Studies on the Ovarian Follicle Cells of Drosophila

1963 ◽  
Vol s3-104 (67) ◽  
pp. 297-320
Author(s):  
R. C. KING ◽  
ELIZABETH A. KOCH
Keyword(s):  
Ovarian Follicle ◽  
Protein A ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Vitelline Membrane ◽  
Membrane Material ◽  
Adjacent Layer ◽  
Membrane Formation ◽  
Precursor Material ◽  
Egg Shell

Studies are described of the ultrastructure of the follicle cells which invest the oocyte of Drosophila melanogaster at the time of vitelline membrane formation. Of particular interest are organelles made up of endoplasmic reticulum organized into a husk of concentric lamellae which surround lipidal droplets. These epithelial bodies are seen only at the time the vitelline membrane is being formed, and it is assumed therefore that the lipidal material of the epithelial body may be utilized somehow in the fabrication of the vitelline membrane. Cytochemical studies have shown this membrane to contain at least 5 classes of compounds; a protein, two lipids (which may be distinguished by differences in their resistance to extraction by various solvents), and 2 polysaccharides (1 neutral and 1 acidic). Studies were made of vitelline membrane formation in the ovaries of flies homozygous for either of 2 recessive, female-sterile genes (tiny and female sterile). In the case of the ty mutation vitelline membrane material is sometimes secreted between follicle and nurse cells, while in the mutant fes vitelline membrane is observed in rare instances to be secreted between follicle cells and an adjacent layer of tumour cells. In the latter case the vitelline membrane shows altered cytochemical properties. The fact that vitelline membrane can be secreted by follicle cells not adjacent to an oocyte demonstrates that it is the follicle cell rather than the oocyte that plays the major role in the secretion of the precursor material of the vitelline membrane. Subsequently the follicle cells secrete the egg-shell, or chorion, which is subdivided into a dense, compartmented, inner endochorion, and a pale, outer exochorion. A description is given of the ultrastructure of the follicle cells during the secretion of the endochorion and the exochorion. The endochorion contains a protein, a polysaccharide, and a lipid, all of which may be distinguished cytochemically from the vitelline membrane compounds. The exochorion contains large amounts of acidic mucopolysaccharides. Specialized follicle cells form the micropylar apparatus and the chorionic appendages. The formation of the chorion and chorionic appendages is discussed in the light of information gained from abnormalities of the chorions and chorionic appendages seen in ty and fs 2.1 oocytes. Subsequent to the time the egg leaves the ovariole a layer of waterproofing wax is secreted between the vitelline membrane and the chorion.

Specific domains drive VM32E protein distribution and integration in Drosophila eggshell layers

2001 ◽  
Vol 114 (15) ◽  
pp. 2819-2829 ◽  
Author(s):  
Davide Andrenacci ◽  
Filippo M. Cernilogar ◽  
Carlo Taddei ◽  
Deborah Rotoli ◽  
Valeria Cavaliere ◽  
...  
Keyword(s):  
Protein A ◽  
The Other ◽  
Follicle Cells ◽  
Vitelline Membrane ◽  
Cross Linking ◽  
Protein Distribution ◽  
Membrane Domain ◽  
Membrane Component ◽  
Synthesis Stage ◽  
Transgenic Flies

A study was made of the localization and assembly of the VM32E protein, a putative vitelline membrane component of the Drosophila eggshell. The results highlight some unique features of this protein compared with the other proteins of the same gene family. At the time of its synthesis (stage 10), the VM32E protein is not detectable in polar follicle cells. However, it is able to move in the extracellular space around the oocyte and, by stage 11 is uniformly distributed in the vitelline membrane. During the terminal stages of oogenesis the VM32E protein is partially released from the vitelline membrane and becomes localized in the endochorion layer also. By analyzing transgenic flies carrying variously truncated VM32E proteins, we could identify the protein domains required for the proper assembly of the VM32E protein in the eggshell. The highly conserved vitelline membrane domain is implicated in the early interactions with other components and is required for cross-linking VM32E protein in the vitelline membrane. The terminal carboxylic domain is necessary for localization to the endochorion layer. Protein with the C-end domain deleted is localized solely to the vitelline membrane and cross-linked only in laid eggs, as occurs for the other vitelline membrane proteins.

