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doi: 10.1242/10.1242/dev.00420

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Bazooka is a permissive factor for the invasive behavior of discs large tumor cells in Drosophila ovarian follicular epithelia

¹ Max Delbrück Center for Molecular Medicine (MDC) Berlin-Buch, Robert-Rössle Strasse 10, D-13125 Berlin-Buch, Germany
² Howard Hughes Medical Institute, Departments of Physiology and Biochemistry, University of California, 533 Parnassus Avenue, San Francisco, CA 94143-0725, USA

View larger version (33K): [in a new window]   Fig. 1. Schematic summary of border cell migration. (A) Border cells are specified within the anterior follicular epithelium that surrounds the germline. The two anterior polar cells and several neighboring follicle cells undergo an epithelial-to-mesenchymal transition, intrude between the germline nurse cells and (B) migrate towards the oocyte at the posterior of the egg chamber. (B') Within the migrating border cell cluster, the two central polar cells (previously the anterior polar cells) are carried along by the migratory rosette cells that surround them.

View larger version (132K): [in a new window]   Fig. 2. Loss of cell polarity in DaPKCk06403 and bazEH171 mutant follicle cells. (A) DaPKCk06403 mutant follicle cells stained for Baz (red) which is mislocalized. (B) Within bazEH171 mutant follicle cells, DaPKC (red) is mislocalized. (C) DaPKCk06403 mutant follicle cells stained for Dlg, which is mislocalized throughout the entire membrane. (D,E) bazEH171 mutant follicle cells stained for Dlg, which is mislocalized throughout the entire membrane (D) and Arm, which is mislocalized to ectopic foci (E). (F) DaPKCk06403 mutant follicle cells stained for DE-cadherin, which is present in ectopic foci (F). In lateral positions, the polarity defects are stronger in the absence of germline DaPKC (left arrow: egg chamber with wild-type germline; right arrow: egg chamber with DaPKCk06403 mutant germline). (G,H) dlgm52 mutant follicle cells stained for Baz display ectopic foci of Baz. Arrowhead indicates wild-type GFP-positive follicle cells; arrows show mutant GFP-negative follicle cells. fc, follicle cells; nc, nurse cells.

View larger version (117K): [in a new window]   Fig. 3. DaPKCk06403 and bazEH171 mutant follicle cells are multi-layered. (A) Wild-type follicle cell epithelium is mono-layered. (B) DaPKCk06403 and (C) lgl4 mutant follicle cells are multi-layered. (D) bazEH171 mutant follicle cell clone is multi-layered (arrow). (E,F) Lateral views of the wild-type and DaPKCk06403 follicle cell epithelium. Density of nuclei is higher in the wild-type epithelium (E) indicating that mispositioning of cells occurs in the lateral DaPKCk06403 mutant follicle cell epithelium (F). Nuclear staining with propidium iodide and GFP clonal marker for wild-type cells (absence of GFP expression indicates mutant follicle cells). fc, follicle cells; nc, nurse cells; o, oocyte.

View larger version (70K): [in a new window]   Fig. 4. dlg mutant follicle cell invasion requires Baz. (A-C) dlgm52 mutant follicle cells cause a rough germline boundary (A, arrow), or are invasive (B,C). Occasionally, wild-type cells are recruited into the streams of invading follicle cells (C, white bracket). (D) lgl4 mutant follicle cells can be invasive (arrow). (E,F) dlgm52 bazEH171 mutant follicle cells are not invasive but can cause a rough germline boundary (E, arrow). Nuclear staining with propidium iodide and GFP clonal marker for wild-type cells (absence of GFP expression indicates mutant follicle cells). fc, follicle cells; nc, nurse cells.

View larger version (107K): [in a new window]   Fig. 5. Baz and DaPKC protein localization within the border cell cluster. (A-F) Late stage 8 and early stage 9 egg chambers stained for DaPKC (A-D) and Baz (E,F). Asterisk indicates central follicle cell prior to invasion (A). Both proteins localize to leading extensions of rosette cells during migration (arrows C-E). (G,H) Within the migrating border cell cluster, DaPKC and Baz strongly localize to the outer surfaces of the rosette cells, facing germline cells. (I-K) Confocal sections through the apical ring between the two central cells, I and J are apical sections, K is a more basal section. Prior to the rosette cells reaching the oocyte, DaPKC, Baz and DE-cadherin overlap on the membranes between rosette cells and in an apical ring between the two central cells. (L) When the cells reach the oocyte (dotted line) Baz localizes to the apical attachment side. (M,N) DaPKC and Baz localize to the apical attachment side between border cells and oocyte (dotted lines) as border cells migrate dorsally. In all panels posterior is to the right.

View larger version (108K): [in a new window]   Fig. 6. Role of baz and DaPKC in border cell migration. (A,B) Egg chambers stained with FasIII. Polar cell induction is not dependent on DaPKC (arrow). (C-F,H) Migrating border cell clusters stained for S1bo (blue) and FasIII (red). (G,J) Border cell cluster stained for S1bo (blue). (I) Border cell cluster stained for DaPKC (sequence of several confocal z-sections). (D-I) bazEH171 mutant border cells (asterisks) are found in leading positions (D,E), trailing behind wild-type cells within the migrating cluster (F,G,I), or in central positions (H). Long FasIII-positive extension can be seen between bazEH171 mutant central polar cells (F, arrow). (I'') Wild-type cells within the cluster are marked with a plus. (J) DaPKCk06403 mutant rosette cells (asterisks) migrate properly to the oocyte (dotted line) and adhesion between border cells is not affected. GFP clonal marker for wild-type cells (absence of GFP expression indicates mutant follicle or border cells). In all panels posterior is to the right.

View larger version (24K): [in a new window]   Fig. 7. Model of baz-dependent interactions between follicle and germline cells. (A) In wild-type, Baz (asterisks) localizes to the apical follicle cell membranes that are in contact with the germline nurse cell membranes and to the entire nurse cell membranes. Within the nurse cell membranes, Baz and Dlg have an overlapping localization pattern. In contrast, follicle cell Dlg localizes only to the basolateral membranes (rectangles). (B) Within invasive dlg mutant follicle cells, Baz functions as a permissive factor that is present along ectopic membrane sites and stabilizes, via baz-dependent interactions, the contacts with nurse cells. (C) dlg baz double mutant follicle cells lack invasive behavior. In the absence of follicle cell Baz, nurse cell Baz enhances germ cell adhesion thereby repressing follicle cell invasion. (D) The repression of baz-deficient follicle cell invasion is released in the absence of nurse cell Baz, possibly due to a reduction of nurse cell adhesion. The cellular machinery underlying this type of follicle cell invasion remains to be identified (X, unknown molecular player mediating cell invasion).

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