scholarly journals Murder on the Ovarian Express: A Tale of Non-Autonomous Cell Death in the Drosophila Ovary

Cells ◽  
2021 ◽  
Vol 10 (6) ◽  
pp. 1454
Author(s):  
Diane Patricia Vig Lebo ◽  
Kimberly McCall
Keyword(s):  
Cell Death ◽  
Follicle Cells ◽  
Nurse Cells ◽  
Fine Line ◽  
Egg Chambers ◽  
Drosophila Ovary ◽  
Size And Structure

Throughout oogenesis, Drosophila egg chambers traverse the fine line between survival and death. After surviving the ten early and middle stages of oogenesis, egg chambers drastically change their size and structure to produce fully developed oocytes. The development of an oocyte comes at a cost, the price is the lives of the oocyte’s 15 siblings, the nurse cells. These nurse cells do not die of their own accord. Their death is dependent upon their neighbors—the stretch follicle cells. Stretch follicle cells are nonprofessional phagocytes that spend the final stages of oogenesis surrounding the nurse cells and subsequently forcing the nurse cells to give up everything for the sake of the oocyte. In this review, we provide an overview of cell death in the ovary, with a focus on recent findings concerning this phagocyte-dependent non-autonomous cell death.

scholarly journals Phagocytosis genes nonautonomously promote developmental cell death in the Drosophila ovary

2016 ◽  
Vol 113 (9) ◽  
pp. E1246-E1255 ◽  
Author(s):  
Allison K. Timmons ◽  
Albert A. Mondragon ◽  
Claire E. Schenkel ◽  
Alla Yalonetskaya ◽  
Jeffrey D. Taylor ◽  
...  
Keyword(s):  
Cell Death ◽  
Large Scale ◽  
Germ Line ◽  
Follicle Cells ◽  
Small Subset ◽  
Nurse Cells ◽  
Cell Death Program ◽  
Cell Death Mechanisms ◽  
Developmental Cell Death ◽  
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 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.

scholarly journals Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis

2010 ◽  
Vol 190 (4) ◽  
pp. 523-531 ◽  
Author(s):  
Ioannis P. Nezis ◽  
Bhupendra V. Shravage ◽  
Antonia P. Sagona ◽  
Trond Lamark ◽  
Geir Bjørkøy ◽  
...  
Keyword(s):  
Cell Death ◽  
Drosophila Melanogaster ◽  
Dna Fragmentation ◽  
Nurse Cell ◽  
Nurse Cells ◽  
Cell Nuclei ◽  
Cytoplasmic Material ◽  
Fragmented Dna ◽  
Egg Chambers ◽  
Autophagic Degradation

Autophagy is an evolutionarily conserved pathway responsible for degradation of cytoplasmic material via the lysosome. Although autophagy has been reported to contribute to cell death, the underlying mechanisms remain largely unknown. In this study, we show that autophagy controls DNA fragmentation during late oogenesis in Drosophila melanogaster. Inhibition of autophagy by genetically removing the function of the autophagy genes atg1, atg13, and vps34 resulted in late stage egg chambers that contained persisting nurse cell nuclei without fragmented DNA and attenuation of caspase-3 cleavage. The Drosophila inhibitor of apoptosis (IAP) dBruce was found to colocalize with the autophagic marker GFP-Atg8a and accumulated in autophagy mutants. Nurse cells lacking Atg1 or Vps34 in addition to dBruce contained persisting nurse cell nuclei with fragmented DNA. This indicates that autophagic degradation of dBruce controls DNA fragmentation in nurse cells. Our results reveal autophagic degradation of an IAP as a novel mechanism of triggering cell death and thereby provide a mechanistic link between autophagy and cell death.

Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes

Development ◽  
1997 ◽  
Vol 124 (24) ◽  
pp. 4927-4937 ◽  
Author(s):  
A. Gonzalez-Reyes ◽  
H. Elliott ◽  
D. St Johnston
Keyword(s):  
Symmetry Breaking ◽  
Germinal Vesicle ◽  
Follicle Cells ◽  
Axis Formation ◽  
Main Body ◽  
Nurse Cells ◽  
Egg Chambers ◽  
Anterior Posterior ◽  
Oocyte Selection

