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First published online 7 July 2004
doi: 10.1242/dev.01254

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Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing

Department of Zoology, University of Wisconsin, 250 North Mills Street, Madison, WI 53706, USA

View larger version (73K): [in a new window]   Fig. 3. Wing hair polarity after patterned ds misexpression. (A-C) Diagrams of hair polarity (red arrows) in adult wings. Approximate regions of Gal4-driven gene misexpression are shown in green. (A) Wild type. Veins are labeled as in Fig. 1, with the addition of the posterior cross vein (PCV). (B,C) Gradients of ds misexpression commonly reorient hairs from regions of high to low expression. (B) UAS-ds/+; salgal4/+. (C) UAS-ds/+; dllgal4/+. (D-F) Hair polarity in a region just distal to the PCV. (D) Wild type. (E) UAS-ds/+; salgal4/+. (F) sal-gal4/+; UAS-fz-GFP/+ induces multiple wing hair phenotype (arrowheads). (G,H) Redistribution of Fz-GFP (green, white) by Ds (red) in sal-gal4/+; UAS-ds/+ wing at 26 hours AP; region shown is posterior to the PCV. The normally distal (right) Fz localization within each cell has frequently changed to the posterior (H, arrowheads).

View larger version (43K): [in a new window]   Fig. 1. Ds and Fj expression, and the signaling model. In this and subsequent figures anterior is up and proximal is to the left. (A,A') Anti-Ds staining (A, white; A', red) in wing at 5 hours AP. The primordia of longitudinal veins one through five (L1-L5) and the anterior cross vein (ACV) are shown in A' by the absence of anti-DSRF staining (green). (B) fj-lacZ (green) is expressed in the distal wing at 5 hours AP, in a region complementary to the region of high anti-Ds staining (red). (C) Expression levels of Ds and fj-lacZ at 5 hours AP. (D) ds-lacZ expression (red) and anti-Ds staining (white) in the ds05142/+ wing at 26 hours AP. Top panel is stained with anti-pMad (green) to identify the veins; lower panels show relative levels of Ds at indicated positions. Broad stripes of Ds expression extend out along the center of the wing, forming a proximal to distal gradient. (E) Signaling model. Ds on one cell binds to Ft on the adjacent cells and inhibits its activity; Fj inhibits this inhibition. Ft activity in the central cell is polarized by the higher levels of Ds and the lower levels of Fj on the proximal side. Polarized Ft activity biases the subsequent Fz signaling between cells, leading to the polarized distribution of proteins to the proximal (Pk, Vang) or distal (Dsh, Fz) faces of the cell, and to the formation of hairs on the distal faces.

View larger version (85K): [in a new window]   Fig. 6. Timed misexpression of Ds, induced in sal-gal4/tubgal80ts; UAS-ds/+ wings using temperature upshifts (induction) or downshifts (suppression). (A,B) Percentage of flies showing PCP defects. Dark gray indicates strong defects; light gray, weak defects. The relationship between the absolute age of the larvae or pupae and the developmental stage was altered by the different rearing temperatures, thus the approximate third instar stages are indicated. Flies reared continuously at 20°C did not show any adult PCP defects or ectopic anti-Ds staining in wing discs (C), whereas those reared continuously at 30°C showed strong hair reorientation (similar to that seen in Fig. 3B,E). (D-H) Anti-Ds staining in pupal wings. A temperature upshift at 0 hours AP induced scattered ectopic anti-Ds staining by 5 hours AP at 30°C (D, approximately equivalent to 6 hours AP at 25°C) and strong misexpression in the broad sal-gal4 pattern by 22 hours AP at 30°C (E, approximately equivalent to 24 hours AP at 25°C). A temperature downshift at 0 hours AP did not suppress ectopic anti-Ds staining by 5 hours AP at 20°C (F, approximately equivalent to 4 hours AP at 25°C) but did by 24 hours AP at 20°C (G, approximately equivalent to 17-19 hours AP at 25°C). The narrow stripe of Ds expression in G is also observed in wild-type wings at this stage (H), and differs in level and extent from that driven by sal-gal4 (E).

