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.

Sequential activation of the EGF receptor pathway during Drosophila oogenesis establishes the dorsoventral axis

Development ◽  
1998 ◽  
Vol 125 (2) ◽  
pp. 191-200 ◽  
Author(s):  
A. Sapir ◽  
R. Schweitzer ◽  
B.Z. Shilo
Keyword(s):  
Target Genes ◽  
Egf Receptor ◽  
Ectopic Expression ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Cell Fates ◽  
Dorsoventral Axis ◽  
Spatial Coordinates ◽  
Sequential Activation

Previous work has demonstrated a role for the Drosophila EGF receptor (Torpedo/DER) and its ligand, Gurken, in the determination of anterioposterior and dorsoventral axes of the follicle cells and oocyte. The roles of DER in establishing the polarity of the follicle cells were examined further, by following the expression of DER-target genes. One class of genes (e.g. kekon) is induced by the DER pathway at all stages. Broad expression of kekon at the stage in which the follicle cells migrate posteriorly over the oocyte, demonstrates the capacity of the pathway to pattern all follicle cells except the ventral-most rows. This may provide the spatial coordinates for the ventral-most follicle cell fates. A second group of target genes (e.g. rhomboid (rho)) is induced only at later stages of oogenesis, and may require additional inputs by signals emanating from the anterior, stretch follicle cells. The function of Rho was analyzed by ectopic expression in the stretch follicle cells, and shown to induce a non-autonomous dorsalizing activity that is independent of Gurken. Rho thus appears to be involved in processing a DER ligand in the follicle cells, to pattern the egg chamber and allow persistent activation of the DER pathway during formation of the dorsal appendages.

Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila

Development ◽  
1999 ◽  
Vol 126 (11) ◽  
pp. 2515-2525 ◽  
Author(s):  
S. Kramer ◽  
M. Okabe ◽  
N. Hacohen ◽  
M.A. Krasnow ◽  
Y. Hiromi
Keyword(s):  
Signaling Pathways ◽  
Intracellular Signaling ◽  
Cellular Proliferation ◽  
Egf Receptor ◽  
Ovarian Follicle ◽  
Follicle Cells ◽  
Chordotonal Organ ◽  
Fgf Signaling ◽  
Tracheal System ◽  
Egf Signaling

Extracellular factors such as FGF and EGF control various aspects of morphogenesis, patterning and cellular proliferation in both invertebrates and vertebrates. In most systems, it is primarily the distribution of these factors that controls the differential behavior of the responding cells. Here we describe the role of Sprouty in eye development. Sprouty is an extracellular protein that has been shown to antagonize FGF signaling during tracheal branching in Drosophila. It is a novel type of protein with a highly conserved cysteine-rich region. In addition to the embryonic tracheal system, sprouty is also expressed in other tissues including the developing eye imaginal disc, embryonic chordotonal organ precursors and the midline glia. In each of these tissues, EGF receptor signaling is known to participate in the control of the correct number of neurons or glia. We show that, in all three tissues, the loss of sprouty results in supernumerary neurons or glia, respectively. Furthermore, overexpression of sprouty in wing veins and ovarian follicle cells, two other tissues where EGF signaling is required for patterning, results in phenotypes that resemble the loss-of-function phenotypes of Egf receptor. These results suggest that Sprouty acts as an antagonist of EGF as well as FGF signaling pathways. These receptor tyrosine kinase-mediated pathways may share not only intracellular signaling components but also extracellular factors that modulate the strength of the signal.

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.

Mosaic Analysis in the Drosophila Ovary Reveals a Common Hedgehog-Inducible Precursor Stage for Stalk and Polar Cells

Genetics ◽  
1999 ◽  
Vol 151 (2) ◽  
pp. 739-748 ◽  
Author(s):  
Michael Tworoger ◽  
Michele Keller Larkin ◽  
Zev Bryant ◽  
Hannele Ruohola-Baker
Keyword(s):  
Cell Fate ◽  
Ovarian Follicle ◽  
Ectopic Expression ◽  
Cell Formation ◽  
Follicle Cells ◽  
Stalk Cell ◽  
Polar Cell ◽  
Drosophila Ovary ◽  
Anterior Posterior