scholarly journals Establishment of dorsal-ventral polarity of theDrosophilaegg requirescapicuaaction in ovarian follicle cells

Development ◽  
2001 ◽  
Vol 128 (22) ◽  
pp. 4553-4562 ◽  
Author(s):  
Deborah J. Goff ◽  
Laura A. Nilson ◽  
Donald Morisato
Keyword(s):  
Target Genes ◽  
Nuclear Translocation ◽  
Ovarian Follicle ◽  
Growth Factor Receptor ◽  
Follicle Cell ◽  
Dorsal Side ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Egfr Signaling ◽  
Cell Nuclei

The dorsal-ventral pattern of the Drosophila egg is established during oogenesis. Epidermal growth factor receptor (Egfr) signaling within the follicular epithelium is spatially regulated by the dorsally restricted distribution of its presumptive ligand, Gurken. As a consequence, pipe is transcribed in a broad ventral domain to initiate the Toll signaling pathway in the embryo, resulting in a gradient of Dorsal nuclear translocation. We show that expression of pipe RNA requires the action of fettucine (fet) in ovarian follicle cells. Loss of maternal fet activity produces a dorsalized eggshell and embryo. Although similar mutant phenotypes are observed with regulators of Egfr signaling, genetic analysis suggests that fet acts downstream of this event. The fet mutant phenotype is rescued by a transgene of capicua (cic), which encodes an HMG-box transcription factor. We show that Cic protein is initially expressed uniformly in ovarian follicle cell nuclei, and is subsequently downregulated on the dorsal side. Earlier studies described a requirement for cic in repressing zygotic target genes of both the torso and Toll pathways in the embryo. Our experiments reveal that cic controls dorsal-ventral patterning by regulating pipe expression in ovarian follicle cells, before its previously described role in interpreting the Dorsal gradient.

scholarly journals The Formation and Structure of the Micropylar Complex in the Egg-Shell of Rhodnius Prolixus Stähl. (Heteroptera Reduviidae)

1947 ◽  
Vol 23 (3-4) ◽  
pp. 213-233 ◽  
Author(s):  
J. W. L. BEAMENT
Keyword(s):  
Follicle Cell ◽  
Rhodnius Prolixus ◽  
Follicle Cells ◽  
Normal Order ◽  
Protein Layer ◽  
Complex Region ◽  
Phase Cycle ◽  
Secretory Products ◽  
Egg Shell ◽  
Pore Canals

An investigation has been made of the junction between the shell and cap in the egg-shell of Rhodnius prolixus. This complex region consists of the thickened rim of the cap connected by a thin sealing bar to the rim of the shell. The secretion of this part of the shell has been followed and compared with the formation of less specialized portions of the shell. The shell has been divided into units, each the product of an individual follicle cell. It has been found that all the seven layers which make up the unspecialized parts of the shell are present in the seal complex; that these consist of five endochorion layers and two exochorion layers in their normal order. The exochorion is secreted around long villi, one from each follicle cell. These give rise to follicular pits in the shell. In this complex region, cells start to secrete at various stages in the seven-phase cycle; their initial secretion is apparently related to the material with which they make contact at that time. After secretion has started, each cell completes the remainder of the cycle. The rim of the cap is the product of four rings of follicle cells; the additional thickness is achieved by an increase in the exochorion layers, secreted around a series of very long follicular pits. The sealing bar, which is produced by one ring of follicle cells, is composed of the inner four layers of the chorion only; the cells do not produce soft endochorion, or exochorion layers. At the cap end of the sealing bar there is the predetermined hatching line. It is apparently produced by the presence in the follicle of cells which are inactive during the secretion of the inner layers, and so prevent co-ordination between the active cells on either side. A weak point is also present at the base of the sealing bar, at the site of other inactive cells, though this fissure is not used at hatching. The rim of the shell is similarly produced by an expansion of the exochorion layers secreted around four rings of follicular villi. Of these, three rings of pits are filled in towards the end of secretion, but the fourth, lying on the upper portion of the rim, remains. These pits become the micropyles and associated structures. There are 200 pits in the completed rim, divided into two groups. About fifteen are micropyles; the remainder are cavities closed at each end, and to which the name ‘pseudomicropyle’ has been given. The pseudomicropyles are formed in a similar way to normal follicular pits, but start in the resistant protein layer, 0.5µ from the inside of the shell. They end in the resistant exochorion, where they are connected to the external surface by small bunches of pore canals. They probably play some part in the respiration of the embryo. The true micropyles form the only free path through the shell. The inner portion of each tube is lined with hydrophilic protein, and the outer portion, which lies slightly posterior to the pseudomicropyles, is composed of hydrophobic lipoprotein. The number of true micropyles is not constant, there being between ten and twenty scattered irregularly around the rim. However, eggs produced by older females contain fewer micropyles; this may account for a higher rate of sterility among these eggs. The cells which form the micropyles and pseudomicropyles are the only ones which do not adhere to the typical cycle of seven secretory products. But in omitting three phases, the attachment of the exochorion to a protein layer is retained. Evidence suggests that the cells forming the micropyles are determined in the earliest stages of secretion by being squeezed out of the pseudomicropylar ring of cells.

