Memoirs: The Rôles of the Nurse-cells, Oocytes and Follicle-cells in Tenthredinid Oogenesis

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.

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.


Development ◽  
1997 ◽  
Vol 124 (22) ◽  
pp. 4661-4671 ◽  
Author(s):  
N.J. Clegg ◽  
D.M. Frost ◽  
M.K. Larkin ◽  
L. Subrahmanyan ◽  
Z. Bryant ◽  
...  

We describe a mutant, maelstrom, that disrupts a previously unobserved step in mRNA localization within the early oocyte, distinct from nurse-cell-to-oocyte RNA transport. Mutations in maelstrom disturb the localization of mRNAs for Gurken (a ligand for the Drosophila Egf receptor), Oskar and Bicoid at the posterior of the developing (stage 3–6) oocyte. maelstrom mutants display phenotypes detected in gurken loss-of-function mutants: posterior follicle cells with anterior cell fates, bicoid mRNA localization at both poles of the stage 8 oocyte and ventralization of the eggshell. These data are consistent with the suggestion that early posterior localization of gurken mRNA is essential for activation of the Egf receptor pathway in posterior follicle cells. Posterior localization of mRNA in stage 3–6 oocytes could therefore be one of the earliest known steps in the establishment of oocyte polarity. The maelstrom gene encodes a novel protein that has a punctate distribution in the cytoplasm of the nurse cells and the oocyte until the protein disappears in stage 7 of oogenesis.


1999 ◽  
Vol 112 (21) ◽  
pp. 3677-3690 ◽  
Author(s):  
W. Deng ◽  
K. Leaper ◽  
M. Bownes

We report that Drosophila unconventional myosin VI, encoded by Myosin heavy chain at 95F (Mhc95F), is required for both imaginal disc and egg chamber morphogenesis. During oogenesis, Mhc95F is expressed in migrating follicle cells, including the border cells, which migrate between the nurse cells to lie at the anterior of the oocyte; the columnar cells that migrate over the oocyte; the centripetal cells that migrate between the oocyte and nurse cells; and the dorsal-anterior follicle cells, which migrate to secrete the chorionic appendages. Its function during development has been studied using a targeted gene silencing technique, combining the Gal4-UAS targeted expression system and the antisense RNA technique. Antibody staining shows that the expression of myosin 95F is greatly decreased in follicle cells when antisense Mhc95F RNA is expressed. Interfering with expression of Drosophila myosin VI at various developmental stages frequently results in lethality. During metamorphosis it results in adult flies with malformed legs and wings, indicating that myosin VI is essential for imaginal disc morphogenesis. During oogenesis, abnormal follicle cell shapes and aberrant follicle cell migrations are observed when antisense Mhc95F is expressed in follicle cells during stages 9 to 10, suggesting that the Drosophila myosin VI is required for follicle cell epithelial morphogenesis.


Development ◽  
2001 ◽  
Vol 128 (10) ◽  
pp. 1845-1856 ◽  
Author(s):  
L.L. Dobens ◽  
E. Martin-Blanco ◽  
A. Martinez-Arias ◽  
F.C. Kafatos ◽  
L.A. Raftery

puckered (puc) encodes a VH1-like phosphatase that down-regulates Jun kinase (JNK) activity during dorsal closure of the Drosophila embryo. We report a role for puc in follicle cell morphogenesis during oogenesis. puc mRNA accumulates preferentially in the centripetally migrating follicle cells and cells of the elongating dorsal appendages. Proper levels of Puc activity in the follicle cells are critical for the production of a normal egg: either reduced or increased Puc activity result in incomplete nurse cell dumping and aberrant dorsal appendages. Phenotypes associated with puc mutant follicle cells include altered DE-cadherin expression in the follicle cells and a failure of nurse cell dumping to coordinate with dorsal appendage elongation, leading to the formation of cup-shaped egg chambers. The JNK pathway target A251-lacZ showed cell-type-specific differences in its regulation by puc and by the small GTPase DRac1. puc mutant cells displayed region-specific ectopic expression of the A251-lacZ enhancer trap whereas overexpression of a transgene encoding Puc was sufficient to suppress lacZ expression in a cell autonomous fashion. Strikingly, decreased or increased puc function leads to a corresponding increase or decrease, respectively, of Fos and Jun protein levels. Taken together, these data indicate that puc modulates gene expression responses by antagonizing a Ρ GTPase signal transduction pathway that stabilizes the AP-1 transcription factor. Consistent with this, overexpression of a dominant negative DRac1 resulted in lower levels of Fos/Jun.