The two main body axes in Drosophila become polarised as a result of a series of symmetry-breaking steps during oogenesis. Two of the sixteen germline cells in each egg chamber develop as pro-oocytes, and the first asymmetry arises when one of these cells is selected to become the oocyte. Anterior-posterior polarity originates when the oocyte then comes to lie posterior to the nurse cells and signals through the Gurken/Egfr pathway to induce the adjacent follicle cells to adopt a posterior fate. This directs the movement of the germinal vesicle and associated gurken mRNA from the posterior to an anterior corner of the oocyte, where Gurken protein signals for a second time to induce the dorsal follicle cells, thereby polarising the dorsal-ventral axis. Here we describe a group of five genes, the spindle loci, which are required for each of these polarising events. spindle mutants inhibit the induction of both the posterior and dorsal follicle cells by disrupting the localisation and translation of gurken mRNA. Moreover, the oocyte often fails to reach the posterior of mutant egg chambers and differentiates abnormally. Finally, double mutants cause both pro-oocytes to develop as oocytes, by delaying the choice between these two cells. Thus, these mutants reveal a novel link between oocyte selection, oocyte positioning and axis formation in Drosophila, leading us to propose that the spindle genes act in a process that is common to several of these events.

scholarly journals INTERCELLULAR MIGRATION OF CENTRIOLES IN THE GERMARIUM OF DROSOPHILA MELANOGASTER

1970 ◽  
Vol 45 (2) ◽  
pp. 306-320 ◽  
Author(s):  
Anthony P. Mahowald ◽  
Joan M. Strassheim
Keyword(s):  
Follicle Cell ◽  
Cell Cluster ◽  
Follicle Cells ◽  
Oocyte Nucleus ◽  
Nurse Cells ◽  
Serial Sections ◽  
Cell Border ◽  
Ring Canals ◽  
Egg Chambers ◽  
Stage 1

A cluster of centrioles has been found in the early Drosophila oocyte. Since the oocyte is connected to 15 nurse cells by a system of intercellular bridges or ring canals, the possibility that the cluster of centrioles arose in the germarium from an intercellular migration of centrioles from the nurse cells to the oocyte was analyzed in serial sections for the electron microscope. Initially, all of the 16 cells of the future egg chambers possess centrioles, which are located in a juxtanuclear position. At the time the 16 cell cluster becomes arranged in a lens-shaped layer laterally across the germarium, the centrioles lose their juxtanuclear position and move towards the oocyte. By the time the 16 cell cluster of cells is surrounded by follicle cells (Stage 1), between 14 and 17 centrioles are found in the oocyte. Later, these centrioles become located between the oocyte nucleus and the follicle cell border and become aggregated into a cluster less than 1.5 µ in its largest dimension. The fate of these centrioles in the oocyte is not known. The fine structure of the germarium and the early oocyte is also described.

scholarly journals An RNAi screen of the kinome in epithelial follicle cells of the Drosophila melanogaster ovary reveals genes required for proper germline death and clearance

2021 ◽  
Vol 11 (2) ◽  
Author(s):  
Diane P V Lebo ◽  
Alice Chirn ◽  
Jeffrey D Taylor ◽  
Andre Levan ◽  
Valentina Doerre Torres ◽  
...  
Keyword(s):  
Cell Death ◽  
Drosophila Melanogaster ◽  
Follicle Cells ◽  
Multiple Time ◽  
Cell Clearance ◽  
Germline Cells ◽  
Multiple Time Points ◽  
Cell Corpse ◽  
Cell Corpse Clearance ◽  
Drosophila Ovary

Abstract Programmed cell death and cell corpse clearance are an essential part of organismal health and development. Cell corpses are often cleared away by professional phagocytes such as macrophages. However, in certain tissues, neighboring cells known as nonprofessional phagocytes can also carry out clearance functions. Here, we use the Drosophila melanogaster ovary to identify novel genes required for clearance by nonprofessional phagocytes. In the Drosophila ovary, germline cells can die at multiple time points. As death proceeds, the epithelial follicle cells act as phagocytes to facilitate the clearance of these cells. We performed an unbiased kinase screen to identify novel proteins and pathways involved in cell clearance during two death events. Of 224 genes examined, 18 demonstrated severe phenotypes during developmental death and clearance while 12 demonstrated severe phenotypes during starvation-induced cell death and clearance, representing a number of pathways not previously implicated in phagocytosis. Interestingly, it was found that several genes not only affected the clearance process in the phagocytes, but also non-autonomously affected the process by which germline cells died. This kinase screen has revealed new avenues for further exploration and investigation.