scholarly journals Drosophila insulin-like peptide 8 (DILP8) in ovarian follicle cells regulates ovulation and metabolism

2020 ◽  
Author(s):  
Sifang Liao ◽  
Dick R. Nässel
Keyword(s):  
Adult Female ◽  
Developmental Stages ◽  
Ovarian Follicle ◽  
Expression Patterns ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Ovary Development ◽  
Peripheral Neurons ◽  
Efferent Neurons

AbstractIn Drosophila eight insulin-like peptides (DILP1-8) are encoded on separate genes. These DILPs are characterized by unique spatial and temporal expression patterns during the lifecycle. Whereas functions of several of the DILPs have been extensively investigated at different developmental stages, the role of DILP8 signaling is primarily known from larvae and pupae where it couples organ growth and developmental transitions. In adult female flies, a study showed that a specific set of neurons that express the DILP8 receptor, Lgr3, is involved in regulation of reproductive behavior. Here, we further investigated the expression of dilp8/DILP8 and Lgr3 in adult female flies and the functional role of DILP8 signaling. The only site where we found both dilp8 expression and DILP8 immunolabeling was in follicle cells of mature ovaries. Lgr3 expression was detected in numerous neurons in the brain and ventral nerve cord, a small set of peripheral neurons innervating the abdominal heart, as well as in a set of follicle cells close to the oviduct. Ovulation was affected in dilp8 mutants as well as after dilp8-RNAi using dilp8 and follicle cell Gal4 drivers. More eggs were retained in the ovaries and fewer were laid, indicating that DILP8 is important for ovulation. Our data suggest that DILP8 signals locally to Lgr3 expressing follicle cells as well as systemically to Lgr3 expressing efferent neurons in abdominal ganglia that innervate oviduct muscle. Thus, DILP8 may act at two targets to regulate ovulation: follicle cell rupture and oviduct contractions. Furthermore, we could show that manipulations of dilp8 expression affect food intake and starvation resistance. Possibly this reflects a feedback signaling between ovaries and the CNS that ensures nutrients for ovary development. In summary, it seems that DILP8 signaling in regulation of reproduction is an ancient function, conserved in relaxin signaling in mammals.

Protein Synthesis and Uptake by Isolated Cecropia Oocytes

1971 ◽  
Vol 8 (3) ◽  
pp. 735-750
Author(s):  
LUCY M. ANDERSON
Keyword(s):  
Amino Acids ◽  
Amino Acid ◽  
Perchloric Acid ◽  
Selection Process ◽  
Ovarian Follicle ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Blood Proteins ◽  
Cell Product

