Cell death in ovarian chambers of Drosophila melanogaster

Development ◽  
1976 ◽  
Vol 35 (3) ◽  
pp. 521-533
Author(s):  
F. Giorgi ◽  
P. Deri

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.

1966 ◽  
Vol 28 (2) ◽  
pp. 199-208 ◽  
Author(s):  
F. A. Muckenthaler ◽  
A. P. Mahowald

Tritiated thymidine was injected into 2-day-old Drosophila melanogaster females, and tissue sections were prepared from the ovary for radioautography with both the light and electron microscopes. Besides the expected incorporation of H3-thymidine into nuclei of nurse cells and follicle cells, there was a relatively high level of incorporation of label into ooplasmic DNA. The highest level of incorporation occurred at stage 12. At the same time, the 15 nurse cell nuclei also incorporate thymidine in spite of the fact that they are breaking down and degenerating. The label in the ooplasm is not removed by extraction with DNase (although this removes nuclear label) unless extraction is preceded by a treatment with protease. Electron microscopic radioautography revealed that 36% of the silver grains resulting from decay of H3-thymidine are found over mitochondria, with a further 28% being located within 0.25 µ of these organelles. The remaining 36% of the silver grains was not found to be associated with any organelles, and it probably represents synthesis in the cytoplasm by the "storage DNA" characteristic of many eggs. It is suggested that one mechanism acting throughout the egg chamber is responsible for the synchronous synthesis of DNA in the degenerating nurse cells, in the mitochondria of the egg, and in the "storage DNA" of the ooplasm.


2005 ◽  
Vol 25 (23) ◽  
pp. 10329-10337 ◽  
Author(s):  
Fabienne Desmots ◽  
Helen R. Russell ◽  
Youngsoo Lee ◽  
Kelli Boyd ◽  
Peter J. McKinnon

ABSTRACT Scythe (BAT3 [HLA-B-associated transcript 3]) is a nuclear protein that has been implicated in apoptosis, as it can modulate Reaper, a central apoptotic regulator in Drosophila melanogaster. While Scythe can markedly affect Reaper-dependent apoptosis in Xenopus laevis cell extracts, the function of Scythe in mammals is unknown. Here, we report that inactivation of Scythe in the mouse results in lethality associated with pronounced developmental defects in the lung, kidney, and brain. In all cases, these developmental defects were associated with dysregulation of apoptosis and cellular proliferation. Scythe − / − cells were also more resistant to apoptosis induced by menadione and thapsigargin. These data show that Scythe is critical for viability and normal development, probably via regulation of programmed cell death and cellular proliferation.


2010 ◽  
Vol 190 (4) ◽  
pp. 523-531 ◽  
Author(s):  
Ioannis P. Nezis ◽  
Bhupendra V. Shravage ◽  
Antonia P. Sagona ◽  
Trond Lamark ◽  
Geir Bjørkøy ◽  
...  

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.


2021 ◽  
Vol 11 (2) ◽  
Author(s):  
Diane P V Lebo ◽  
Alice Chirn ◽  
Jeffrey D Taylor ◽  
Andre Levan ◽  
Valentina Doerre Torres ◽  
...  

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.


Development ◽  
2020 ◽  
Vol 147 (20) ◽  
pp. dev191759
Author(s):  
Anita I. E. Faber ◽  
Marianne van der Zwaag ◽  
Hein Schepers ◽  
Ellie Eggens-Meijer ◽  
Bart Kanon ◽  
...  

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.


Cells ◽  
2021 ◽  
Vol 10 (6) ◽  
pp. 1454
Author(s):  
Diane Patricia Vig Lebo ◽  
Kimberly McCall

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.