View larger version (134K): [in a new window]   Fig. 2. Interactions between Ds and Ft. (A) S2 cells transformed with gfp (green) alone do not adhere. (B) Cells co-transfected with ft and gfp do not adhere. (C) Cells cotransfected with ds, ft and gfp form large clusters (arrowheads). (D) The addition of 1 mM EGTA to cells co-transfected with ds, ft and gfp blocks adhesion. (E,F) Cells transformed with only ds (E) or ft (F) have only low levels of Ds or Ft on the cell surface. (G-J) Mixtures of cells separately transformed with ft (I, anti-Ft, red) and with ds and gfp (H, anti-Ds, blue; J, GFP, green) adhere. Adhering cells have higher levels of anti-Ds and anti-Ft staining at the interface between ds-expressing and ft-expressing cells (G-I, arrows), but low levels of anti-Ds staining at the interface between ds-expressing cells (G,H; arrowheads). (K-N) Changes in Ft or Ds stability and distribution induced by misexpression of ds or ft in late third instar wing discs. (K,L) Misexpression of ds in the posterior using en-gal4 (K) or in clones using FLPout-gal4 (L; identified by UAS-GFP, green) causes heightened anti-Ft staining at the cell surface. Wild-type cells at the interface with the ds-expressing clone (L) had a lower than normal anti-Ft staining, but staining was higher at the interface with the clone. (M,N) Misexpression of ft in the posterior using en-gal4 (M), or in clones using FLPout-gal4 (N; identified by UAS-GFP, green), causes heightened anti-Ds staining at the cell surface. Wild-type cells at the interface with the ft-expressing clone (N) had a lower than normal anti-Ds staining, but staining was higher at the interface with the clone. This was noted especially in clones in the prospective notum and wing hinge. Some ft-misexpressing filopodia or cell remnants extend from the clone (arrowheads) and have high levels of Ds.

View larger version (137K): [in a new window]   Fig. 4. Wing hair polarity in regions of uniform ds misexpression. (A-D) Diagrams of hair polarity in adult wings. (A) ds05142. (B) engal4/+; UAS-ds/+. Hair polarity is normal except near the boundary of misexpression. (C) tub-gal4/UAS-ds. Hair polarity is normal. (D) ds05142; tub-gal/UAS-ds. Hair polarity is rescued (compare with A), except in the proximal wing. (E,F) Comparison of anti-Ds staining in the proximal region of 5 hour AP wings in wild type (E) and tub-gal4/UAS-ds (F). Wings were stained in the same well and photos were taken using identical settings. (G-J) Comparison of hair polarity between ds05142 (G,I) and ds05142; tub-gal/UAS-ds (H,J) wings. Uniform ds expression rescues the PCP defect in the distal region between L3 and L4 (G,H), but not in the proximal region just posterior to L1 (I,J).

View larger version (70K): [in a new window]   Fig. 5. The Fj gradient plays only a minor role in PCP. (A-D) Hair polarity in adult wings. (A) ds05142 fjd1. Polarity is not appreciably worse than in ds05142 (see Fig. 4A). (B) UAS-ds/+; fjd1; tub-ga4/+ and (C) tub-gal4/UAS-ds UAS-fj. Polarity is normal, except in the proximal wing. (D,F) UAS-ds/+; fjd1 sal-gal4/fjd1. (E) UAS-ds; sal-gal4/+. (E,F) The hair polarity near the tip of L2 was abnormal in a fjd1 background (also compare D with Fig. 3B).

View larger version (139K): [in a new window]   Fig. 7. Wing hair polarity after ft and fj misexpression. (A-H) Hair polarity in adult wings. (A) UAS-ft/+; en-gal4/+. (B) Dorsal hairs in UAS-ft/+; ap-gal4/+. (C) UAS-ft/+; ptc-gal4/+. (D) sal-gal4/+; UAS-ft/+. (E) UAS-ft/+; ds05142 en-gal4/ds05142. (F) UAS-ft/+; fjd1 en-gal4/fjd1. (G) sal-gal4/+; UAS-fj/+. (H) fjd1 sal-gal4/fjd1; UAS-fj/+. (I-P) Examples of wing hair polarity. The regions shown are between distal L3 and L4 for I and K, posterior to the PCV for J, L, M and N, and between distal L4 and L5 for O and P. (I,J) en-gal4/+; UAS-ft/+. (K) UAS-ft/+; ptcgal4/+, (L) sal-gal4/+; UAS-ft/+. Hairs are often repolarized towards regions with higher ft expression (A,C,I,K, near the anteroposterior boundary), although exceptions are observed. Hairs near the PCV are repolarized within regions of uniform misexpression (A,B,J). (M) UAS-ft/+; ds05142 en-gal4/ds05142. Posterior polarity defects are decreased in the ds mutant background (compare with J), but are not eliminated; the polarity differs from that in the same region of the ds mutant (Fig. 4A). (N) UAS-ft/+; fjd1 en-gal4/fjd1. Posterior polarity defects are decreased by the loss of fj (compare with J). (O) sal-gal4/+; UAS-fj/+. (P) fjd1 sal-gal4/fjd1; UAS-fj/+. The hair polarity induced by fj misexpression was normal between L4 and L5 (O), but was altered in the fjd1 background (P). Hairs point towards regions with higher fj expression (H,P).

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