A procedure has been developed for separating the oocytes and follicular epithelium-nurse cell complexes making up the vitellogenic ovarian follicle of the Cecropia moth. Both components remained viable during short-term in vitro incubation in female blood. Isolated epithelial cells were found by autoradiography to incorporate tritiated amino acids and to secrete a fixable, non-dialysable labelled material. Isolated oocytes incubated in a blood medium containing this tritiated, dialysed follicle cell product incorporated it in small cortical yolk bodies, presumably by pinocytosis. Quantitative perchloric acid-precipitation and scintillation counting indicated that the amount of labelled material incorporated by the oocytes increased with time. These results provide direct confirmation of a follicle contribution to the yolk. Isolated oocytes were also tested for their ability to incorporate labelled amino acids. Fixable label was observed autoradiographically throughout the oocyte cytoplasm, with the greatest concentration in the cortex, but little appeared in the yolk spheres. The amount of perchloric acid-precipitable amino acid in oocytes incubated in female blood increased with time for up to 2 h and then remained constant or decreased slightly. In medium that had been previously conditioned by follicle cells and dialysed, however, incorporation of labelled amino acid continued for at least 4 h. A possible interpretation of this result is that stimulation of pinocytosis by the epithelial cell products causes increased turnover of cell membrane and demands continued synthesis of new proteins. Labelled female blood proteins were not incorporated into yolk to an appreciable extent by isolated oocytes, even in the presence of follicle cell product. Perhaps extracellular preconcentration, as occurs in the intact follicle, is necessary for effective accrual of blood proteins. The female blood proteins did become associated with the oocyte cortex, however, and exhibited a higher affinity for the oocyte than male blood proteins. Thus preferential adsorption to the oocyte surface may be a component of the selection process in vitellogenesis.

Drosophila bunched integrates opposing DPP and EGF signals to set the operculum boundary

Development ◽  
2000 ◽  
Vol 127 (4) ◽  
pp. 745-754 ◽  
Author(s):  
L.L. Dobens ◽  
J.S. Peterson ◽  
J. Treisman ◽  
L.A. Raftery
Keyword(s):  
Cell Fate ◽  
Egf Receptor ◽  
Ovarian Follicle ◽  
Ectopic Expression ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Sharp Boundary ◽  
Smad Protein ◽  
Multiple Cell ◽  
Egf Signaling

The Drosophila BMP homolog DPP can function as a morphogen, inducing multiple cell fates across a developmental field. However, it is unknown how graded levels of extracellular DPP are interpreted to organize a sharp boundary between different fates. Here we show that opposing DPP and EGF signals set the boundary for an ovarian follicle cell fate. First, DPP regulates gene expression in the follicle cells that will create the operculum of the eggshell. DPP induces expression of the enhancer trap reporter A359 and represses expression of bunched, which encodes a protein similar to the mammalian transcription factor TSC-22. Second, DPP signaling indirectly regulates A359 expression in these cells by downregulating expression of bunched. Reduced bunched function restores A359 expression in cells that lack the Smad protein MAD; ectopic expression of BUNCHED suppresses A359 expression in this region. Importantly, reduction of bunched function leads to an expansion of the operculum and loss of the collar at its boundary. Third, EGF signaling upregulates expression of bunched. We previously demonstrated that the bunched expression pattern requires the EGF receptor ligand GURKEN. Here we show that activated EGF receptor is sufficient to induce ectopic bunched expression. Thus, the balance of DPP and EGF signals sets the boundary of bunched expression. We propose that the juxtaposition of cells with high and low BUNCHED activity organizes a sharp boundary for the operculum fate.

Characterization and sequence of follicle cell genes selectively expressed during vitelline membrane formation in Drosophila

1987 ◽  
Vol 124 (2) ◽  
pp. 441-450 ◽  
Author(s):  
Thomas Burke ◽  
Gail L. Waring ◽  
Ellen Popodi ◽  
Parviz Minoo
Keyword(s):  
Follicle Cell ◽  
Vitelline Membrane ◽  
Membrane Formation

scholarly journals Transcriptional Repressor Functions of Drosophila E2F1 and E2F2 Cooperate To Inhibit Genomic DNA Synthesis in Ovarian Follicle Cells

2003 ◽  
Vol 23 (6) ◽  
pp. 2123-2134 ◽  
Author(s):  
Pelin Cayirlioglu ◽  
William O. Ward ◽  
S. Catherine Silver Key ◽  
Robert J. Duronio
Keyword(s):  
Gene Expression ◽  
Cell Cycle ◽  
Dna Synthesis ◽  
Gene Amplification ◽  
Cell Cycle Progression ◽  
Ovarian Follicle ◽  
Cell Cycle Control ◽  
Control Cell ◽  
Follicle Cell ◽  
Follicle Cells

