Combined Inhibition of Autophagy and Caspases Fails to Prevent Developmental Nurse Cell Death in the Drosophila melanogaster Ovary

Peterson, Jeanne S.; McCall, Kimberly

doi:10.1371/journal.pone.0076046

Cited by 36 publications

(41 citation statements)

References 36 publications

(51 reference statements)

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“…The average length of control stage 14 oocytes is 523.3 ± 31.8 μm, and muskelin RNAi stage 14 oocytes are on average 520.7 ± 28.7 μm (n = 80 and n = 127 stage 14 oocytes for control and muskelin RNAi, respectively, measured in the total of three replicates; Welch two sample t test P = 0.06). Although distinct from "dumpless" mutants, the effect of muskelin RNAi on the mature egg chambers is comparable to the loss of apoptotic caspases or autophagy players (35). Loss of Muskelin may cause a delay rather than a complete block of nurse cell nuclear degradation, as the number of persisting nurse cell nuclei is reduced in muskelin RNAitreated females with aged mature egg chambers.…”

Section: Functional Classes Of Proteins Changed During Oocyte Maturatmentioning

confidence: 90%

Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

Kronja

Whitfield

Yuan

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The onset of development is marked by two major, posttranscriptionally controlled, events: oocyte maturation (release of the prophase I primary arrest) and egg activation (release from the secondary meiotic arrest). Using quantitative mass spectrometry, we previously described proteome remodeling during Drosophila egg activation. Here, we describe our quantitative mass spectrometry-based analysis of the changes in protein levels during Drosophila oocyte maturation. This study presents the first quantitative survey, to our knowledge, of proteome changes accompanying oocyte maturation in any organism and provides a powerful resource for identifying both key regulators and biological processes driving this critical developmental window. We show that Muskelin, found to be up-regulated during oocyte maturation, is required for timely nurse cell nuclei clearing from mature egg chambers. Other proteins up-regulated at maturation are factors needed not only for late oogenesis but also completion of meiosis and early embryogenesis. Interestingly, the down-regulated proteins are predominantly involved in RNA processing, translation, and RNAi. Integrating datasets on the proteome changes at oocyte maturation and egg activation uncovers dynamics in proteome remodeling during the change from oocyte to embryo. Notably, 66 proteins likely act uniquely during late oogenesis, because they are up-regulated at maturation and down-regulated at activation. We find down-regulation of this class of proteins to be mediated partially by APC/C CORT , a meiosis-specific form of the E3 ligase anaphase promoting complex/ cyclosome (APC/C).he change from oocyte to embryo marks the onset of development. Oocyte maturation is a prerequisite for the oocyte-toembryo transition. In most animals, oocytes undergo a prolonged arrest in prophase I to permit oocyte growth, differentiation, and stockpiling of maternal components. This arrest is released at oocyte maturation, commonly in response to hormonal cues. The nuclear envelope then breaks down, followed by assembly of the meiotic spindle. A secondary meiotic arrest ensues, occurring at metaphase II in most vertebrates and metaphase I in insects (1). The oocyte-to-embryo transition initiates with egg activation, which causes the release of the secondary arrest and the completion of meiosis. In many organisms, egg activation requires fertilization, but egg activation is independent of fertilization in Drosophila (1). In all cases, the onset of embryogenesis requires sperm entry, fusion of the male and female pronuclei, and the start of the mitotic embryonic divisions.How is this complex transition from differentiated oocyte into totipotent embryo regulated? Both oocyte maturation and egg activation occur in a transcriptionally silent context (2-4). These events are thus posttranscriptionally controlled, and translational regulation has been shown to play a crucial role. For example, resumption of meiosis in Xenopus depends on translational activation of cyclin B and mos mRNA by CPEB-mediated polyad...

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Section: Functional Classes Of Proteins Changed During Oocyte Maturatmentioning

confidence: 90%

Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

Kronja

Whitfield

Yuan

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…The following stocks were used: Bam-GFP (kind gift of Dr. D. McKearin)(Chen and McKearin, 2003), UASp-DIAP1 (kind gift of Dr. K. McCall) (Peterson and McCall, 2013), Nanos-Gal4 (kind gift of Dr. E Selva) (White-Cooper, 2012), Bam-Gal4 (kind gift of Dr. D. McKearin)(White-Cooper, 2012), c587-Gal4 (kind gift of Dr. A. Spradling)(Skora and Spradling, 2010), HS-Upd (kind gift of Dr. D. Harrison) (McGregor et al, 2002), UASt-DIAP1-RNAi (kind gift of Dr. A. Bashirullah) (Huh et al, 2004) and HS-DIAP1-RNAi (kind gift of Dr. A. Bashirullah) (Yin and Thummel, 2004). Other stocks were from the Bloomington Drosophila Stock Center (BDSC).…”

