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 The Drosophila anterior-posterior axis is polarized by asymmetric myosin activation

2021 ◽  
Author(s):  
Helene Doerflinger ◽  
Vitaly Zimyanin ◽  
Daniel St Johnston
Keyword(s):  
Light Chain ◽  
Kinase Inhibitor ◽  
Germ Line ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Axis Formation ◽  
Posterior Cortex ◽  
Cortical Tension ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

The Drosophila anterior-posterior (AP) axis is specified at mid-oogenesis when Par-1 kinase is recruited to the posterior cortex of the oocyte, where it polarises the microtubule cytoskeleton to define where the axis determinants, bicoid and oskar mRNAs localise. This polarity is established in response to an unknown signal from the follicle cells, but how this occurs is unclear. Here we show that the myosin chaperone, Unc-45 and Non-Muscle Myosin II (MyoII) are required in the germ line upstream of Par-1 in polarity establishment. Furthermore, the Myosin regulatory Light Chain (MRLC) is di-phosphorylated at the oocyte posterior in response to the follicle cell signal, inducing longer pulses of myosin contractility at the posterior and increased cortical tension. Over-expression of MRLC-T21A that cannot be di-phosphorylated or acute treatment with the Myosin light chain kinase inhibitor ML-7 abolish Par-1 localisation, indicating that posterior of MRLC di-phosphorylation is essential for polarity. Thus, asymmetric myosin activation polarizes the anterior-posterior axis by recruiting and maintaining Par-1 at the posterior cortex. This raises an intriguing parallel with AP axis formation in C. elegans where MyoII is also required to establish polarity, but functions to localize the anterior PAR proteins rather than PAR-1.

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.

The Drosophila AP axis is polarised by the cadherin-mediated positioning of the oocyte

Development ◽  
1998 ◽  
Vol 125 (18) ◽  
pp. 3635-3644 ◽  
Author(s):  
A. Gonzalez-Reyes ◽  
D. St Johnston
Keyword(s):  
Germ Cell ◽  
Follicle Cell ◽  
Cell Types ◽  
Follicle Cells ◽  
Cell Rearrangement ◽  
Germline Cyst ◽  
Germline Cells ◽  
Adhesion Complex ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

The anterior-posterior axis of Drosophila originates from two symmetry-breaking steps during early oogenesis. First, one of the two pro-oocytes within the cyst of 16 germline cells is selected to become the oocyte. This cell then comes to lie posterior to the other germline cells of the cyst, thereby defining the polarity of the axis. Here we show that the oocyte reaches the posterior of the cyst in two steps. (1) The cyst flattens as it enters region 2b of the germarium to place the two pro-oocytes in the centre of the cyst, where they contact the posterior follicle cells. (2) One cell is selected to become the oocyte and protrudes into the posterior follicle cell layer when the cyst rounds up on entering region 3. During this germ cell rearrangement, the components of the homophilic cadherin adhesion complex, DE-cadherin, Armadillo and alpha-catenin, accumulate along the border between the oocyte and the posterior follicle cells. Furthermore, the positioning of the oocyte requires cadherin-dependent adhesion between these two cell types, since the oocyte is frequently misplaced when DE-cadherin is removed from either the germline or the posterior follicle cells. We conclude that the oocyte reaches the posterior of the germline cyst because it adheres more strongly to the posterior follicle cells than its neighbours during the germ cell rearrangement that occurs as the cyst moves into region 3. The Drosophila anterior-posterior axis therefore becomes polarised by an unusual cadherin-mediated adhesion between a germ cell and mesodermal follicle cells.

scholarly journals Misshapen decreases integrin levels to promote epithelial motility and planar polarity in Drosophila

2013 ◽  
Vol 200 (6) ◽  
pp. 721-729 ◽  
Author(s):  
Lindsay Lewellyn ◽  
Maureen Cetera ◽  
Sally Horne-Badovinac
Keyword(s):  
Individual Cell ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Primary Role ◽  
Planar Polarity ◽  
Egg Chamber ◽  
And Migration ◽  
Anterior Posterior ◽  
Complex Organ ◽  
Anterior Posterior Axis