ABSTRACT Individual members of the E2F/DP protein family control cell cycle progression by acting predominantly as an activator or repressor of transcription. In Drosophila melanogaster the E2f1, E2f2, Dp, and Rbf1 genes all contribute to replication control in ovarian follicle cells, which become 16C polyploid and subsequently undergo chorion gene amplification late in oogenesis. Mutation of E2f2, Dp, or Rbf1 causes ectopic DNA replication throughout the follicle cell genome during gene amplification cycles. Here we show by both reverse transcription-PCR and DNA microarray analysis that the transcripts of prereplication complex (pre-RC) genes are elevated compared to the wild type in E2f2, Dp, and Rbf1 mutant follicle cells. For some genes the magnitude of this transcriptional derepression is greater in Rbf1 than in E2f2 mutants. These differences correlate with differences in the magnitude of the replication defects in follicle cells, which attain an inappropriate 32C DNA content in both Rbf1 and Dp mutants but not in E2f2 mutants. The ectopic genomic replication of E2f2 mutant follicle cells can be suppressed by reducing the Orc2, Orc5, or Mcm2 gene dose by half, indicating that small changes in pre-RC gene expression can affect DNA synthesis in these cells. We conclude that RBF1 forms complexes with both E2F1/DP and E2F2/DP that cooperate to repress the expression of pre-RC genes, which helps confine DNA synthesis to sites of gene amplification. In contrast, E2F1 and E2F2 repressors function redundantly for some genes in the embryo. Thus, the relative functional contributions of E2F1 and E2F2 to gene expression and cell cycle control depends on the developmental context.

scholarly journals fs (1) Yb is required for ovary follicle cell differentiation in Drosophila melanogaster and has genetic interactions with the Notch group of neurogenic genes.

Genetics ◽  
1995 ◽  
Vol 140 (1) ◽  
pp. 207-217 ◽  
Author(s):  
E Johnson ◽  
S Wayne ◽  
R Nagoshi
Keyword(s):  
Cell Fate ◽  
Ovarian Follicle ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Female Sterility ◽  
Specific Factor ◽  
Temperature Sensitive ◽  
Egg Maturation ◽  
Egg Chambers ◽  
Mutant Phenotypes

Abstract Phenotypic and genetic analyses demonstrate that fs (1) Yb activity is required in the soma for the development of a subset of ovarian follicle cells and to support later stages of egg maturation. Mutations in fs (1) Yb cause a range of ovarian phenotypes, from the improper segregation of egg chambers to abnormal dorsal appendage formation. The mutant phenotypes associated with fs (1) Yb are very similar to the ovarian aberrations produced by temperature-sensitive alleles of Notch and Delta. Possible functional or regulatory interactions between fs (1) Yb and Notch are suggested by genetic studies. A duplication of the Notch locus partially suppresses the female-sterility caused by fs (1) Yb mutations, while reducing Notch dosage makes the fs (1) Yb mutant phenotype more severe. In addition, fs (1) Yb alleles also interact with genes that are known to act with or regulate Notch activity, including Delta, daughterless, and mastermind. However, differences between the mutant ovarian phenotype of fs (1) Yb and that of Notch or Delta indicate that the genes do not have completely overlapping functions in the ovary. We propose that fs (1) Yb acts as an ovary-specific factor that determines follicle cell fate.

The neurogenic locus brainiac cooperates with the Drosophila EGF receptor to establish the ovarian follicle and to determine its dorsal-ventral polarity

Development ◽  
1992 ◽  
Vol 116 (1) ◽  
pp. 177-192 ◽  
Author(s):  
S. Goode ◽  
D. Wright ◽  
A.P. Mahowald
Keyword(s):  
Nurse Cell ◽  
Egf Receptor ◽  
Ovarian Follicle ◽  
Follicle Cell ◽  
Cell Complex ◽  
Follicle Cells ◽  
Sensitive Period ◽  
Cell Fates ◽  
Genetic Mosaic

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.

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