Combined activities of Gurken and decapentaplegic specify dorsal chorion structures of the Drosophila egg

Development ◽  
2000 ◽  
Vol 127 (4) ◽  
pp. 841-850 ◽  
Author(s):  
F. Peri ◽  
S. Roth
Keyword(s):  
Egf Receptor ◽  
Receptor Activation ◽  
Posterior Pole ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Oocyte Nucleus ◽  
Main Body ◽  
Dorsal Appendage ◽  
Broad Complex ◽  
Anterior Posterior

During Drosophila oogenesis Gurken, associated with the oocyte nucleus, activates the Drosophila EGF receptor in the follicular epithelium. Gurken first specifies posterior follicle cells, which in turn signal back to the oocyte to induce the migration of the oocyte nucleus from a posterior to an anterior-dorsal position. Here, Gurken signals again to specify dorsal follicle cells, which give rise to dorsal chorion structures including the dorsal appendages. If Gurken signaling is delayed and starts after stage 6 of oogenesis the nucleus remains at the posterior pole of the oocyte. Eggs develop with a posterior ring of dorsal appendage material that is produced by main-body follicle cells expressing the gene Broad-Complex. They encircle terminal follicle cells expressing variable amounts of the TGFbeta homologue, decapentaplegic. By ectopically expressing decapentaplegic and clonal analysis with Mothers against dpp we show that Decapentaplegic signaling is required for Broad-Complex expression. Thus, the specification and positioning of dorsal appendages along the anterior-posterior axis depends on the intersection of both Gurken and Decapentaplegic signaling. This intersection also induces rhomboid expression and thereby initiates the positive feedback loop of EGF receptor activation, which positions the dorsal appendages along the dorsal-ventral egg axis.

scholarly journals The origin of dorsoventral polarity in Drosophila

2003 ◽  
Vol 358 (1436) ◽  
pp. 1317-1329 ◽  
Author(s):  
Siegfried Roth
Keyword(s):  
Concentration Gradient ◽  
Messenger Rna ◽  
Egf Receptor ◽  
Transforming Growth Factor ◽  
Receptor Activation ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Oocyte Nucleus ◽  
Cortical Region ◽  
Extracellular Matrix Components

In Drosophila dorsoventral (DV) polarity arises during oogenesis when the oocyte nucleus moves from a central posterior to an asymmetrical anterior position. Nuclear movement is a symmetry–breaking step and establishes orthogonality between the anteroposterior and the DV axes. The asymmetrically anchored nucleus defines a cortical region within the oocyte which accumulates high levels of gurken messenger RNA (mRNA) and protein. Gurken is an ovarian–specific member of the transforming growth factor–α (TGF–α) family of secreted ligands. Secreted Gurken forms a concentration gradient that results in a dorsal–to–ventral gradient of EGF receptor activation in the follicle cells surrounding the oocyte. This leads to concentration–dependent activation or repression of target genes of the EGF pathway in the follicular epithelium. One outcome of this process is the restriction of pipe expression to a ventral domain that comprises 40% of the egg circumference. Pipe presumably modifies extracellular matrix components that are secreted by the follicle cells and are present at the ventral side of embryo after egg deposition. Here, they activate a proteolytic cascade that generates a gradient of the diffusible ligand, Spätzle. Spätzle activates the Toll receptor at the surface of the embryo that stimulates the nuclear uptake of the transcription factor Dorsal. This leads to a nuclear concentration gradient of Dorsal that specifies the cell types along the DV axis of the embryo.

Patterning of the follicle cell epithelium along the anterior-posterior axis during Drosophila oogenesis

Development ◽  
1998 ◽  
Vol 125 (15) ◽  
pp. 2837-2846 ◽  
Author(s):  
A. Gonzalez-Reyes ◽  
D. St Johnston
Keyword(s):  
Follicle Cell ◽  
Cell Types ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Axis Formation ◽  
Main Body ◽  
Drosophila Oogenesis ◽  
Egfr Mutant ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

