Regulation of cell proliferation and patterning in Drosophila oogenesis by Hedgehog signaling

Development ◽  
2000 ◽  
Vol 127 (10) ◽  
pp. 2165-2176 ◽  
Author(s):  
Y. Zhang ◽  
D. Kalderon
Keyword(s):  
Hedgehog Signaling ◽  
Developmental Stages ◽  
Somatic Cells ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Cell Lineages ◽  
Egg Chambers ◽  
Hh Signaling ◽  
Egg Chamber ◽  
Activity Loss

The localized expression of Hedgehog (Hh) at the extreme anterior of Drosophila ovarioles suggests that it might provide an asymmetric cue that patterns developing egg chambers along the anteroposterior axis. Ectopic or excessive Hh signaling disrupts egg chamber patterning dramatically through primary effects at two developmental stages. First, excess Hh signaling in somatic stem cells stimulates somatic cell over-proliferation. This likely disrupts the earliest interactions between somatic and germline cells and may account for the frequent mis-positioning of oocytes within egg chambers. Second, the initiation of the developmental programs of follicle cell lineages appears to be delayed by ectopic Hh signaling. This may account for the formation of ectopic polar cells, the extended proliferation of follicle cells and the defective differentiation of posterior follicle cells, which, in turn, disrupts polarity within the oocyte. Somatic cells in the ovary cannot proliferate normally in the absence of Hh or Smoothened activity. Loss of protein kinase A activity restores the proliferation of somatic cells in the absence of Hh activity and allows the formation of normally patterned ovarioles. Hence, localized Hh is not essential to direct egg chamber patterning.

hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila

Development ◽  
1996 ◽  
Vol 122 (4) ◽  
pp. 1125-1135 ◽  
Author(s):  
A.J. Forbes ◽  
H. Lin ◽  
P.W. Ingham ◽  
A.C. Spradling
Keyword(s):  
Cell Proliferation ◽  
Somatic Cells ◽  
Follicle Cells ◽  
Cell Identity ◽  
Neurogenic Genes ◽  
Terminal Filament ◽  
Hh Signaling ◽  
Egg Chamber

The hedgehog (hh) gene plays a role in regulating cell proliferation and specifying cell identity in diverse systems. We show that hh is expressed at the extreme apical end of Drosophila ovarioles in terminal filament cells and a newly identified group of associated somatic cells. Reducing or ectopically expressing hh affects somatic cells in region 2 of the germarium, 2–5 cells away from the cells in which Hh protein is detected. hh activity stimulates the proliferation of pre-follicle somatic cells, and promotes the specification of polar follicle cells. hh signaling during egg chamber assembly appears to be closely related to, or part of pathways involving the neurogenic genes.

A targeted gene silencing technique shows that Drosophila myosin VI is required for egg chamber and imaginal disc morphogenesis

1999 ◽  
Vol 112 (21) ◽  
pp. 3677-3690 ◽  
Author(s):  
W. Deng ◽  
K. Leaper ◽  
M. Bownes
Keyword(s):  
Gene Silencing ◽  
Imaginal Disc ◽  
Developmental Stages ◽  
Expression System ◽  
Follicle Cell ◽  
Follicle Cells ◽  
Myosin Vi ◽  
Nurse Cells ◽  
Cell Shapes ◽  
Egg Chamber

We report that Drosophila unconventional myosin VI, encoded by Myosin heavy chain at 95F (Mhc95F), is required for both imaginal disc and egg chamber morphogenesis. During oogenesis, Mhc95F is expressed in migrating follicle cells, including the border cells, which migrate between the nurse cells to lie at the anterior of the oocyte; the columnar cells that migrate over the oocyte; the centripetal cells that migrate between the oocyte and nurse cells; and the dorsal-anterior follicle cells, which migrate to secrete the chorionic appendages. Its function during development has been studied using a targeted gene silencing technique, combining the Gal4-UAS targeted expression system and the antisense RNA technique. Antibody staining shows that the expression of myosin 95F is greatly decreased in follicle cells when antisense Mhc95F RNA is expressed. Interfering with expression of Drosophila myosin VI at various developmental stages frequently results in lethality. During metamorphosis it results in adult flies with malformed legs and wings, indicating that myosin VI is essential for imaginal disc morphogenesis. During oogenesis, abnormal follicle cell shapes and aberrant follicle cell migrations are observed when antisense Mhc95F is expressed in follicle cells during stages 9 to 10, suggesting that the Drosophila myosin VI is required for follicle cell epithelial morphogenesis.

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.