Complex organ shapes arise from the coordinate actions of individual cells. The Drosophila egg chamber is an organ-like structure that lengthens along its anterior–posterior axis as it grows. This morphogenesis depends on an unusual form of planar polarity in the organ’s outer epithelial layer, the follicle cells. Interestingly, this epithelium also undergoes a directed migration that causes the egg chamber to rotate around its anterior–posterior axis. However, the functional relationship between planar polarity and migration in this tissue is unknown. We have previously reported that mutations in the Misshapen kinase disrupt follicle cell planar polarity. Here we show that Misshapen’s primary role in this system is to promote individual cell motility. Misshapen decreases integrin levels at the basal surface, which may facilitate detachment of each cell’s trailing edge. These data provide mechanistic insight into Misshapen’s conserved role in cell migration and suggest that follicle cell planar polarity may be an emergent property of individual cell migratory behaviors within the epithelium.

scholarly journals Expression of constitutively active Notch arrests follicle cells at a precursor stage during Drosophila oogenesis and disrupts the anterior-posterior axis of the oocyte

Development ◽  
1996 ◽  
Vol 122 (11) ◽  
pp. 3639-3650 ◽  
Author(s):  
M.K. Larkin ◽  
K. Holder ◽  
C. Yost ◽  
E. Giniger ◽  
H. Ruohola-Baker
Keyword(s):  
Cell Fate ◽  
Ovarian Follicle ◽  
Follicle Cells ◽  
Cell Fates ◽  
Drosophila Oogenesis ◽  
Cell Fate Decisions ◽  
Notch Gene ◽  
Anterior Posterior ◽  
Anterior Posterior Axis ◽  
Constitutively Active

During early development, there are numerous instances where a bipotent progenitor divides to give rise to two progeny cells with different fates. The Notch gene of Drosophila and its homologues in other metazoans have been implicated in many of these cell fate decisions. It has been argued that the role of Notch in such instances may be to maintain cells in a precursor state susceptible to specific differentiating signals. This has been difficult to prove, however, due to a lack of definitive markers for precursor identity. We here perform molecular and morphological analyses of the roles of Notch in ovarian follicle cells during Drosophila oogenesis. These studies show directly that constitutively active Notch arrests cells at a precursor stage, while the loss of Notch function eliminates this stage. Expression of moderate levels of activated Notch leads to partial transformation of cell fates, as found in other systems, and we show that this milder phenotype correlates with a prolonged, but still transient, precursor stage. We also find that expression of constitutively active Notch in follicle cells at later stages leads to a defect in the anterior-posterior axis of the oocyte.

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.

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.

Mechanisms of Gurken-dependentpiperegulation and the robustness of dorsoventral patterning inDrosophila

Development ◽  
2002 ◽  
Vol 129 (12) ◽  
pp. 2965-2975 ◽  
Author(s):  
Francesca Peri ◽  
Martin Technau ◽  
Siegfried Roth
Keyword(s):  
Egf Receptor ◽  
Follicle Cell ◽  
Dorsal Side ◽  
Drosophila Embryo ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Axis Formation ◽  
Embryonic Patterning ◽  
Cell Fates ◽  
Egg Chamber

The restriction of Pipe, a potential glycosaminoglycan-modifying enzyme, to ventral follicle cells of the egg chamber is essential for dorsoventral axis formation in the Drosophila embryo. pipe repression depends on the TGFα-like ligand Gurken, which activates the Drosophila EGF receptor in dorsal follicle cells. An analysis of Raf mutant clones shows that EGF signalling is required cell-autonomously in all dorsal follicle cells along the anteroposterior axis of the egg chamber to repress pipe. However, the autoactivation of EGF signalling important for dorsal follicle cell patterning has no influence on pipe expression. Clonal analysis shows that also the mirror-fringe cassette suggested to establish a secondary signalling centre in the follicular epithelium is not involved in pipe regulation. These findings support the view that the pipe domain is directly delimited by a long-range Gurken gradient. Pipe induces ventral cell fates in the embryo via activation of the Spätzle/Toll pathway. However, large dorsal patches of ectopic pipe expression induced by Raf clones rarely affect embryonic patterning if they are separated from the endogenous pipe domain. This indicates that potent inhibitory processes prevent pipe dependent Toll activation at the dorsal side of the egg.

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