Abstract The fates of two small subgroups of the ovarian follicle cells appear to be linked: mutations in Notch, Delta, fs(1)Yb, or hedgehog cause simultaneous defects in the specification of stalk cells and polar cells. Both of these subgroups are determined in the germarium, and both cease division early in oogenesis. To test the possibility that these subgroups are related by lineage, we generated dominantly marked mitotic clones in ovaries. Small, restricted clones in stalk cells and polar cells were found adjacent to each other at a frequency much too high to be explained by independent induction. We therefore propose a model in which stalk cells and polar cells are derived from a precursor population that is distinct from the precursors for other follicle cells. We support and extend this model by characterization of mutants that affect stalk and polar cell formation. We find that ectopic expression of Hedgehog can induce both polar and stalk cell fate, presumably by acting on the precursor stage. In contrast, we find that stall affects neither the induction of the precursors nor the decision between the stalk cell and polar cell fate but, rather, some later differentiation step of stalk cells. In addition, we show that ectopic polar and stalk cells disturb the anterior-posterior polarity of the underlying oocyte.

Pointed, an ETS domain transcription factor, negatively regulates the EGF receptor pathway in Drosophila oogenesis

Development ◽  
1996 ◽  
Vol 122 (12) ◽  
pp. 3745-3754 ◽  
Author(s):  
A.M. Morimoto ◽  
K.C. Jordan ◽  
K. Tietze ◽  
J.S. Britton ◽  
E.M. O'Neill ◽  
...  
Keyword(s):  
Transcription Factor ◽  
Cell Fate ◽  
Egf Receptor ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Dorsal Region ◽  
Epidermal Growth ◽  
Ets Domain ◽  
Ets Transcription Factor ◽  
Midline Cells

Spatially regulated activation of the Drosophila epidermal growth factor (EGF) receptor by its ligand, Gurken, is required for establishment of the dorsal/ventral axis of the oocyte and embryo. During mid-oogenesis, Gurken is concentrated at the dorsal-anterior of the oocyte and is thought to activate the EGF receptor pathway in adjacent follicle cells. In response to this signal, dorsal follicle cell fate is determined. These cells further differentiate into either appendage-producing or midline cells, resulting in patterning in the dorsal follicle cell layer. We show here that Pointed, an ETS transcription factor, is required in dorsal follicle cells for this patterning. Loss of pointed results in the loss of midline cells and an excess of appendage-forming cells, a phenotype associated with overactivation of the EGF receptor pathway in the dorsal region. Overexpression of pointed leads to a phenotype similar to that generated by loss of the EGF receptor pathway. This suggests that Pointed normally down-regulates EGF receptor signaling in the midline to generate patterning in the dorsal region. Interestingly, pointed expression is induced by the EGF receptor pathway. These data indicate a novel antagonistic function for Pointed in oogenesis; in response to activation of the EGF receptor, pointed is expressed and negatively regulates the EGF receptor pathway, possibly by integrating information from a second pathway.

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.

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 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.

scholarly journals Expression of fringe is down regulated by Gurken/Epidermal Growth Factor Receptor signalling and is required for the morphogenesis of ovarian follicle cells

2000 ◽  
Vol 113 (21) ◽  
pp. 3781-3794 ◽  
Author(s):  
D. Zhao ◽  
D. Clyde ◽  
M. Bownes
Keyword(s):  
Epidermal Growth Factor Receptor ◽  
Growth Factor ◽  
Epidermal Growth Factor ◽  
Cell Fate ◽  
Ovarian Follicle ◽  
Growth Factor Receptor ◽  
Signal Transduction Pathway ◽  
Follicle Cells ◽  
Egg Chambers ◽  
Epidermal Growth

Signalling by the Gurken/Epidermal Growth Factor Receptor (Grk/EGFR) pathway is involved in epithelial cell fate decision, morphogenesis and axis establishment in Drosophila oogenesis. In the search for genes downstream of the Grk/EGFR signal transduction pathway (STP), we isolated a number of genes that are components of other STPs. One of them is a known gene, called fringe (fng). Drosophila fng encodes a putative secreted protein that is required at other development stages for mediating interactions between dorsal and ventral cells via Notch signalling. Here we show that fng has a dynamic expression pattern in oogenesis and that its expression in specific groups of follicle cells along the anterior-posterior and dorsal-ventral axes is defined by the repression of fng by Grk. Interfering with fng expression using antisense RNA experiments resulted in a typical fng mutant phenotype in the wing, and malformed egg chambers and abnormal organisation of the follicle cells in the ovaries, revealing that fng is essential in oogenesis for the proper formation of the egg chamber and for epithelial morphogenesis. This has been confirmed by re-examination of fng mutants and analysis of fng mutant clones in oogenesis.

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