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doi: 10.1242/10.1242/dev.00313

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Apoptosis-mediated cell death within the ovarian polar cell lineage of Drosophila melanogaster

Florence Besse and Anne-Marie Pret*

Institut Jacques Monod, (UMR 7592 — CNRS/Université Pierre et Marie Curie/Université Denis Diderot), Laboratoire de Génétique du Développement et Evolution, 2-4, place Jussieu, 75251 Paris Cedex 05, France



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  		Fig. 1. Progressive definition of polar cell marker expression. A101/TM6 (A,B) and PZ80/Cy0 (C) ovarioles stained with anti-ß-galactosidase antibodies. Insets in A and C show magnification of indicated groups of 3 polar cell marker-expressing cells found in stage 2 to 4 egg chambers. B shows a group of 5 A101+ cells found in a stage 2 egg chamber.

 


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  		Fig. 2. Polyclonal origin of A101+ cells. hsp-flp/+; A101/Act>CD2>Gal4, UAS-GFP ovarioles stained with anti-ß-galactosidase (red/A101, A,B,D) or anti-Fas III antibodies (red, C), GFP (green, A-D), and DAPI (white, A-D). In A-D, yellow marks the superimposition of A101 or Fas III staining and GFP staining. (a1-d1) Magnifications of the boxed regions in A-D showing A101 (a1,b1,d1, red) or Fas III (c1, red) staining and GFP staining (green). (a2-d2) Magnifications of the boxed regions in A-D showing A101 (a2,b2,d2) or Fas III (c2) staining. As shown in c2, Fas III accumulates most strongly at the contact surface between the two polar cells of a given pair in late egg chambers. F III denotes Fas III.

 


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  		Fig. 3. Apoptosis-dependent elimination of supernumerary A101+ cells. (A) A101/TM6 ovariole triple-stained with DAPI (A, a1), anti-ß-galactosidase antibodies (red, A',a2,a3) and TUNEL (green, a2). (a1-a3) Magnification of the boxed region in A, A'. Arrows point to the dying A101+/TUNEL+ cell. (B) Wild-type ovariole triple-stained with DAPI (B), anti-Fas III antibodies (red, B') and TUNEL (green, B'). Arrowheads point to early germarial region 2b/3 Fas III+ somatic cells undergoing apoptosis. (C,D) hsp-flp/+; +/SM6; Act>CD2>Gal4, UAS-GFP/TM6 (C) and hsp-flp/+; +/UAS-p35; Act>CD2>Gal4, UAS-GFP/+ (D) stage 5-6 egg chambers double-stained for DAPI (C,D) and anti-Fas III antibodies (C',D'). (C') In a wild-type egg chamber, Fas III is expressed at a basal level in follicular cells, but is strongly expressed in pairs of polar cells. Six anterior Fas III+ polar cells are present in D'. All follicular cells of the ovarioles in C and D exhibited GFP staining (data not shown). (E,E') UAS-p35/neuP72-Gal4; UAS-Histone YFP/+ stage 6 egg chamber triple-stained with DAPI (E), anti-Fas III antibodies (red, E') and YFP (green, E'). Four Fas III+ polar cells are present posteriorly in E'. (F,F') UAS-p35/+; neuP72-Gal4/rpr-lacZ egg chamber triple-stained with DAPI (F), anti-Fas III (red, F') and anti-ß-galactosidase (green, F') antibodies. Among the 4 Fas III+ cells present anteriorly (F', boxed area and close up in inset), 2 also exhibit reaper-lacZ expression (boxed area). FIII denotes Fas III and rpr denotes reaper-lacZ.

 


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  		Fig. 4. Polar cell differentiation is delayed in fused mutant females. (A,B) fuJB3; A101/+ ovarioles double stained with DAPI (A,B) and anti-ß-galactosidase antibodies (A',B'). Higher magnification of two groups of three A101+ cells (inset A') and two groups of 5 and 6 A101+ cells (left and right, respectively, inset B') are shown. The A101 enhancer-trap line was used to visualize polar cells since introduction of this insertion in a fu mutant context does not modify fu ovarian phenotypes. (C) Percentage of fuJB3/FM6 (blue) and fuJB3 (pink) stage 1 to 5 egg chambers containing 0, 1, 2, 3 or 4 and more polar cells (n>=23 for each stage). Note that reported data are of anterior polar cells.

 


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  		Fig. 5. Egg chambers with extra polar cells exhibit late defects in anterior somatic cell morphogenesis. (A,B) Control (A) and hsp-flp/+; +/UAS-p35; Act>CD2>Gal4, UAS-GFP/+ (B) egg chambers double-stained with phalloidin (green) and anti-Fas III antibodies (red). Magnification of the basal follicular epithelium (insets, bottom-left) and the anterior polar cells (insets, top-right) are shown. The bright fringe-like structure visible in B (bottom-right) are the remnants of the external sheath. (C-F) Control (C-C'',E,E'), and hsp-flp/+; +/UAS-p35; Act>CD2>Gal4, UAS-GFP/+ (D-D'',F,F') ovarioles triple-stained with DAPI (C,D,E,F), phalloidin (C',C'',D',D''E',F', green) and anti-Fas III (C',C'',D',D'',E',F', red). Magnification of stage 9 anterior polar cells and the adjacent follicular epithelium (insets, C'',D''), and of stage 10 border cells and polar cells (insets, E,F and E',F', respectively) are shown. Four and 5 polar cells are found anteriorly in D'' and F', respectively.

 


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  		Fig. 6. Proposed polar cell lineage. Given that polar cells and stalk cells have been shown to have common precursors, we propose the existence of at least 3 stalk and polar cell precursors (white circles, first row) for each polar cell pair and neighboring stalk cells. The stalk cells considered are not necessarily those immediately adjacent to the polar cell pair since intercalation events disperse the cells giving rise to an interfollicular stalk. Such precursors would first generate groups of pre-polar (pink circles) and pre-stalk (blue circles) cells. Divergence between pre-stalk and pre-polar cells could occur either in the course of stalk cell/polar cell precursor divisions (1, arrow), or after completion of divisions (2, arrow). A subsequent step involving apotosis-mediated selection of the final polar cell pair (red) would then take place among groups of up to 6 pre-polar cells (indicated by Xs in boxed area). Although we do not have any evidence yet for the existence of a selection process among pre-stalk cells, such a mechanism could also be part of the stalk cell maturation program (X ? in boxed area).

 

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