD, indicating an insulin independent regulation of PCD via Tor signaling. These results suggest that inhibition of the insulin signaling pathway is not sufficient to regulate starvation-induced PCD in mid oogenesis. Furthermore, starvation-induced PCD is regulated by Tor signaling converging with the canonical insulin signaling pathway. The insulin-mediated class I phosphoinositide kinase-3 (PI3K) pathway is a highly conserved nutrient-sensing pathway in diverse organisms. In mammals, insulin signaling affects oocyte maturation and fertilization. 1,2 Mutations in the insulin signaling pathway in C. elegans can lengthen life span but reduce fertility. 3,4 Improper insulin signaling in Drosophila leads to reduced body size and female sterility. 5 Thus, insulin signaling is essential for reproduction in diverse organisms, but how this pathway regulates fertility is not fully understood.Proper nutrition during Drosophila oogenesis is critical for egg chamber production. 6-8 Depriving flies of yeast as a protein source leads to programmed cell death (PCD) at two stages: early oogenesis in the germarium and mid oogenesis during stages 7-9. 7 Egg chambers undergoing PCD during mid oogenesis are characterized by nuclear condensation and fragmentation of germline-derived nurse cells (NCs), engulfment by somatic follicle cells (FCs), and ultimately FC death. 5 During PCD in mid oogenesis, dying NCs show characteristics of both apoptotic and autophagic PCD. 5 The effector caspase Death caspase-1 (Dcp-1) is essential for germline PCD in mid oogenesis. dcp-1 mutants that have been starved display mid-stage egg chambers that have a persistence of uncondensed NC nuclei but an absence of FCs. 5 This phenotype indicates that the dcp-1 mutant germline is unable to die in response to starvation, although the FCs respond and undergo PCD. dcp-1 mutants ...

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Section: Methodsmentioning

confidence: 93%

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confidence: 99%

Role of the insulin/Tor signaling network in starvation-induced programmed cell death in Drosophila oogenesis

Pritchett

McCall

2012

Cell Death Differ

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“…This PCD is dependent on nutrient availability and involves ecdysone in mid-stage egg chambers (Pritchett et al, 2009). Much of the cell death in Drosophila ovaries is mediated by noncanonical pathways that do not require RHG proteins (Peterson et al, 2007). Interestingly, similar to the larval salivary glands, starvation-induced cell death in the ovary is dependent on both apoptosis and autophagy (Hou et al, 2008, Nezis et al, 2009.…”

Section: Adult Ovarymentioning

confidence: 99%

Ecdysone-mediated programmed cell death in Drosophila

Nicolson

Denton²,

Kumar³

2015

Int. J. Dev. Biol.

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During Drosophila development, the steroid hormone ecdysone plays a key role in the transition from embryo into larva and then into pupa. It is during larval-pupal metamorphosis that extensive programmed cell death occurs to remove large obsolete larval tissues. During this transition, ecdysone pulses control the expression of specific transcription factors which drive the expression of key genes involved in cell death, thus spatially and temporally controlling programmed cell death. Ecdysone also controls cell death in specific larval and adult tissues. This review focuses on the current knowledge of ecdysone-mediated cell death in Drosophila.

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“…Cell death in the ovary occurs independently of the major initiators of cell death, Reaper, Hid and Grim (Foley and Cooley, 1998;Peterson et al, 2007). The Drosophila ovary contains egg chambers that progress through 14 defined stages of development (King, 1970).…”

Section: Introductionmentioning

confidence: 99%

Bcl-2 proteins and autophagy regulate mitochondrial dynamics during programmed cell death in theDrosophilaovary

et al. 2011

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SUMMARYThe Bcl-2 family has been shown to regulate mitochondrial dynamics during cell death in mammals and C. elegans, but evidence for this in Drosophila has been elusive. Here, we investigate the regulation of mitochondrial dynamics during germline cell death in the Drosophila melanogaster ovary. We find that mitochondria undergo a series of events during the progression of cell death, with remodeling, cluster formation and uptake of clusters by somatic follicle cells. These mitochondrial dynamics are dependent on caspases, the Bcl-2 family, the mitochondrial fission and fusion machinery, and the autophagy machinery. Furthermore, Bcl-2 family mutants show a striking defect in cell death in the ovary. These data indicate that a mitochondrial pathway is a major mechanism for activation of cell death in Drosophila oogenesis.

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Noncanonical cell death pathways act during Drosophila oogenesis

Cited by 34 publications

References 51 publications

Role of the insulin/Tor signaling network in starvation-induced programmed cell death in Drosophila oogenesis

Role of the insulin/Tor signaling network in starvation-induced programmed cell death in Drosophila oogenesis

Ecdysone-mediated programmed cell death in Drosophila

Bcl-2 proteins and autophagy regulate mitochondrial dynamics during programmed cell death in theDrosophilaovary

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