1930 ◽  
Vol s2-73 (292) ◽  
pp. 617-630
Author(s):  
R.A. R. GRESSON

1. By the use of Feulgen's ‘nuclealreaktion’ certain points of Tenthredinid oogenesis have been subjected to closer study. The chromatin of the early nurse-cells of Allantus pallipes exists in the form of granules, the majority of which occur close to the nuclear membrane. In the older cells a nuclear network appears in which is distributed granules of chromatin. In Thrinax mixta, where the ovarioles were more highly developed, the chromatin of the nurse-cells occurs as granules scattered through the nucleus; a nuclear network is not present, but certain granules appear to be connected by a thread. The granules which were shown to surround the nurse-cell nuclei (in material treated by Bensley's method and also by fixation in Bouin's picro-formol and subsequently stained in iron haematoxylin) and which were formerly regarded as chromatin emissions from the nurse-cell nuclei (9) were not revealed by Feulgen's technique. They therefore cannot be regarded as chromatin. Their precise nature and origin remains undetermined. 2. The nucleoli of the early nurse-cells of both species, as revealed by Mann's methyl-blue eosin, are faintly basophil. Later they break up into a number of basophil bodies which undergo fragmentation; formerly (technique and reference as in 1) the basophil nucleolus and the basophil bodies originating from it were termed ‘nuclear material’ undergoing fragmentation. While this basophil nucleolar material presents a fragmented appearance, it increases in amount as evidenced by the large number of basophil bodies present in the older nurse-cell nuclei. This material is utilized for the nourishment of the egg after the latter engulfs the nurse-cell nuclei. Nucleolar extrusions to the cytoplasm do not occur. 3. The behaviour of the chromatin of the follicle-cell nuclei is similar to that of the nurse-cell nuclei except that in Allantus pallipes the nuclear chromatin network as demonstrated by Feulgen's technique disappears in the older cells. 4. The nucleoli of the follicle-cells are basophil. They become broken up in the older cells, but in most cases the resulting masses remain in contact. Nucleolar extrusions to the cytoplasm do not occur. 5. The occurrence of deeply basophil material in the cytoplasm of the follicle-cells of Thrinax mixta stained with Mann's methyl-blue eosin, formerly described for Bouin fixed material stained in iron haematoxylin (9), suggests that some substance in solution may be passed into the ooplasm; extrusion of granules from the follicle-cells to the ooplasm does not take place. 6. The absence or non-visibility of chromatin (Feulgen's technique) from the oocytes of Thrinax mixta, and its disappearance from the older oocytes of Allantus pallipes , would indicate that the chromatin undergoes a chemical change during oogenesis such as suggested by Koch for Chilopods. 7. The oxyphil and basophil nucleoli of the oocytes do not react to Feulgen's technique for chromatin; this agrees with Ludford's findings for the mouse and for Limnaeastagnalis.


1928 ◽  
Vol s2-71 (284) ◽  
pp. 541-561
Author(s):  
A. D. PEACOCK ◽  
R.A. R. GRESSON

1. Ovary formation in Tenthredinidae follows the general hymenopterous plan. 2. Nurse-cell phenomena are as follows: the nuclei of the first nutritive chamber are surrounded by a chromatin cloud and many of them contain irregular darkly-staining masses of nuclear material, which masses may also be present in the riper chambers; the granules given off from the nuclei into the chromatin cloud eventually become surrounded by a vesicle and give rise to the ‘secondary’ or ‘accessory’ nuclei. 3. Oocyte nucleolar phenomena show the following: the nucleoli in Thrinax mixta and Platycampus luridiventris give rise to buds which become free; in one case buds were observed close to the inner surface of the nuclear membrane in Allantus (Emphytus) pallipes are shown what are apparently later stages of this process, viz. the passage of the buds through the nuclear membrane into the egg substance and their formation there into accessory nuclei. 4. The fate of the nurse-cells is shown in the older nutritive chambers and oocytes--the cell boundaries become indistinct and some of the cytoplasm, together with contained accessory nuclei, passes by a narrow channel into the oocyte. The cytoplasmic flow becomes more marked in the last chamber. In the final stages, shown in the last chamber, all the cells lose their boundaries and the common cytoplasm passes into the oocyte, carrying with it the free nuclei to their engulfment and absorption in the ooplasm. 5. Some of the follicle-cells surrounding the last oocyte in Pristiphora padi, and the fifth, sixth, and seventh of Thrinax mixta, contain granular dark-staining material which may completely fill the cell, these granules probably originating from the nucleus. They pass out of the follicle-cell into the egg where they become surrounded by vesicles, and, finally, present an appearance indistinguishable from that of accessory nuclei. 6. Secondary or accessory nuclei, therefore, have a threefold origin, namely, from the nuclei, of nurse-cells and oocytes and from follicle-cells, their source of derivation in the last being the follicular nuclei. 7. The follicle-cells of the distal pole of the last oocyte of one ovariole of Pristiphora padi have processes which insinuate themselves into the ooplasm. 8. The phenomena of oogenesis described in these four species of sawflies, while embracing certain which have not hitherto been recorded, conform, in essentials, with those already discovered for Hymenoptera generally.


2016 ◽  
Vol 113 (9) ◽  
pp. E1246-E1255 ◽  
Author(s):  
Allison K. Timmons ◽  
Albert A. Mondragon ◽  
Claire E. Schenkel ◽  
Alla Yalonetskaya ◽  
Jeffrey D. Taylor ◽  
...  

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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