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

During the final stages of Drosophila melanogaster oogenesis fifteen nurse cells, sister cells to the oocyte, degenerate as part of normal development. This process involves at least two cell death mechanisms, caspase-dependent cell death and autophagy, as indicated by apoptosis and autophagy markers. In addition, mutations affecting either caspases or autophagy partially reduce nurse cell removal, leaving behind end-stage egg chambers with persisting nurse cell nuclei. To determine whether apoptosis and autophagy work in parallel to degrade and remove these cells as is the case with salivary glands during pupariation, we generated mutants doubly affecting caspases and autophagy. We found no significant increase in either the number of late stage egg chambers containing persisting nuclei or in the number of persisting nuclei per egg chamber in the double mutants compared to single mutants. These findings suggest that there is another cell death mechanism functioning in the ovary to remove all nurse cell remnants from late stage egg chambers.

• Publication year

  2013

• Venue

  PLoS ONE

• Publication date

  2013-09-30

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1371/journal.pone.0076046PMID 24098761PMCID 3786910
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Control of Nonapoptotic Developmental Cell Death in Caenorhabditis elegans by a Polyglutamine-Repeat Protein

  2012cited by this paper
• Eaten alive! Cell death by primary phagocytosis: 'phagoptosis'.

  2012cited by this paper
• The lack of autophagy triggers precocious activation of Notch signaling during Drosophila oogenesis

  2012influential reference
• Draper acts through the JNK pathway to control synchronous engulfment of dying germline cells by follicular epithelial cells

  2012cited by this paper
• Neuronal Death Induced by Nanomolar Amyloid β Is Mediated by Primary Phagocytosis of Neurons by Microglia*

  2011cited by this paper
• Inhibition of Microglial Phagocytosis Is Sufficient To Prevent Inflammatory Neuronal Death

  2011cited by this paper
• p62, Ref(2)P and ubiquitinated proteins are conserved markers of neuronal aging, aggregate formation and progressive autophagic defects

  2011cited by this paper
• Autophagy in Drosophila ovaries is induced by starvation and is required for oogenesis

  2011cited by this paper
• Genetic control of necrosis - another type of programmed cell death.

  2010cited by this paper
• Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis

  2010influential reference
• Autophagy, not apoptosis, is essential for midgut cell death in Drosophila.

  2009cited by this paper
• Cracking open cell death in the Drosophila ovary

  2009cited by this paper
• The development of Drosophila melanogaster

  2009cited by this paper
• Cell-autonomous requirement for DNaseII in non-apoptotic cell death

  2009cited by this paper
• The cell biology of autophagy in metazoans: a developing story

  2008cited by this paper
• Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila.

  2007influential reference
• Engulfment is required for cell competition.

  2007influential reference
• A morphologically conserved nonapoptotic program promotes linker cell death in Caenorhabditis elegans.

  2007cited by this paper
• The Drosophila caspases Strica and Dronc function redundantly in programmed cell death during oogenesis

  2007cited by this paper
• A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion.

  2007cited by this paper
• Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death.

  2007cited by this paper
• Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila.

  2007cited by this paper
• Noncanonical cell death pathways act during Drosophila oogenesis

  2007cited by this paper
• A dual function for Deep orange in programmed autophagy in the Drosophila melanogaster fat body.

  2006cited by this paper
• Role and regulation of starvation-induced autophagy in the Drosophila fat body.

  2004cited by this paper
• Stage-specific regulation of caspase activity in drosophila oogenesis.

  2003influential reference
• Germline cell death is inhibited by P-element insertions disrupting the dcp-1/pita nested gene pair in Drosophila.

  2003influential reference
• Phagocytosis promotes programmed cell death in C. elegans

  2001cited by this paper
• Altered Cytochrome c Display Precedes Apoptotic Cell Death in Drosophila

  1999cited by this paper
• G alphas-induced neurodegeneration in Caenorhabditis elegans.

  1998cited by this paper
• Requirement for DCP-1 caspase during Drosophila oogenesis.

  1998cited by this paper
• Apoptosis of nurse cells at the late stages of oogenesis of Drosophila melanogaster

  1998cited by this paper
• Apoptosis in late stage Drosophila nurse cells does not require genes within the H99 deficiency.

  1998cited by this paper
• Identifying loci required for follicular patterning using directed mosaics.

  1998cited by this paper
• Gαs-Induced Neurodegeneration inCaenorhabditis elegans

  1998cited by this paper
• Neuropathology of Degenerative Cell Death in Caenorhabditis elegans

  1997cited by this paper
• The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster.