Gurken signals from the oocyte to the adjacent follicle cells twice during Drosophila oogenesis; first to induce posterior fate, thereby polarising the anterior-posterior axis of the future embryo and then to induce dorsal fate and polarise the dorsal-ventral axis. Here we show that Gurken induces two different follicle cell fates because the follicle cells at the termini of the egg chamber differ in their competence to respond to Gurken from the main-body follicle cells in between. By removing the putative Gurken receptor, Egfr, in clones of cells, we show that Gurken signals directly to induce posterior fate in about 200 cells, defining a terminal competence domain that extends 10–11 cell diameters from the pole. Furthermore, small clones of Egfr mutant cells at the posterior interpret their position with respect to the pole and differentiate as the appropriate anterior cell type. Thus, the two terminal follicle cell populations contain a symmetric prepattern that is independent of Gurken signalling. These results suggest a three-step model for the anterior-posterior patterning of the follicular epithelium that subdivides this axis into at least five distinct cell types. Finally, we show that Notch plays a role in both the specification and patterning of the terminal follicle cells, providing a possible explanation for the defect in anterior-posterior axis formation caused by Notch and Delta mutants.

scholarly journals mago nashi mediates the posterior follicle cell-to-oocyte signal to organize axis formation in Drosophila

Development ◽  
1997 ◽  
Vol 124 (16) ◽  
pp. 3197-3207 ◽  
Author(s):  
P.A. Newmark ◽  
S.E. Mohr ◽  
L. Gong ◽  
R.E. Boswell
Keyword(s):  
Germ Plasm ◽  
Egf Receptor ◽  
Germ Line ◽  
Follicle Cell ◽  
Posterior Pole ◽  
Follicle Cells ◽  
Oocyte Nucleus ◽  
Axis Formation ◽  
Pole Plasm ◽  
Mago Nashi

Establishment of the anteroposterior and dorsoventral axes in the Drosophila egg chamber requires reciprocal signaling between the germ line and soma. Upon activation of the Drosophila EGF receptor in the posterior follicle cells, these cells signal back to the oocyte, resulting in a reorganization of the oocyte cytoplasm and anterodorsal migration of the oocyte nucleus. We demonstrate that the gene mago nashi (mago) encodes an evolutionarily conserved protein that must be localized within the posterior pole plasm for germ-plasm assembly and Caenorhabditis elegans mago is a functional homologue of Drosophila mago. In the absence of mago+ function during oogenesis, the anteroposterior and dorsoventral coordinates of the oocyte are not specified and the germ plasm fails to assemble.

The relationship between ovarian and embryonic dorsoventral patterning in Drosophila

Development ◽  
1994 ◽  
Vol 120 (8) ◽  
pp. 2245-2257 ◽  
Author(s):  
S. Roth ◽  
T. Schupbach
Keyword(s):  
Egf Receptor ◽  
Germ Line ◽  
Early Embryo ◽  
Follicular Epithelium ◽  
Forming Process ◽  
Cell Fates ◽  
Dorsoventral Axis ◽  
Potential Ligand ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

In Drosophila, the dorsoventral asymmetry of the egg chamber depends on a dorsalizing signal that emanates from the oocyte. This signal is supplied by the TGF alpha-like gurken protein whose RNA is localized to the dorsal-anterior corner of the oocyte, gurken protein is the potential ligand of the Drosophila EGF receptor homolog (torpedo), which is expressed in the follicular epithelium surrounding the oocyte. Here, we describe how changes in the dorsalizing germ-line signal affect the embryonic dorsoventral pattern. A reduction in strength of the germ-line signal as produced by mutations in gurken or torpedo does not change the slope of the embryonic dorsoventral morphogen gradient, but causes a splitting of the gradient ventrally. This leads to embryos with two partial dorsoventral axes. A change in distribution of the germ-line signal as caused by fs(1)K10, squid and orb mutations leads to a shift in the orientation of the embryonic dorsoventral axis relative to the anterior-posterior axis. In extreme cases, this results in embryos with a dorsoventral axis almost parallel to the anterior-posterior axis. These results imply that gurken, unlike other localized cytoplasmic determinants, is not directly responsible for the establishment of cell fates along a body axis, but that it restricts and orients an active axis-forming process which occurs later in the follicular epithelium or in the early embryo.

Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis

Development ◽  
1997 ◽  
Vol 124 (22) ◽  
pp. 4639-4647 ◽  
Author(s):  
W.M. Deng ◽  
M. Bownes
Keyword(s):  
Growth Factor ◽  
Transforming Growth Factor Beta ◽  
Egf Receptor ◽  
Transforming Growth Factor ◽  
Growth Factor Receptor ◽  
Signalling Pathway ◽  
Follicle Cells ◽  
Signalling Pathways ◽  
Gene Encoding ◽  
Broad Complex

The Drosophila eggshell, which has a pair of chorionic appendages (dorsal appendages) located asymmetrically along both the anterior/posterior and dorsal/ventral axes, provides a good model to study signal instructed morphogenesis. We show that the Broad-Complex, a gene encoding zinc-finger transcription factors, is essential for the morphogenesis of dorsal appendages and is expressed in a bilaterally symmetrical pattern in the lateral-dorsal-anterior follicle cells during late oogenesis. This is induced and specified along the dorsoventral axis by an epidermal growth factor receptor signalling pathway, which includes a localised transforming growth factor-alpha like molecule, Gurken, in the oocyte and the Drosophila EGF receptor homologue, Torpedo, in the surrounding somatic follicle cells. Furthermore, the precisely localised expression of BR-C along the AP axis requires a separate signalling pathway, initiated by a transforming growth factor-beta homologue, Decapentaplegic, in nearby follicle cells. These two signalling pathways, one from the oocyte and the other from the follicle cells, co-ordinately specify patches of follicle cells to express the Broad-Complex in a unique position in respect to both major axes, which in turn directs the differentiation of the dorsal appendages in the correct position on the eggshell.

Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo

Development ◽  
1997 ◽  
Vol 124 (19) ◽  
pp. 3871-3880 ◽  
Author(s):  
A.M. Queenan ◽  
A. Ghabrial ◽  
T. Schupbach
Keyword(s):  
Cell Fate ◽  
Growth Factor Receptor ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Cell Fates ◽  
Egfr Activation ◽  
Egg Chamber ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

The Drosophila gene torpedo/Egfr (top/Egfr) encodes a homolog of the vertebrate Epidermal Growth Factor receptor. This receptor is required several times during the life cycle of the fly for the transmisson of developmental cues. During oogenesis, Top/Egfr activation is required for the establishment of the dorsal/ventral axis of the egg and the embryo. To examine how ectopic Top/Egfr activation affects cell fate determination, we constructed an activated version of the protein. Expression of this activated form (lambda top) in the follicle cells of the ovary induces dorsal cell fates in both the follicular epithelium and the embryo. Different levels of expression resulted in different dorsal follicle cell fates. These dorsal cell fates were expanded in the anterior, but not the posterior, of the egg, even in cases where all the follicle cells covering the oocyte expressed lambda top. The expression of genes known to respond to top/Egfr activation, argos (aos), kekkon1 (kek 1) and rhomboid (rho), was also expanded in the presence of the lambda top construct. When lambda top was expressed in all the follicle cells covering the oocyte, kek 1 and argos expression was induced in follicle cells all along the anterior/posterior axis of the egg chamber. In contrast, rho RNA expression was only activated in the anterior of the egg chamber. These data indicate that the response to Top/Egfr signaling is regulated by an anterior/posterior prepattern in the follicle cells. Expression of lambda top in the entire follicular epithelium resulted in an embryo dorsalized along the entire anterior/posterior axis. Expression of lambda top in anterior or posterior subpopulations of follicle cells resulted in regionally autonomous dorsalization of the embryos. This result indicates that subpopulations of follicle cells along the anterior/posterior axis can respond to Top/Egfr activation independently of one another.

Laser ablation studies of the role of the Drosophila oocyte nucleus in pattern formation

Science ◽  
1991 ◽  
Vol 254 (5029) ◽  
pp. 290-293
Author(s):  
DJ Montell ◽  
H Keshishian ◽  
AC Spradling
Keyword(s):  
Laser Ablation ◽  
Pattern Formation ◽  
Posterior Pole ◽  
Follicle Cells ◽  
Oocyte Nucleus ◽  
Dorsoventral Patterning ◽  
Egg Chambers ◽  
Germline Cells

Somatic and germline cells interact during oogenesis to establish the pattern axes of the Drosophila eggshell and embryo. The role of the oocyte nucleus in pattern formation was tested with the use of laser ablation. Ablation in stage 6 to 9 egg chambers caused partial or complete ventralization of the eggshell, phenotypes similar to those of eggs produced by gurken or torpedo females. Accumulation of vasa protein at the posterior pole of treated oocytes was also disrupted. Thus the oocyte nucleus is required as late as stage 9 for dorsoventral patterning within the follicle cells and for polar plasm assembly in the oocyte.