scholarly journals Vps13 is required for timely removal of nurse cell corpses

Development ◽  
2020 ◽  
Vol 147 (20) ◽  
pp. dev191759
Author(s):  
Anita I. E. Faber ◽  
Marianne van der Zwaag ◽  
Hein Schepers ◽  
Ellie Eggens-Meijer ◽  
Bart Kanon ◽  
...  
Keyword(s):  
Cell Death ◽  
Plasma Membrane ◽  
Programmed Cell Death ◽  
Nurse Cell ◽  
Close Association ◽  
Follicle Cells ◽  
Nurse Cells ◽  
Lipid Transfer ◽  
Membranous Structure ◽  
Membrane Contact Sites

ABSTRACTProgrammed cell death and consecutive removal of cellular remnants is essential for development. During late stages of Drosophila melanogaster oogenesis, the small somatic follicle cells that surround the large nurse cells promote non-apoptotic nurse cell death, subsequently engulf them, and contribute to the timely removal of nurse cell corpses. Here, we identify a role for Vps13 in the timely removal of nurse cell corpses downstream of developmental programmed cell death. Vps13 is an evolutionarily conserved peripheral membrane protein associated with membrane contact sites and lipid transfer. It is expressed in late nurse cells, and persistent nurse cell remnants are observed when Vps13 is depleted from nurse cells but not from follicle cells. Microscopic analysis revealed enrichment of Vps13 in close proximity to the plasma membrane and the endoplasmic reticulum in nurse cells undergoing degradation. Ultrastructural analysis uncovered the presence of an underlying Vps13-dependent membranous structure in close association with the plasma membrane. The newly identified structure and function suggests the presence of a Vps13-dependent process required for complete degradation of bulky remnants of dying cells.

scholarly journals Mutations in the midway Gene Disrupt a Drosophila Acyl Coenzyme A: Diacylglycerol Acyltransferase

Genetics ◽  
2002 ◽  
Vol 160 (4) ◽  
pp. 1511-1518
Author(s):  
Michael Buszczak ◽  
Xiaohui Lu ◽  
William A Segraves ◽  
Ta Yuan Chang ◽  
Lynn Cooley
Keyword(s):  
Cell Death ◽  
Insect Cells ◽  
Coenzyme A ◽  
Neutral Lipids ◽  
Diacylglycerol Acyltransferase ◽  
Nurse Cells ◽  
Germline Expression ◽  
Egg Chambers ◽  
Acyl Coenzyme A

Abstract During Drosophila oogenesis, defective or unwanted egg chambers are eliminated during mid-oogenesis by programmed cell death. In addition, final cytoplasm transport from nurse cells to the oocyte depends upon apoptosis of the nurse cells. To study the regulation of germline apoptosis, we analyzed the midway mutant, in which egg chambers undergo premature nurse cell death and degeneration. The midway gene encodes a protein similar to mammalian acyl coenzyme A: diacylglycerol acyltransferase (DGAT), which converts diacylglycerol (DAG) into triacylglycerol (TAG). midway mutant egg chambers contain severely reduced levels of neutral lipids in the germline. Expression of midway in insect cells results in high levels of DGAT activity in vitro. These results show that midway encodes a functional DGAT and that changes in acylglycerol lipid metabolism disrupt normal egg chamber development in Drosophila.

An ultrastructural study of ovarian development in the otu7 mutant of Drosophila melanogaster

1984 ◽  
Vol 67 (1) ◽  
pp. 87-119
Author(s):  
D.L. Bishop ◽  
R.C. King
Keyword(s):  
Polytene Chromosomes ◽  
Vital Role ◽  
Follicle Cells ◽  
Vitelline Membrane ◽  
Nurse Cells ◽  
Border Cells ◽  
Stage Of Development ◽  
Ring Canals ◽  
Egg Chambers ◽  
Reduced Rate

