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First published online 25 August 2004
doi: 10.1242/dev.01351

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Cell interactions and planar polarity in the abdominal epidermis of Drosophila

¹ MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK
² Howard Hughes Medical Institute, Columbia University College of Physicians and Surgeons, 701 West 168th Street, New York, NY 10032, USA

View larger version (55K): [in a new window]   Fig. 1. Summary model and results. (A) Pattern formation in the abdomen. Two segments are shown, each with an A and a P (blue) compartment stratified into different types of cuticle (shown at bottom of the panel). The Hh and Wg gradients pattern the cuticle (Struhl et al., 1997b; Lawrence et al., 2002). The gradient of `X' may have opposing slopes in A and P; its vector determines the orientation of the hairs in A (up the gradient) and P (down the gradient) as shown by the arrows. Anterior is to the left. (B) A field guide to the main results; the genotypes of clones are shown inside the ellipses. Genotype symbols outside the clone, say, fz–, indicate the genetic background in which the clone was induced (fz–). Red arrows mark where polarity is reversed or normalised. Anterior is up.

View larger version (86K): [in a new window]   Fig. 2. Clones involving fz. (A) Two fz– clones in the pleura (marked with tricornered, which makes each cell form a cluster of variously pointing hairs; genotype 2). Here and in most other figures, anterior is up and clones are outlined in red. Note the reversal of polarity (red arrows) for several rows of cells, behind the clones. (B) A UAS.fz clone reverses in front (genotype 3). This clone, stained in blue, consists of cells at the anterior limit of the P compartment. Repolarisation includes the front part of the clone and extends well into the A compartment (red arrow). Clones made with other drivers show similar phenotypes (genotypes 4 and 5). Note that here and in other figures the orientation of bristles is inconstant; this is an artefact caused by the need to flatten the preparations when mounting. (C) A UAS.fz clone (marked with pawn, which makes the hairs more tenuous and the bristles stunted) in a fz– fly (genotype 6). The background fz– territory has dishevelled hair polarity (compare with the left edge of A to see the wild-type pattern), and the clone imposes normal polarity for about one cell behind and reversed polarity for about one cell in front (red arrows).

View larger version (94K): [in a new window]   Fig. 3. Providing Fz locally to fz– territory. en.Gal4 driving UAS.fz in fz– flies provides a band of Fz expression in the P compartment (genotype 8). This appears to have two effects: 1. The interface at the front causes a reversal of polarity around that interface that extends one cell into the fz– territory but more cells into the P compartment. 2. The remainder of the P compartment is rescued, with the rescue extending one cell into the fz– territory behind. Overall, we see a band of order imposed on the disorder seen in the majority of the A compartment. The detail on the right shows the two zones of organised polarity and our estimate of where the P compartment is (estimated from clones, and from other experiments where UAS.fz is driven by hh.Gal4 in flies carrying ptc.lacZ).

View larger version (145K): [in a new window]   Fig. 4. Clones involving prickle (pk). (A) Part of the pleura of a fly lacking pk and stained for hh.lacZ to demarcate the P compartments (genotype 11). Note the alternating zones of polarity, with much of the back half of the A compartment having reversed hairs (red arrows). (B,B') Uniform overexpression of sple gives zones of reversed polarity coinciding more or less with the P compartments (genotype 12). P compartments of the first and second abdominal segments are shown, with a magnified view of part of the second (B'). Anterior to left. (C) A clone lacking pk (marked with shavenoid which removes most of the hairs). The hair orientation within the clone is whorly (genotype 24). (D) A clone expressing sple in the P compartment. Most of the cells in the clone, and some cells behind, have reversed polarity. The front of the clone displays normal polarity (genotype 25). (E) Two clones lacking fz, marked with tricornered in a pk– fly (genotype 19). Note that, in spite of the varying zones of polarity in the background, the hairs point consistently into the clones. Phase image, clone outlines were ratified in a DIC image (not shown). (F-H) Expressing fz in the P compartment causes a zone of reversed polarity across the A/P border of wild type (F, genotype 9) and also pk– flies (G, genotype 20). Note that in pk– flies polarity is normal in that region (H, genotype 21).

