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First published online 14 May 2008
doi: 10.1242/dev.014498

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Tracheal branching morphogenesis in Drosophila: new insights into cell behaviour and organ architecture

Biozentrum der Universität Basel, Klingelbergstrasse 70, CH-4056 Basel, Switzerland.

View larger version (78K): [in this window] [in a new window]   Fig. 1. Branching morphogenesis of the Drosophila tracheal system during embryonic development. Stills from time-lapse movies showing Drosophila embryos expressing either (A) His2AvD::mRFP ubiquitously or (B-D) GFP::Actin in the tracheal system (see Movie 1 in the supplementary material). (A) Stage 11 of embryonic development. Tracheal cells invaginate (arrowheads) and form tracheal sacs during the initial phase of germ band retraction. (B) Stage 12 of embryonic development. Tracheal sacs extend branches in stereotyped directions (asterisks). (C) Stage 14 of embryonic development. Tracheal branches elongate. (D) Stage 15 of embryonic development. Some branches are fusing to form an interconnected network of tracheal tubes (arrowheads). DBs, dorsal branches; DT, dorsal trunk; TCs, transverse connectives. Anterior is to the left and dorsal to the top. Scale bars: 100 µm.

View larger version (19K): [in this window] [in a new window]   Fig. 2. Tracheal cell invagination. (A) A transverse representation of tracheal placode invagination. Tracheal placodes are clusters of ectodermal cells that express trh (red). These cells stop dividing shortly before apical constriction occurs and before the tracheal placodes invaginate into the embryo. They then re-enter mitosis and undergo one last round of cell division towards the end of the invagination process. The orientation of the cell division axis is biased towards the center of the tracheal pit and might help to direct cells to flow into the site of invagination (Nishimura et al., 2007). (B) A model of the signaling and cell remodeling events required for ordered tracheal cell invagination. The patterning information from trh (red) is translated through cell signaling processes (green) and cytoskeleton reorganization (blue) to cell remodeling events (orange; see text for details). Dashed lines indicate effects eventually caused by a factor. Adapted, with permission, from Brodu and Casanova (Brodu and Casanova, 2006).

View larger version (91K): [in this window] [in a new window]   Fig. 3. Formation of a dorsal branch. Dorsal branch development from embryonic stage 12 to stage 15. Stills from a time-lapse movie showing an embryo expressing GFP::Actin in the tracheal system (see Movie 2 in the supplementary material). (A) A few tracheal cells at the tip of the tracheal bud (asterisk) form filopodial extensions under the control of FGF signalling. Tracheal cells in the dorsal branch stalk are initially paired (arrows), connecting the dorsal branch tip cells to the tracheal sac (dotted circle), and enclosing the dorsal branch lumen (arrowhead). (B) Gradually, as the dorsal branch elongates, the cells of the dorsal branch stalk adopt an end-to-end configuration (arrows). (C) In this image, stalk cells have fully intercalated (arrows). The terminal cell (TC) and the fusion cell (FC) continue to form filopodial extensions. Scale bars: 10 µm.

View larger version (13K): [in this window] [in a new window]   Fig. 4. Signalling via two receptor tyrosine kinases, Fgfr and Egfr, controls the directed outgrowth of the primordium of the dorsal air sac in the Drosophila larva. Fgf signalling (green), triggered by the presence of Bnl (blue) at the tip of the outgrowing air sac primordium, controls the direction of the outgrowth. Fgf signalling requires the Ras/MAPK cascade and Pointed (Pnt). Egf signalling is required more widely in the primordium, and regulates cell proliferation and cell death. Egf signalling does not require Pnt (for details, see Cabernard and Affolter, 2005).

View larger version (23K): [in this window] [in a new window]   Fig. 5. Genetic control of cell intercalation during branch outgrowth. A four-step model of cell intercalation in a dorsal branch stalk. See also text for details. (A-D) Four representative micrographs, visualizing the AJs using Cat::GFP expression in the tracheal system, are shown in parallel with (E) four sketches representing the same steps. (F) The proteins involved in the genetic control of this process. (A-E) To better understand the `topology' of the cells, the edges of two neighbour cells were colored in red and green, respectively. (A) Pairing: tracheal cells are in a side-by-side arrangement along the branch lumen. (B) Reaching around the lumen: individual cells establish contact with themselves and start to form the first autocellular AJs (arrowhead). (C) Zipping up: autocellular AJs extend as the two cells, which were initially paired, change their respective positions. (D) Termination: in order not to lose all intercellular AJs (and thus the adhesion between neighbouring cells), the transformation of intercellular AJs into autocellular AJs stops, with small intercellular AJ loops connecting adjacent cells to each other. Adapted, with permission, from Ribeiro et al. (Ribeiro et al., 2004). (F) The genetic control of these intercalation steps is beginning to be characterized. Proteins involved in this process are indicated with blue boxes.

View larger version (16K): [in this window] [in a new window]   Fig. 6. Sequential control of lumen expansion and lumen clearance in the Drosophila tracheal system. At stage 14 of embryonic development, chitin (red) coordinates the radial expansion of the lumen by forming, upon secretion, a transient fibrillar chitin-based matrix (red lines). These chitin cables are also required for the normal organization of the apical βH spectrin cytoskeleton (blue). At stage 16 of embryonic development, septate junction proteins are required for the apical secretion of Verm, which, together with Serp, is required for modifying the chitin matrix to prevent the tracheal tubes from becoming too long (Wang et al., 2006). At stage 17 of embryonic development, Wurst is essential for remodeling the chitin matrix and for clearing the tracheal airway.

View larger version (38K): [in this window] [in a new window]   Fig. 7. Similar functions of tip cells in the tracheal system and in the developing vasculature. (A) A terminal cell (TC) and a fusion cell (FC) of the Drosophila tracheal system, which form the tip of a dorsal branch and express GFP::Actin (stage 15 of embryonic development). Note the presence of filopodial extensions in the TC and the FC, and their absence in stalk cells (SCs). (B) An endothelial tip cell, expressing GFP in a developing intersegmental vessel of an early zebrafish embryo (image courtesy of Y. Blum). (C) Isolectin B4-labelled endothelial tip cell (green) at the leading front of the developing vasculature in the retina of a 5-day postnatal mouse. Nuclei are labelled with DAPI (blue; image courtesy of H. Gerhardt).

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