Females homozygous for the otu7 allele produce ovarian tumours, as well as egg chambers that reach a relatively late stage of development. Mutant ovarian nurse cells contain giant polytene chromosomes. These are transcriptionally active, and RNA is transported to the oocyte through ring canals, although at reduced rate. Vitellogenic oocytes are endocytotically active. Protein (alpha yolk) spheres are formed, but glycogen (beta yolk) spheres were never seen in the ooplasm. Follicle cells migrate normally and secrete more vitelline membrane and chorion than is required to cover the slowly growing oocyte. Specialized follicle cells also secrete relatively normal dorsal appendages. The micropylar cone is secreted by another cluster of specialized follicle cells called border cells. These are out of phase with the oocyte, and the forming micropylar cone prevents the nurse cells from passing the remainder of their cytoplasm to the oocyte. The result is a morphologically abnormal chamber blocked at the p-12 stage. Sections through the micropylar cone of a p-12 chamber demonstrated that one of the border cells formed a projection containing a bundle of microtubules. Secretions of the border cells were deposited against this tube, which later degenerates or is withdrawn. Normally this results in a canal, the micropyle, through which the sperm enters the egg. The slowed growth of the mutant oocyte presumably results from a defect in the transport of fluids or charged molecules to it, and the otu+ gene is therefore believed to play a vital role in this process.

Cell death in ovarian chambers of Drosophila melanogaster

Development ◽  
1976 ◽  
Vol 35 (3) ◽  
pp. 521-533
Author(s):  
F. Giorgi ◽  
P. Deri
Keyword(s):  
Cell Death ◽  
Drosophila Melanogaster ◽  
Morphological Change ◽  
Current Literature ◽  
Normal Development ◽  
Nuclear Material ◽  
Ultrastructural Analysis ◽  
Follicle Cells ◽  
Nurse Cells ◽  
Cell Cytoplasm

An ultrastructural analysis has been made of certain ovarian chambers undergoing ab-normal development. The earliest morphological change in these chambers consists of thealteration of the nuclear material which is then followed by engulfment of portions of thenurse cell cytoplasm, including the nuclear fragments, into the overlying follicle cells. Thecontinuation of this process leads to the progressive disappearance of nurse cells with theconcomitant formation of huge dense vacuoles in the follicle layer. The morphological featuresdescribed in the present investigation are similar to those found in other tissues and inter-preted as leading to cell death. It is suggested that certain ovarian chambers undergo celldeath as a result of the incapability of furthering their development. The role played by celldeath in oogenesis is also discussed on the basis of the current literature.

Different 3′ untranslated regions target alternatively processed hu-li tai shao (hts) transcripts to distinct cytoplasmic locations during Drosophila oogenesis

1999 ◽  
Vol 112 (19) ◽  
pp. 3385-3398 ◽  
Author(s):  
K.L. Whittaker ◽  
D. Ding ◽  
W.W. Fisher ◽  
H.D. Lipshitz
Keyword(s):  
Germ Line ◽  
Protein Isoforms ◽  
Follicle Cells ◽  
Untranslated Regions ◽  
Nurse Cells ◽  
Anterior Pole ◽  
Amino Terminal ◽  
Alternative Processing ◽  
Carboxy Terminal ◽  
Drosophila Ovary

Cytoplasmic mRNA localization is one method by which protein production is restricted to a particular intracellular site. We report here a novel mechanism for localization of transcripts encoding distinct protein isoforms to different destinations. Alternative processing of transcripts produced in the Drosophila ovary by the hu-li tai shao (hts) locus introduces distinct 3′ untranslated regions (3′UTRs) that differentially localize the mRNAs. Three classes of hts mRNA (R2, N32 and N4) are synthesized in the germ line nurse cells and encode proteins with adducin-homologous amino-terminal regions but divergent carboxy-terminal domains. The R2 and N32 classes of mRNA remain in the nurse cells and are not transported into the oocyte. In contrast, the N4 class of transcripts is transported from the nurse cells into the oocyte starting at stage 1, is subsequently localized to the oocyte cortex at stage 8 and then to the anterior pole from stage 9 on. All aspects of N4 transcript transport and localization are directed by the 345-nucleotide(nt)-long 3′ untranslated region (3′UTR). The organization of localization elements in the N4 3′UTR is modular: a 150 nt core is sufficient to direct transport and localization throughout oogenesis. Additional 3′UTR elements function additively together with this core region at later stages of oogenesis to maintain or enhance anterior transcript anchoring. The swallow locus is required to maintain hts transcripts at the anterior pole of the oocyte and functions through the N4 3′UTR. In addition to the three classes of germ line-expressed hts transcripts, a fourth class (R1) is expressed in the somatic follicle cells that surround the germ line cells. This transcript class encodes the Drosophila orthologue of mammalian adducin.

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