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.

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.

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.

Cumulus expansion initiates physical and developmental autonomy of the oocyte

Zygote ◽  
1996 ◽  
Vol 4 (04) ◽  
pp. 335-341 ◽  
Author(s):  
William J. Larsen ◽  
Lin Chen ◽  
Robert Powers ◽  
Hong Zhang ◽  
Paul T. Russell ◽  
...  
Keyword(s):  
Gap Junctions ◽  
Germ Cell ◽  
Cell Population ◽  
Follicle Cell ◽  
Ovarian Cycle ◽  
Follicle Cells ◽  
Cumulus Expansion ◽  
Primary Oocyte ◽  
Female Germ Cell

As meiosis is initiated and the oogonium is transformed into a primary oocyte, the female germ cell becomes intimately invested by a single squamous layer of sex cord epithelium. As the follicle cell population expands during the initial stages of the ovarian cycle, oocyte and follicle cells become increasingly connected to one another by one of the most extensive populations of gap junctions documented in any epithelium (reviewed in Larsen & Wert, 1988).

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.

scholarly journals The receptor-like tyrosine phosphatase Lar is required for epithelial planar polarity and for axis determination with Drosophila ovarian follicles

Development ◽  
2001 ◽  
Vol 128 (16) ◽  
pp. 3209-3220 ◽  
Author(s):  
Horacio M. Frydman ◽  
Allan C. Spradling
Keyword(s):  
Tyrosine Phosphatase ◽  
Cell Monolayer ◽  
Follicle Cell ◽  
Positional Information ◽  
Follicle Cells ◽  
Dependent Manner ◽  
Cell Specification ◽  
Major Function ◽  
Polar Cell ◽  
Anterior Posterior

The follicle cell monolayer that encircles each developingDrosophila oocyte contributes actively to egg development and patterning, and also represents a model stem cell-derived epithelium. We have identified mutations in the receptor-like transmembrane tyrosine phosphataseLar that disorganize follicle formation, block egg chamber elongation and disrupt Oskar localization, which is an indicator of oocyte anterior-posterior polarity. Alterations in actin filament organization correlate with these defects. Actin filaments in the basal follicle cell domain normally become polarized during stage 6 around the anterior-posterior axis defined by the polar cells, but mutations in Lar frequently disrupt polar cell differentiation and actin polarization. Lar function is only needed in somatic cells, and (for Oskar localization) its action is autonomous to posterior follicle cells. Polarity signals may be laid down by these cells within the extracellular matrix (ECM), possibly in the distribution of the candidate Lar ligand Laminin A, and read out at the time Oskar is localized in a Lar-dependent manner. Lar is not required autonomously to polarize somatic cell actin during stages 6. We show thatLar acts somatically early in oogenesis, during follicle formation,and postulate that it functions in germarium intercyst cells that are required for polar cell specification and differentiation. Our studies suggest that positional information can be stored transiently in the ECM. A major function of Lar may be to transduce such signals.

scholarly journals Topographic distribution pattern of morphologically different G cells in the murine antral mucosa

2017 ◽  
Vol 61 (3) ◽  
Author(s):  
Claudia Frick ◽  
Hanna Luisa Martin ◽  
Johanna Bruder ◽  
Kerstin Lang ◽  
Heinz Breer
Keyword(s):  
Distribution Pattern ◽  
Cell Types ◽  
Enteroendocrine Cells ◽  
Antral Mucosa ◽  
G Cells ◽  
G Cell ◽  
Ec Cells ◽  
D Cells ◽  
Anterior Posterior ◽  
Anterior Posterior Axis

