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First published online August 3, 2005
doi: 10.1242/10.1242/jcs.02464

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Signaling interactions between squamous and columnar epithelia of the Drosophila wing disc

Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad, 500 007 India

View larger version (102K): [in a new window]   Fig. 1. Morphological features of peripodial and disc proper cells. (A) Thin squamous peripodial cells overlaying long columnar disc proper cells. (B) A top view of peripodial membrane of a wild-type wing disc stained for Armadillo expression. Left: large PM cells, which normally overlay the pouch and the notum. Right: an optical section at a lower focal plane showing medial edge (arrows) cells normally found on the lateral sides. These cells are more elongated than the PM cells overlaying the pouch and the notum.

View larger version (59K): [in a new window]   Fig. 2. Peripodial cells exhibit apical-basal polarity and their apical surfaces face the apical side of disc proper cells. (A1,A2) Two representative optical sections of peripodial cells of a wild-type wing disc stained for ARM (red) and DLG (green). The plane of focus in A1 is the top surface (away from the disc proper cells) and A2 is at a lower surface than the A1 (more towards the disc proper cells) of PM cells. Note staining for DLG is stronger in A1 (arrows) and that for ARM is stronger in A2 (arrows), suggesting that peripodial cells have their apical side towards the disc proper. (B-D) Cross-section along the Z-axis of wild-type wing discs stained for rhodamine conjugated phalloidin (which binds F-actin) and DLG (B), ARM and FAS (C) or ARM and DLG (D). Actin marks the apical side, ARM marks subapical side, and DLG and FAS mark lateral and basal sides. Note that regions of intense actin or ARM staining in PM cells face the corresponding regions of DP cells (B-D). (E) Proposed model of organization of peripodial and disc proper cells, with respect to their apical (a) -basal (b) polarities. Only a small section of wing disc is shown here. PM cells are shown in red and DP cells are in green. The apical sides of PM and DP cells are shown in patterned red and green lines, respectively.

View larger version (97K): [in a new window]   Fig. 3. Overexpression of Delta in the peripodial cells induces WG expression in the wing pouch. (A,B) Wild-type wing discs showing the expression pattern of WG (A). WG is expressed only in DP cells. (B) Wing disc of a Ubx-GAL4/UAS-lacZ larva stained for lacZ (red) and WG (green). Note that lacZ, and therefore Ubx-GAL4, is expressed only in peripodial cells. (C) Wing disc of a Ubx-GAL4/UAS-Delta larva stained for WG (green) and UBX (red). Note ectopic activation of WG all over the pouch and the resultant overgrowth phenotype. No such ectopic activation of WG is observed in the notum region of the disc proper, nor was there any notum-to-wing transformation normally associated with ectopic WG. Also note that peripodial cells (even the medial edge or margin peripodial cells) themselves do not express WG in response to ectopic Delta. (D,E) Wing disc of a Ubx-GAL4/UAS-Delta larva stained for ARM. The focal plane in D is at the level of wing pouch and medial edge cells of PM. Both DP and medial edge cells are normal. In E, only PM cells are shown at higher magnification. Note that PM cells are more elongated and densely arranged than in wild-type (Fig. 1B). It is possible that Dl-induced overgrowth in DP cells may have stretched PM and hence changes in cell morphology. Nevertheless, the identity of PM cells is still maintained as they continue to express UBX and do not express WG.

View larger version (128K): [in a new window]   Fig. 4. Anterior-posterior patterning in the peripodial membrane. (A,A') Wild-type wing disc stained for UBX (red) and EN (green) expression. All UBX-expressing PM cells express EN. (B,C) Wild-type wing discs stained for hh-lacZ (green) and UBX (red) expression (B) or for HH protein (green) and UBX (red) expression (C). HH expression is not detectable in PM cells. (D) Wild-type wing disc stained for CI (green) and UBX (red) expression. CI too is not expressed in PM cells. (E) dpp-lacZ wing disc stained for lacZ (green) and UBX (red). DPP is expressed in a subset of PM cells, overlaying the anterior compartment of DP. (F) Wing disc of the genotype dpp-lacZ; Ubx-GAL4/UAS-CI stained for lacZ (green) and UBX (red). Note ectopic activation of DPP in all cells overexpressing CI. (G) Wild-type wing disc stained for PTC (green) and UBX (red) expression. In DP, PTC is expressed in the anterior compartment with A/P boundary expressing the highest levels, whereas it is not detected in PM cells. (H) Wing disc of the genotype dpp-lacZ; Ubx-GAL4/UAS-PTC stained for lacZ. DPP expression in PM cells is not affected by ectopic PTC. (I) 426-GAL4/UAS-nuclear lacZ wing disc showing expression pattern of 426-GAL4 driver. It is not expressed in PM cells. (J,J') Wing disc of the genotype dpp-lacZ; 426-GAL4/UAS-HH stained for lacZ (green) and UBX (red). Note ectopic DPP in the anterior compartment of DP. No such ectopic DPP is observed in PM cells.

View larger version (78K): [in a new window]   Fig. 5. Signaling by HH is dependent on cell-cell contacts, and HH does not diffuse through trans-membrane extensions that bridge peripodial and disc proper cells of the notum. Discs in A, B, E-G are stained for dpp-lacZ (green) along with either UBX or WG (red) as shown on individual images. Discs in C and D are stained for pMAD. (A,C) Expression pattern of dpp-lacZ (A) and pMAD (C) in wild-type background. (B,D-E) Wing disc (of the genotype dpp-lacZ; Ubx-GAL4/UAS-HH), wherein wild-type HH is overexpressed in the peripodial cells. Note ectopic DPP expression, which is restricted to the anterior compartment of the pouch region (B). As a consequence, these discs show increased levels of pMAD in the entire anterior wing pouch (D). No DPP and pMAD activation or much less DPP and pMAD activation is observed in the notum, which is connected to the peripodial membrane through long microtubule-membrane extensions. (F) Wing disc (of the genotype dpp-lacZ; Ubx-GAL4/UAS-HH-N), wherein the cholesterol-unmodified form of HH is overexpressed in the peripodial cells. This form of HH does not have cholesterol moiety and therefore diffuses freely in the extracellular space. Note activation of DPP in the anterior compartments of both the pouch and the notum. (G) Wing disc (of the genotype dpp-lacZ; Ubx-GAL4/UAS-CD2::HH), wherein the membrane-tethered form of HH is overexpressed in the peripodial cells. Note that similar to wild-type HH, membrane-tethered HH is capable of inducing the activation of DPP only in the anterior compartment of the pouch region. All the three forms of HH caused considerable overgrowth in the anterior pouch. In addition to the pouch, HH-N caused overgrowth phenotype in the notum. However, all the three forms of HH failed to activate DPP in the peripodial membrane itself. None of the three HH forms affected WG expression in either the pouch or the notum.

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