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doi: 10.1242/10.1242/dev.00524

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wingless signaling regulates the maintenance of ovarian somatic stem cells in Drosophila

¹ Stowers Institute for Medical Research, 1000 East 50th Street, Kansas City, MO 64110, USA
² Department of Anatomy and Cell Biology, University of Kansas School of Medicine, 3901 Rainbow Blvd, Kansas City, KS 66160, USA

View larger version (56K): [in a new window]   Fig. 1. wg signaling regulates follicle cell production or differentiation in the Drosophila ovary. (A) Cross-sectional diagram of a Drosophila germarium. Two or three SSCs, follicle cell progenitors and differentiated follicle cells are located in regions 2A, 2B and 3, respectively. The micrographs in B-E represent one confocal cross section of the germarium or ovariole. (B) A wild-type germarium labeled for Wg (red) and nuclei (blue). Terminal filament and cap cells in the germarium express Wg proteins (cap cells indicated by arrowheads). (C) A wild-type germarium labeled for Hts (red) and nuclei (blue) showing 16-cell cysts (outlined). (D) A mutant wgts germarium labeled for Hts (red) and nuclei (blue) showing accumulation of extra 16-cell cysts (outlined). (E) A mutant wgts germarium labeled for Hts (red) and nuclei (blue) showing ongoing encapsulation of two cysts (outlined and indicated by arrows) into an egg chamber. All the germaria are shown at the same scale. Scale bar in B: 10 µm. CB, cystoblast; CPC, cap cell; DCs, developing cysts; FC, follicle cell; FS, fusome; GSCs, germline stem cells; IGS, inner germarial sheath cell; SS, spectrosomes; SSCs, somatic stem cells; TF, terminal filament cell.

View larger version (74K): [in a new window]   Fig. 2. Increasing wg signaling by over-expressing wg downstream components can promote follicle cell proliferation. The ovariole from the females over-expressing (A) no genes (control), (B) Fz2, (C) dsh and (D) an activated arm for four days are labeled for Vasa (red) and Hts (green). A shows normal stalk cells (arrows), whereas B-D show extra stalk cells (arrows). A and D represent one confocal section, whereas B and C show images of multiple sections. All the germaria are shown at the same scale. Scale bar in A: 10 µm.

View larger version (101K): [in a new window]   Fig. 3. wg downstream components are required for SSC maintenance. Germaria are labeled for lacZ (red), Hts (green), nuclei (blue). All the micrographs represent one confocal cross section of the germarium. Marked wild-type (A,B) or mutant (C-E) clones are outlined and are identified by loss of lacZ expression. (A) A germarium showing a one-week-old wild-type SSC clone and its follicle cell progeny (outlined). The putative marked SSC is indicated by an arrowhead. (B) A germarium showing a three-week-old wild-type SSC clone in which all follicle cells (outlined) are marked, indicating that all the SSCs are marked. One of the putative marked SSCs is indicated by an arrowhead. (C) A germarium showing a one-week-old mutant dshVA135 SSC clone (outlined). The putative marked dsh mutant SSC is indicated by an arrowhead. (D) A germarium showing loss of a marked mutant dshVA135 SSC clone three weeks after clone induction indicated by absence of marked follicle cells in the germarium but their presence in a late egg chamber (outlined in the inset). (E) A germarium with a marked mutant sgg clone three weeks after clone induction. (F) A germarium with all SSCs mutant for sgg three weeks after clone induction, indicated by loss of lacZ expression in all the follicle cells. All the germaria are shown at the same scale. Scale bar in A: 10 µm. SSCs, somatic stem cells.

View larger version (80K): [in a new window]   Fig. 4. wg signaling is not required for the proliferation of follicle cells on egg chambers. All egg chambers are labeled for lacZ (red), Hts (green) and nuclei (blue). The micrographs in A and B represent one confocal cross section of an egg chamber, whereas the micrograph in C is one confocal section along the surface of an egg chamber. Marked mutant follicle cell clones are identified by loss of lacZ expression (outlined in panels A-D). (A) A stage-8 egg chamber carrying marked mutant arm2 follicle cell clones. The arm2 mutant follicle cells have normal accumulation of Hts in lateral membranes. (B) A stage-6 egg chamber carrying mutant arm4 follicle cell clones in which Hts accumulates abnormally on apical membranes. In this egg chamber the oocyte is mislocalized to the anterior end because of a defect in DE-cadherin-mediated cell adhesion. However, the mutant follicle cell clones appear to have a normal size. (C) A stage-10 egg chamber showing a mutant dshVA135 follicle cell clone. The mutant clone appears to have a normal size and normal expression of Hts on lateral membranes. (D) A stage-9 egg chamber carrying twin follicle cell clones. The mutant dsh follicle cell clone, which is identified by loss of lacZ expression and highlighted by broken lines, appears to proliferate normally in comparison with the corresponding wild-type twin clone. The wild-type clone (highlighted by a solid line) carries two copies of the lacZ gene and thus shows stronger lacZ expression than the rest of lacZ-positive follicle cells (carrying one copy of the lacZ gene). The mutant clone appears to have a normal size and normal expression of Hts on lateral membranes. Scale bars: 10 µm.

View larger version (60K): [in a new window]   Fig. 5. Constitutive wg signaling causes follicle cell over-proliferation and abnormal accumulation of Hts protein on the membranes of follicle cells. All egg chambers and ovarioles are labeled for lacZ (red), Hts (green) and nuclei (blue). The micrographs in A-C represent one confocal cross section of an ovariole or an egg chamber, whereas the micrograph in D is one confocal section along the surface of an egg chamber. Marked mutant follicle cell clones are identified by loss of lacZ expression (outlined in A,C,D). (A) An ovariole showing abnormal accumulation of extra mutant Axn somatic cells (outlined) between egg chambers that also express higher levels of Hts than wild-type ones. (B) An ovariole carrying only marked mutant sggM1-1 follicle cells. Extra mutant sgg follicle cells accumulate abnormally between egg chambers and break germline cysts into small clusters (arrows). (C) Egg chambers with mutant Axn follicle cell clones that express higher levels of Hts (outlined). (D) A stage-8 egg chamber with a mutant sgg clone in which mutant follicle cells have abnormal morphology and higher levels of Hts expression. Scale bars: 10 µm.

View larger version (91K): [in a new window]   Fig. 6. Constitutive wg signaling blocks normal differentiation pathways of follicle cells. The micrograph in A represents a confocal section along the surface of an ovariole, whereas the rest are one confocal cross section of an egg chamber or an ovariole. (A,B) Parts of two ovarioles labeled for lacZ (red) and pH3 (green) showing marked mutant Axn follicle cell clones (outlined). (C,D) Parts of two ovarioles labeled for lacZ (red) and Lamin C (green), showing marked mutant Axn follicle cell clones (outlined) and normal (C, arrowhead) or mutant (D, arrowhead) Axn stalk cells. (E-J) Parts of ovarioles labeled for lacZ (red) and Fas3 (green) showing (E,G,I) marked mutant Axn (outlined) or (F,H,J) sgg follicle cell clones (outlined). The mutant Axn follicle cells between egg chambers express high levels of Fas3, but those that are integrated into egg follicle epithelium fail to express Fas3 at high levels. Arrows in I and J indicate wild-type polar cells. Scale bars: 10 µm.