JAK-STAT pathway in Drosophila morphogenesis: From organ selector to cell behavior regulator

Abstract

One of the main contributions of Drosophila to the JAK-STAT field is the study of morphogenesis. JAK-STAT signaling controls the formation of many different structures through surprisingly different morphogenetic behaviors that include induction of cell rearrangements, invagination, folding of tissues, modulation of cell shape, and migration. This variability may be explained by the many transcription factors and signaling molecules STAT regulates at early stages of development. But is STAT just acting as an upstream inducer of morphogenesis or does it have a more direct role in controlling cell behaviors? Here we review what is known about how the canonical phosphorylation of STAT contributes to shaping the embryonic and imaginal structures.

Keywords: Drosophila; JAK; STAT; development; morphogenesis; organogenesis; signaling.

Figure 1.upd expression and JAK-STAT pathway activation during embryogenesis. Embryonic upd RNA expression (A–F) and activity of the ×STAT-GFP reporter at comparable stages (G–L). upd has a very dynamic pattern of expression ranging from a striped pattern at st9 (A) that develops a transient anterior-posterior stripe ([B], arrows), and then restricts to organ primordia (C–F). Note the similarity of the upd expression and the ×STAT-GFP reporter patterns. Anterior is left and dorsal up except in (D and J), which show dorsal views. asp, anterior spiracle; psp, posterior spiracle; tr, trachea; si, small intestine; ph, pharynx.

Figure 2. JAK-STAT function during embryonic gut development. Schematic representation of the embryonic foregut (A) and hindgut (E) and their localization at different embryonic stages (B–D). In the schemes, upd expression is shadowed in blue. Expression of upd transcripts in embryos at st11 (B), st13 (C), and st14 (D). In (B–D) red lines mark the position of the foregut and yellow lines of the hindgut. (A) upd expression is restricted to a group of ectoderm cells from where it diffuses to control the proventriculus folding (the enveloping visceral mesoderm is labeled in red). (E) In the hindgut, upd expression is restricted to the small intestine from where it coordinates the cell rearrangements and gut bending (blue, small intestine; orange, large intestine; light green, rectum).

Figure 3. JAK-STAT activity in imaginal discs. Activation of the pathway visualized using the ×STAT-GFP reporter in the wing disc (left disc in [A]) and eye-antennal disc (B). (A and B) Color images show the imaginal discs stained for GFP (green), aPKC (red), and Discs large (blue). The corresponding GFP single channel image by its side shows schematically the extent of GFP (green line) and the approximate expression patterns of Dpp (blue lines), Odd (orange line), and Wingless (red lines). The localization of the wing blade is highlighted by a yellow line. Wingless expression in the wing blade and hinge is omitted. (C) Schematic representation of JAK-STAT functions at different larval stages and imaginal discs. w, wing; h, haltere; LII, mesothorathic leg; e, eye; a, antenna. Asterisk in (A) marks the hinge region. ×STAT-GFP reporter expression in the leg disc has been omitted since it does not correctly recapitulate JAK-STAT activation.