  1996cited by this paper
• Cell death in ovarian chambers of Drosophila melanogaster.

  1976cited by this paper
• Ovarian Development in Drosophila Melanogaster

  1970influential reference
• Development in DROSOPHILA MELANOGASTER.

  1927cited by this paper

• Sacrificing cells of the cyst: non-apoptotic cell death in germline cysts via acidification

  2025cites this paper
• Drosophila as a model to study autophagy during oogenesis.

  2025cites this paper
• Multi-modal comparison of molecular programs driving nurse cell death and clearance in Drosophila melanogaster oogenesis

  2024cites this paper
• Finishing the egg.

  2023cites this paper
• Understanding the diversity and dynamics of in vivo efferocytosis: Insights from the fly embryo

  2023cites this paper
• Murder on the Ovarian Express: A Tale of Non-Autonomous Cell Death in the Drosophila Ovary

  2021cites this paper
• Role of autophagy in follicular development and maintenance of primordial follicular pool in the ovary

  2021cites this paper
• Elimination of nurse cell nuclei that shuttle into oocytes during oogenesis

  2021cites this paper
• An RNAi screen of the kinome in epithelial follicle cells of the Drosophila melanogaster ovary reveals genes required for proper germline death and clearance

  2021cites this paper
• An overview of autophagy: Mechanism, regulation and research progress.

  2021cites this paper
• Major Scenarios of Genetically Regulated Cell Death during Oogenesis in Drosophilamelanogaster

  2020cites this paper
• Fusion of Drosophila oocytes with specified germline sister cells

  2020cites this paper
• An ultrastructural study of the ovary cord organization and oogenesis in the amphibian leech Batracobdella algira (Annelida, Clitellata, Hirudinida)

  2020cites this paper
• Vps13 is required for timely removal of nurse cell corpses

  2020cites this paper
• Cell death in animal development

  2020cites this paper
• Lysosomal Machinery Drives Extracellular Acidification to Direct Non-apoptotic Cell Death

  2019cites this paper
• VPS13A: shining light on its localization and function

  2019cites this paper
• Nuclear degradation dynamics in a nonapoptotic programmed cell death

  2019cites this paper
• Phagocyte Responses to Cell Death in Flies.

  2019cites this paper
• Components Required for the Death and Degradation of the Linker Cell in C. Elegans

  2018cites this paper
• The ABC Transporter Eato Promotes Cell Clearance in the Drosophila melanogaster Ovary

  2018cites this paper
• Redefining reproductive dormancy in Drosophila as a general stress response to cold temperatures.

  2018cites this paper
• I Spy in the Developing Fly a Multitude of Ways to Die

  2018cites this paper
• Captivity effects on immune response and steroid plasma levels of a Brazilian toad (Rhinella schneideri)

  2017cites this paper
• Control of non-apoptotic nurse cell death by engulfment genes in Drosophila

  2017cites this paper
• Ovaries of the white worm (Enchytraeus albidus, Annelida, Clitellata) are composed of 16-celled meroistic germ-line cysts.

  2017cites this paper
• White blood cell profiles in amphibians help to explain disease susceptibility following temperature shifts.

  2017cites this paper
• Non-apoptotic cell death in animal development

  2017cites this paper
• Caspase involvement in autophagy

  2017cites this paper
• Phagocytosis genes nonautonomously promote developmental cell death in the Drosophila ovary

  2016cites this paper
• Protease signaling in animal and plant‐regulated cell death

  2016cites this paper
• A LAPF/phafin1-like protein regulates TORC1 and lysosomal membrane permeabilization in response to endoplasmic reticulum membrane stress

  2015cites this paper
• Phagocytosis genes and the JNK signaling pathway promote developmental programmed cell death and are essential for engulfment of the dying germline in the Drosophila ovary

  2015influential citation
• The End of the Beginning: Cell Death in the Germline.

  2015cites this paper
• Niche signaling promotes stem cell survival in the Drosophila testis via the JAK-STAT target DIAP1.

  2015cites this paper
• Detection of Cell Death and Phagocytosis in the Drosophila Ovary.

  2015cites this paper
• Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

  2014cites this paper
• Autophagy in Drosophila: From Historical Studies to Current Knowledge

  2014cites this paper
• Detecting apoptosis in Drosophila tissues and cells.

  2014cites this paper
• Nuclear positioning by actin cables and perinuclear actin

  2014cites this paper
• Diversity of cell death pathways: insight from the fly ovary.

  2013cites this paper
• Sacri fi cing cells of the cyst: non-apoptotic cell death in germline cysts via acidi fi cation

  year unknowncites this paper