Development ◽  
1992 ◽  
Vol 116 (1) ◽  
pp. 177-192 ◽  
Author(s):  
S. Goode ◽  
D. Wright ◽  
A.P. Mahowald

We have characterized the function of a new neurogenic locus, brainiac (brn), during oogenesis. Homozygous brn females lay eggs with fused dorsal appendages, a phenotype associated with torpedo (top) alleles of the Drosophila EGF receptor (DER) locus. By constructing double mutant females for both brn and top, we have found that brn is required for determining the dorsal-ventral polarity of the ovarian follicle. However, embryos from mature brn eggs develop a neurogenic phenotype which can be zygotically rescued if a wild-type sperm fertilizes the egg. This is the first instance of a Drosophila gene required for determination of dorsal-ventral follicle cell fates that is not required for determination of embryonic dorsal-ventral cell fates. The temperature-sensitive period for brn dorsal-ventral patterning begins at the inception of vitellogenesis. The interaction between brn and DER is also required for at least two earlier follicle cell activities which are necessary to establish the ovarian follicle. Prefollicular cells fail to migrate between each oocyte/nurse cell complex, resulting in follicles with multiple sets of oocytes and nurse cells. brn and DER function is also required for establishing and/or maintaining a continuous follicular epithelium around each oocyte/nurse cell complex. These brn functions as well as the brn requirement for determination of dorsal-ventral polarity appear to be genetically separable functions of the brn locus. Genetic mosaic experiments show that brn is required in the germline during these processes whereas the DER is required in the follicle cells. We propose that brn may be part of a germline signaling pathway differentially regulating successive DER-dependent follicle cell activities of migration, division and/or adhesion and determination during oogenesis. These experiments indicate that brn is required in both tyrosine kinase and neurogenic intercellular signaling pathways. Moreover, the functions of brn in oogenesis are distinct from those of Notch and Delta, two other neurogenic loci that are known to be required for follicular development.


1970 ◽  
Vol 45 (2) ◽  
pp. 306-320 ◽  
Author(s):  
Anthony P. Mahowald ◽  
Joan M. Strassheim

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.


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.


1978 ◽  
Vol 31 (1) ◽  
pp. 137-143
Author(s):  
A. Fiil

In the mosquito, Culex pipiens quinqefasciatus, the follicle cells enveloping the oocyte and the nurse cells are connected by intercellular bridges. The bridges are formed by incomplete cytokinesis, and they persist for more than 30 h after their formation. Reconstructions from serial sections showed that one syncytial group contained at least 32 cells; several cells continued outside the series. The cells in a syncytium divide asynchronously; this results in an irregular, branched orgainzation. The bridges may be either embedded in the cytoplasm of the cells, or they may form an extracellular connexion.


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.


1986 ◽  
Vol 80 (1) ◽  
pp. 159-169 ◽  
Author(s):  
H.O. Gutzeit

During the last phase of oogenesis in Drosophila, nurse cell cytoplasm can be seen to be streaming into the growing oocyte when visualized in time-lapse films. This process can be reversibly inhibited by cytochalasins. The distribution of F-actin filaments in the nurse cells has been studied by staining with rhodamine-conjugated phalloidin. At the beginning of cytoplasmic streaming (stage 10B) increasingly thick bundles of microfilaments formed, many of which spanned the nurse cell cytoplasm from the cell membrane to the nuclear membrane. The association of F-actin with the nuclear membrane persisted when nurse cell nuclei were isolated mechanically. The experimental evidence suggests that microfilament contraction in the nurse cells leads to cytoplasmic streaming by pressure flow.


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