Section: Methodsmentioning

confidence: 99%

Niche signaling promotes stem cell survival in the Drosophila testis via the JAK–STAT target DIAP1

Hasan

Hétié

Matunis

2015

Developmental Biology

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Tissue-specific stem cells are thought to resist environmental insults better than their differentiating progeny, but this resistance varies from one tissue to another, and the underlying mechanisms are not well-understood. Here, we use the Drosophila testis as a model system to study the regulation of cell death within an intact niche. This niche contains sperm-producing germline stem cells (GSCs) and accompanying somatic cyst stem cells (or CySCs). Although many signals are known to promote stem cell self-renewal in this tissue, including the highly conserved JAK-STAT pathway, the response of these stem cells to potential death-inducing signals, and factors promoting stem cell survival, have not been characterized. Here we find that both GSCs and CySCs resist cell death better than their differentiating progeny, under normal laboratory conditions and in response to potential death-inducing stimuli such as irradiation or starvation. To ask what might be promoting stem cell survival, we characterized the role of the anti-apoptotic gene Drosophila inhibitor of apoptosis 1 (diap1) in testis stem cells. DIAP1 protein is enriched in the GSCs and CySCs and is a Jak-STAT target. diap1 is necessary for survival of both GSCs and CySCs, and ectopic up-regulation of DIAP1 in somatic cyst cells is sufficient to non-autonomously rescue stress-induced cell death in adjacent differentiating germ cells (spermatogonia). Altogether, our results show that niche signals can promote stem cell survival by up-regulation of highly conserved anti-apoptotic proteins, and suggest that this strategy may underlie the ability of stem cells to resist death more generally.

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“…Shortly after, it was shown that activation of PCD relied on the apical degradation of dBruce by autophagy, which enhanced Dcp-1 function and autophagy upregulation in a positive feedback loop, involving Dcp-1 translocation to mitochondria and its localized suppression of a recently identified autophagy-inhibitor [108], [111]. Nevertheless, since the effective removal of nurse cells has also been reported even when inhibiting both apoptosis and autophagy [112], the conditions under which autophagy functions as or contributes to deathmediating pathways require further elucidation.…”

Section: Functional Conservation Of the Caspase-autophagy Cross-regulmentioning

confidence: 99%

Caspase involvement in autophagy

2017

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Caspases are a family of cysteine proteases widely known as the principal mediators of the apoptotic cell death response, but considerably less so as the contributors to the regulation of pathways outside cellular demise. In regards to autophagy, the modulatory roles of caspases have only recently begun to be adequately described. In contrast to apoptosis, autophagy promotes cell survival by providing energy and nutrients through the lysosomal degradation of cytoplasmic constituents. Under basal conditions autophagy and apoptosis cross-regulate each other through an elaborate network of interconnections which also includes the interplay between autophagyrelated proteins (ATGs) and caspases. In this review we focus on the effects of this crosstalk at the cellular level, as we aim to concentrate the main observations from research conducted so far on the fine-tuning of autophagy by caspases. Several members of this protease-family have been found to directly interact with key ATGs involved in different tiers across the autophagic cascade. Therefore, we firstly outline the core mechanism of macroautophagy in brief. In an effort to emphasize the importance of the intricate cross-regulation of ATGs and caspases, we also present examples drawn from Drosophila and plant models regarding the contribution of autophagy to apoptotic cell death during normal development. Keywords and abbreviationsautophagy; macroautophagy; mammals; caspases; apoptosis; crosstalk; regulation AMBRA-1Activating-molecule-in-Beclin1-regulated-autophagy-1 AMPK AMP-activated-protein-kinase ATG Autophagy-related gene ATG14L ATG14-likeBcl-2 B-cell lymphoma 2 • Autophagy is implicated in many physiological and pathological processes, where apoptosis is also involved DISC Death-inducing signalling complex FADD Fas-associated protein with death domain Open Questions• Does control of autophagy by caspases represent a central or a supplementary mode of regulation of this pathway?• Is caspase activation required to control autophagy?• To what extent do caspases affect autophagy and how exactly their effects on the pathway vary across different contexts?4

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Combined Inhibition of Autophagy and Caspases Fails to Prevent Developmental Nurse Cell Death in the Drosophila melanogaster Ovary

Cited by 36 publications

References 36 publications

Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

Niche signaling promotes stem cell survival in the Drosophila testis via the JAK–STAT target DIAP1

Caspase involvement in autophagy

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