View larger version (168K): [in a new window]   Fig. 5. Clones involving Vang. (A) Vang– clone in anterior tergites marked with pawn. Note that the rows of hairs in the clones are disordered and the orientation is disturbed (genotype 28). Anterior to the clone, there is some reversal of hair polarity (yellow arrowheads). (B) This clone carries only the pawn marker and can be compared with A (genotype 30). Note that the rows of hairs are well ordered and the polarity normal (blue arrowheads). (C) Vang– clone (marked with pawn) in the pleura. Hairs in the clone are dishevelled, but the hairs in front are reversed in polarity (genotype 28). (D) A clone expressing Vang (marked with pawn) showing slight disarray inside the clone, and the reversal of polarity of the hairs behind (yellow arrowheads, genotype 31). (E) A clone expressing Vang (marked with multiple wing hairs, in which every cell has multiple hairs that point in all directions), in a Vang– fly. Note that the background hairs are higgledy-piggledy in orientation, but, unlike in D, they are not affected by the clone (genotype 32). (F) A clone expressing Vang (marked with pawn), in a fz– fly. Note that the hairs in front of the clone are dishevelled because fz– affects that region of the A compartment, but behind they are normal, and, unlike in Fig. 5D, they are unaltered by the clone (blue arrowheads, genotype 36).

View larger version (101K): [in a new window]   Fig. 6. Clones involving starry night (stan). (A) stan– clones marked with pawn; inside the clones the polarity is dishevelled but there are no consistent effects on neighbouring cells outside the clone (genotype 45). (B) A stan– clone expressing fz marked with pawn, note the dishevelled rows and orientation of hairs inside the clone but the lack of effect on polarity outside the clone (blue arrowheads, genotype 46). Compare with (C) a stan+ clone overexpressing fz; the clonal hairs are well-ordered but there is reversed polarity within the front and anterior to the clone (yellow arrowheads, genotype 4). (D) Part of a clone overexpressing stan marked with pawn in the pleura, note the substantial reversal at the back of the clone and behind (red arrow, genotype 50). (E) Two stan– clones expressing Vang marked with pawn; note the disarray in the clones and the lack of reversal behind them (blue arrowheads, genotype 51). Compare with Fig. 5D. (F) Clones overexpressing stan in a fz– background fail to repolarise behind (blue arrowheads, genotype 52).

View larger version (46K): [in a new window]   Fig. 7. The averaging model. (A) Imagine a gradient of Fz activity from 1000 downwards (see top diagram, upper row). A cell takes into account both its position, given to it by the scalar of an X gradient, but also the scalars of its neighbours. After five iterations (lower row) the gradient does not change (see supplementary material). (B) However, now introduce a fz– clone of five cells across with an activity level of 0. At the edge of a clone, a cell (say, at level 930) now finds itself between a fz– cell (with level 0) and its normal neighbour (level 920). After the same five iterations (lower row), the values of several of the fz+ cells have changed and, consequently, the scalars, the vectors and the polarity as shown. Red indicates a cell whose polarity has been reversed (a=0.75, see supplementary material). (C) A simple but speculative model of the functional interactions. This model is based on our results and helps explain them. Using Stan, each cell compares the Fz activity of adjoining cells, forming hairs that point towards the neighbour with the lowest activity. The top row shows the normal epithelium, with an activity gradient of Fz (increased activities are indicated by larger fonts). The cadherin Stan bridges from cell to cell and activates Vang. This activation is repressed by Fz activity. Within the cell, Vang, a membrane protein, represses Fz. Consider any three consecutive cells. High Fz activity in cell 1 inhibits Stan in the same cell, an effect which passes across the Stan-Stan bridge to repress Stan in cell 2, thus reducing Vang activation and increasing Fz activity in cell 2. This effect on Fz activity is counterbalanced by cell 3, which has itself lower Fz activity and hence higher Stan activity; this propagates back, via the Stan-Stan bridge, to enhance Stan activity on the opposite surface of cell 2, thus enhancing Vang activation and reducing Fz activity in cell 2. The whole field is subject to the X gradient which limits the tendency of Fz activity to rise. The effects of stan–, fz– and Vang– clones are shown in the bottom three rows.