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First published online 3 May 2006
doi: 10.1242/dev.02369

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Capicua regulates follicle cell fate in the Drosophila ovary through repression of mirror

Department of Biology, McGill University, 1205 Doctor Penfield Avenue, Montreal, QC H3A 1B1, Canada.

View larger version (88K): [in a new window]   Fig. 1. cic mutant females produce eggs with a range of dorsalized phenotypes. (A) Wild-type egg (lateral view), exhibiting two dorsal appendages separated by an appendage-free dorsal midline region. (B-F) Eggs from cic mutant females, ventral or lateral views, as indicated. Eggs are grouped into five classes according to phenotypic severity. (B) Weak cic eggshell phenotype (lateral view). The dorsal midline region is expanded (arrow) and the appendages are broader and positioned laterally with a trace of ventral collar material (arrowhead). (C) Similar to B, but exhibiting a ventral collar of ectopic appendage-like material. (D) Egg with a thicker ventral collar (arrowhead). Lateral view illustrates that the collar is strictly ventrolateral and does not extend to the dorsal side (arrow). (E) Collar is more pronounced than in D. (F) Similar to E, with small anterior projections. (G-H') Eggs from females with follicle cell clones homozygous for cicfetU6. (G) Foci of ectopic appendage material are observed in the ventral and lateral anterior region. (H,H') At the extreme anterior, ectopic appendage-like projections can be observed (arrow). H is a dorsal view, H' a ventral view.

View larger version (132K): [in a new window]   Fig. 2. Ventral anterior follicle cells adopt an appendage-producing fate in cic mutant egg chambers. BR-C expression was visualized in wild-type (A,B) and cic mutant (C-F) egg chambers using an antibody recognizing all BR-C isoforms (Emery et al., 1994). (A) Wild-type stage 10 egg chamber (dorsal view). (B) Wild type, stage 12, dorsal (top) and ventral (bottom) views. (C) Stage 12 cicfetU6/cicfetT6 egg chambers, dorsolateral (top) and ventrolateral (bottom) views. The high BR-C nuclei are more densely organized than those with low BR-C. (D) Stage 10B egg chamber (ventral view) with homozygous cicfetU6 follicle cell clones marked by the absence of N-Myc (green). (E,E') Close-up of box I in D; clone boundary outlined in gray. In the vast majority of clones, ectopic elevated BR-C is cell autonomous. (F,F') Close-up of box II in D. Rare cases of nonautonomy (arrow, arrowhead) were observed near the endogenous appendage primordia. (G) Wild type, stage 12 (dorsal view), stained with rhodamine-labeled phalloidin. The cells of the appendage primordia are constricted apically. (H) Stage 12 ventral anterior cicfetU6 follicle cell clones marked by the absence of N-Myc. (H') Rhodamine phalloidin staining of the clones in H reveals similar cell shape changes in cic mutant cells.

View larger version (73K): [in a new window]   Fig. 3. cic mutant follicle cells exhibit ectopic mirr expression. (A-A'') Wild-type stage 10B egg chamber (dorsolateral view). (A) mirr-lacZ is expressed in dorsal anterior follicle cells. (A') At this stage, the two dorsal anterior high BR-C domains (outlined) have been established. (A'') Overlay illustrates that the mirr-lacZ domain aligns with the high BR-C domains. (B) Stage 10B cic mutant egg chamber, dorsal (top) and ventral (bottom) views. (C) Stage 10B (ventrolateral view). Homozygous cicfetU6 follicle cell clones are marked by the absence of nuclear GFP. (C') Endogenous dorsal anterior (top arrow) and ectopic anterior mirr-lacZ expression in the egg chamber in C. Ectopic mirr-lacZ is observed in cells in the anterior half (arrowheads), but not in the posterior half (arrows), of the columnar epithelium. (D) Ventral cicfetU6 mutant follicle cell clone (stage 10B) marked by the absence of N-Myc. (D') Ectopic mirr-lacZ expression is cell autonomous. (E-E'') Stage 14 egg chamber with a ventral cicfetU6 mutant clone (E, arrow) exhibiting ectopic mirr-lacZ expression (E', arrow) and ectopic appendage material (E", arrow).

View larger version (148K): [in a new window]   Fig. 4. Ectopic mirr expression is necessary and sufficient to induce appendage-producing fate. (A,A') Ventral anterior region of stage 11 cicfetT6/cicfetU6 egg chamber bearing follicle cell clones homozygous for mirre48 (A, absence of green). Ectopic high BR-C expression (A', red) is abolished in the mirr mutant cells. (B,B') Stage 14 egg chamber (lateral view) with follicle cell clones expressing UAS-mirr positively marked with GFP (green). BR-C expression (red) is also shown. (C,C') Stage 12 egg chamber (dorsolateral view) with positively-marked follicle cell clones expressing UAS-mirr (green). DE-Cadherin expression (red) was visualized with an anti-DE-cadherin antibody. (D,D') Stage 14 egg chamber (ventrolateral view) with homozygous fng13 follicle cell clones (D, absence of green). BR-C expression is shown in red.

View larger version (114K): [in a new window]   Fig. 5. Ectopic mirr expression in cic mutant egg chambers is grk independent. Anterior is to the upper left in all panels. (A) cic mutant egg chamber heterozygous for grk (lateral view, dorsal to the upper right) exhibiting ectopic mirr-lacZ expression. (B) grk2B6/grkHK egg chamber heterozygous for cic. The exposure time has been increased to emphasize the lack of mirr-lacZ expression. (C) Stage 14 grk2B6/grkHK egg chamber exhibiting a typical lack of dorsal appendages. (D,D') Top and bottom focal planes of a grk2B6/grkHK; cicfetU6/cicfetT6 egg chamber. Uniform mirr-lacZ expression is observed around the anterior circumference. (E) Stage 14 grk2B6/grkHK; cicfetU6/cicfetT6 egg chamber. The eggshell lacks dorsal appendages but exhibits a pronounced collar of appendage material. (F-F'') cicfetU6/cicfetT6 egg chamber with homozygous rhomboid6 clones (ventral view). (F) rhomboid6 clones (lack of green) including most of the follicular epithelium. (F') The ectopic expression of high BR-C levels is unaffected. (F'') Merged image. Identical results were obtained with two different strong rhomboid alleles.

View larger version (25K): [in a new window]   Fig. 6. Model for integration of AP and DV positional information and eggshell patterning. (A) Cartoon depicting a lateral surface view of a stage 10B egg chamber. A single appendage primordium (green) is shown. Cic is downregulated in dorsal follicle cells, allowing Dpp to induce mirr expression; dorsally-localized Egfr activation also positively regulates mirr independently of Cic. Cic remains present in the remaining follicle cells and prevents the induction of mirr by an anterior positional cue, probably Dpp. (B) Diagram of an anterior cross section through an egg chamber, illustrating the follicular epithelium (shaded outer section) surrounding the oocyte (inner large circle). The oocyte nucleus (gray circle in oocyte) marks the dorsal side. Cic (dark brown) is lost from dorsal follicle cells where Egfr signaling exceeds a certain threshold, rendering these follicle cells competent to express mirr and adopt an appendage-producing fate (green), and thus defining the ventral limit of the appendage primordia. As proposed previously (Wasserman and Freeman, 1998), Aos (red) is induced in dorsalmost follicle cells in response to higher levels of Egfr activation (circles), resulting in local downregulation of Egfr activation and generating a dorsal midline fate (light brown) that marks the dorsal limit of the appendage primordia.

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