<p>Gastrin-secreting enteroendocrine cells (G cells) in the antrum play an important role in the regulation of gastric secretion, gastric motility and mucosal cell proliferation. Recently we have uncovered the existence of two subpopulations of G cells with pivotally different morphology and a distinct localization in the antral invaginations; the functional implications of the different G cell types are still elusive. In this study a transgenic mouse line in which EGFP is expressed under the control of a gastrin promoter was used to elucidate the distribution pattern of the two G cell types throughout the different regions of the antrum. The results of immunohistochemical analyses revealed that G cells were not equally distributed along the anterior/posterior axis of the antrum. The “typical” pyramidal- or roundish-shaped G cells, which are located in the basal region of the antral invaginations, were more abundant in the proximal antrum bordering the corpus region but less frequent in the distal antrum bordering the pylorus. In contrast, the “atypical” G cells, which are located in the upper part of the antral invaginations and have a spindle-like contour with long processes, were evenly distributed along the anterior/posterior axis. This characteristic topographic segregation supports the notion that the two G cell types may serve different functions. A comparison of the antrum specific G cells with the two pan-gastrointestinal enteroendocrine cell types, somatostatin-secreting D cells and serotonin-secreting enterochromaffin (EC) cells, revealed a rather similar distribution pattern of G and D cells, but a fundamentally different distribution of EC cells. These observations suggest that distinct mechanisms govern the spatial segregation of enteroendocrine cells in the antrum mucosa.</p>

The Drosophila ribosome protein S5 paralog RpS5b promotes germ cell and follicle cell differentiation during oogenesis

Development ◽  
2021 ◽  
Author(s):  
Seoyeon Jang ◽  
Jeon Lee ◽  
Jeremy Mathews ◽  
Holly Ruess ◽  
Anna O. Williford ◽  
...  
Keyword(s):  
Germ Cell ◽  
Notch Pathway ◽  
Follicle Cell ◽  
Cell Types ◽  
Female Sterility ◽  
Drosophila Genome ◽  
Post Translational Modification ◽  
Specific Expression ◽  
Pathway Activation ◽  
Egg Chambers

Emerging evidence suggests that ribosome heterogeneity may have important functional consequences in the translation of specific mRNAs within different cell types and under various conditions. Ribosome heterogeneity comes in many forms including post-translational modification of ribosome proteins (RPs), absence of specific RPs, and inclusion of different RP paralogs. The Drosophila genome encodes two RpS5 paralogs, RpS5a and RpS5b. While RpS5a is ubiquitously expressed, RpS5b exhibits enriched expression in the reproductive system. Deletion of RpS5b results in female sterility marked by developmental arrest of egg chambers at stages 7-8, disruption of vitellogenesis, and posterior follicle cell (PFC) hyperplasia. While transgenic rescue experiments suggest functional redundancy between RpS5a and RpS5b, molecular, biochemical, and ribo-seq experiments indicate that RpS5b mutants display increased rRNA transcription and RP production, accompanied by increased protein synthesis. Loss of RpS5b results in microtubule-based defects and mislocalization of Delta and Mindbomb1, leading to failure of Notch pathway activation in PFCs. Together, our results indicate that germ cell specific expression of RpS5b promotes proper egg chamber development by ensuring the homeostasis of functional ribosomes.

scholarly journals The role of integrins in Drosophila egg chamber morphogenesis

2019 ◽  
Author(s):  
Holly E. Lovegrove ◽  
Dan T. Bergstralh ◽  
Daniel St Johnston
Keyword(s):  
Basement Membrane ◽  
Cell Polarity ◽  
Cell Shape ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Follicular Epithelium ◽  
Egg Chambers ◽  
Germline Cyst ◽  
Egg Chamber

AbstractA Drosophila egg chamber is comprised of a germline cyst surrounded by a tightly-organised epithelial monolayer, the follicular epithelium (FE). Loss of integrin function from the FE disrupts epithelial organisation at egg chamber termini, but the cause of this phenotype remains unclear. Here we show that the β-integrin Myospheroid (Mys) is only required during early oogenesis when the pre-follicle cells form the FE. mys mutants disrupt both the formation of a monolayered epithelium at egg chamber termini and the morphogenesis of the stalk between adjacent egg chambers, which develops through the intercalation of two rows of cells into a single-cell wide stalk. Secondary epithelia, like the FE, have been proposed to require adhesion to the basement membrane to polarise. However, Mys is not required for pre-follicle cell polarisation, as both follicle and stalk cells localise polarity factors correctly, despite being mispositioned. Instead, loss of integrins causes pre-follicle cells to basally constrict, detach from the basement membrane and become internalised. Thus, integrin function is dispensable for pre-follicle cell polarity but is required to maintain cellular organisation and cell shape during morphogenesis.

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