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.

cut interacts with Notch and protein kinase A to regulate egg chamber formation and to maintain germline cyst integrity during Drosophila oogenesis

Development ◽  
1997 ◽  
Vol 124 (18) ◽  
pp. 3663-3672 ◽  
Author(s):  
S.M. Jackson ◽  
K. Blochlinger
Keyword(s):  
Protein Kinase ◽  
Protein Kinase A ◽  
Structural Integrity ◽  
Follicle Cells ◽  
Drosophila Oogenesis ◽  
Cell Complexes ◽  
Genetic Manipulations ◽  
Egg Chambers ◽  
Egg Chamber ◽  
Kinase A

Communications between the germline and the soma during Drosophila oogenesis have been previously shown to be essential for the formation of egg chambers and to establish polarity in the developing oocyte. In this report, we demonstrate that the function of a somatically expressed gene, cut, is critical for maintaining the structural integrity of germline-derived cells and their arrangement within an egg chamber. Genetic manipulations of cut activity resulted in defective packaging of germline-derived cysts into egg chambers and disintegration of the structural organization of oocyte-nurse cell complexes to generate multinucleate germline-derived cells. We also found that cut interacts genetically with the Notch gene and with the catalytic subunit of Protein kinase A gene during egg chamber morphogenesis. Since cut expression is restricted to the somatic follicle cells and cut mutant germline clones are phenotypically normal, we propose that the defects in the assembly of egg chambers and the changes in germline cell morphology observed in cut mutant egg chambers are the result of altered interactions between follicle cells and germline cells. cut encodes a nuclear protein containing DNA-binding motifs, and we suggest that it participates in intercellular communications by regulating the expression of molecules that directly participate in this process.

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 Mechanochemical regulation of oscillatory follicle cell dynamics in the developing Drosophila egg chamber

2014 ◽  
Vol 25 (22) ◽  
pp. 3709-3716 ◽  
Author(s):  
Sarita Koride ◽  
Li He ◽  
Li-Ping Xiong ◽  
Ganhui Lan ◽  
Denise J. Montell ◽  
...  
Keyword(s):  
Contractile Activity ◽  
Rho Kinase ◽  
Follicle Cell ◽  
Oscillation Period ◽  
Follicle Cells ◽  
Spatiotemporal Pattern ◽  
Activation Process ◽  
Epithelial Layer ◽  
Cell Dynamics ◽  
Egg Chamber

During tissue elongation from stage 9 to stage 10 in Drosophila oogenesis, the egg chamber increases in length by ∼1.7-fold while increasing in volume by eightfold. During these stages, spontaneous oscillations in the contraction of cell basal surfaces develop in a subset of follicle cells. This patterned activity is required for elongation of the egg chamber; however, the mechanisms generating the spatiotemporal pattern have been unclear. Here we use a combination of quantitative modeling and experimental perturbation to show that mechanochemical interactions are sufficient to generate oscillations of myosin contractile activity in the observed spatiotemporal pattern. We propose that follicle cells in the epithelial layer contract against pressure in the expanding egg chamber. As tension in the epithelial layer increases, Rho kinase signaling activates myosin assembly and contraction. The activation process is cooperative, leading to a limit cycle in the myosin dynamics. Our model produces asynchronous oscillations in follicle cell area and myosin content, consistent with experimental observations. In addition, we test the prediction that removal of the basal lamina will increase the average oscillation period. The model demonstrates that in principle, mechanochemical interactions are sufficient to drive patterning and morphogenesis, independent of patterned gene expression.

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 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.

Drosophila puckered regulates Fos/Jun levels during follicle cell morphogenesis

Development ◽  
2001 ◽  
Vol 128 (10) ◽  
pp. 1845-1856 ◽  
Author(s):  
L.L. Dobens ◽  
E. Martin-Blanco ◽  
A. Martinez-Arias ◽  
F.C. Kafatos ◽  
L.A. Raftery
Keyword(s):  
Nurse Cell ◽  
Ectopic Expression ◽  
Follicle Cell ◽  
Small Gtpase ◽  
Dominant Negative ◽  
Drosophila Embryo ◽  
Follicle Cells ◽  
Cell Morphogenesis ◽  
Jnk Pathway ◽  
Egg Chambers

puckered (puc) encodes a VH1-like phosphatase that down-regulates Jun kinase (JNK) activity during dorsal closure of the Drosophila embryo. We report a role for puc in follicle cell morphogenesis during oogenesis. puc mRNA accumulates preferentially in the centripetally migrating follicle cells and cells of the elongating dorsal appendages. Proper levels of Puc activity in the follicle cells are critical for the production of a normal egg: either reduced or increased Puc activity result in incomplete nurse cell dumping and aberrant dorsal appendages. Phenotypes associated with puc mutant follicle cells include altered DE-cadherin expression in the follicle cells and a failure of nurse cell dumping to coordinate with dorsal appendage elongation, leading to the formation of cup-shaped egg chambers. The JNK pathway target A251-lacZ showed cell-type-specific differences in its regulation by puc and by the small GTPase DRac1. puc mutant cells displayed region-specific ectopic expression of the A251-lacZ enhancer trap whereas overexpression of a transgene encoding Puc was sufficient to suppress lacZ expression in a cell autonomous fashion. Strikingly, decreased or increased puc function leads to a corresponding increase or decrease, respectively, of Fos and Jun protein levels. Taken together, these data indicate that puc modulates gene expression responses by antagonizing a Ρ GTPase signal transduction pathway that stabilizes the AP-1 transcription factor. Consistent with this, overexpression of a dominant negative DRac1 resulted in lower levels of Fos/Jun.

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