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.

Sprouty is a general inhibitor of receptor tyrosine kinase signaling

Development ◽  
1999 ◽  
Vol 126 (18) ◽  
pp. 4139-4147 ◽  
Author(s):  
A. Reich ◽  
A. Sapir ◽  
B. Shilo
Keyword(s):  
Tyrosine Kinase ◽  
Map Kinase ◽  
Receptor Tyrosine Kinase ◽  
Egf Receptor ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Fgf Receptor ◽  
Dorsal Appendage ◽  
Egfr Activation

Sprouty was originally identified as an inhibitor of Drosophila FGF receptor signaling during tracheal development. By following the capacity of ectopic Sprouty to abolish the pattern of activated MAP kinase in embryos, we show that Sprouty can inhibit other receptor tyrosine kinase (RTK) signaling pathways, namely the Heartless FGF receptor and the EGF receptor. Similarly, in wing imaginal discs, ectopic Sprouty abolishes activated MAP kinase induced by the EGF receptor pathway. Sprouty expression is induced by the EGFR pathway in some, but not all, tissues in which EGFR is activated, most notably in follicle cells of the ovary, the wing imaginal disc and the eye disc. In the ovary, induction of sprouty expression follows the pattern of EGFR activation in the follicle cells. Generation of homozygous sprouty mutant follicle-cell clones demonstrates an essential role for Sprouty in restricting EGFR activation throughout oogenesis. At the stage when dorso-ventral polarity of the follicle cells is established, Sprouty limits the ventral expansion of the activating Gurken signal. Later, when dorsal appendage fates are determined, reduction of signaling by Sprouty facilitates the induction of inter-appendage cell fates. The capacity of Sprouty to reduce or eliminate accumulation of activated MAP kinase indicates that in vivo it intersects with the pathway upstream to MAP kinase. The ability of ectopic Sprouty to rescue lethality caused by activated Raf suggests that it may impinge upon the pathway by interacting with Raf or downstream to it.

scholarly journals Post-transcriptional regulation of gurken by encore is required for axis determination in Drosophila

Development ◽  
1997 ◽  
Vol 124 (23) ◽  
pp. 4801-4810 ◽  
Author(s):  
N.C. Hawkins ◽  
C. Van Buskirk ◽  
U. Grossniklaus ◽  
T. Schupbach
Keyword(s):  
Transcriptional Regulation ◽  
Cell Fate ◽  
Egf Receptor ◽  
Follicle Cell ◽  
Follicular Epithelium ◽  
Protein Levels ◽  
Correct Pattern ◽  
Egg Shell ◽  
Post Transcriptional Regulation ◽  
Anterior Posterior

Establishment of anterior-posterior and dorsal-ventral polarity within the Drosophila egg chamber requires signaling between the germline and the somatic cells of the ovary. The gene gurken (grk) encodes a TGFalpha-like protein that is localized within the developing oocyte and is thought to locally activate torpedo/Egfr (top/Egfr), the Drosophila homolog of the EGF receptor, which is expressed throughout the follicular epithelium surrounding the oocyte. grk-Egfr signaling is required early in oogenesis for specification of posterior follicle cell fate and later in oogenesis for dorsal follicle cell fate determination, thus establishing the axes of the egg shell and embryo. Previous studies have shown that these patterning processes are highly sensitive to changes in the levels and localization of grk mRNA. Here we show that post-transcriptional regulation of Grk protein levels is required for correct pattern formation. encore (enc), a gene that functions in the regulation of germline mitosis and maintenance of oocyte identity, is also required for the accumulation of Grk protein during oogenesis. We present evidence that enc regulates Grk post-transcriptionally to ensure adequate levels of signaling for establishment of the anterior-posterior and dorsal-ventral axes.

Sign in / Sign up

Export Citation Format

Share Document