Genetic control of epithelial tube fusion during Drosophila tracheal development (original) (raw)
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Genetic Control of Cell Intercalation during Tracheal Morphogenesis in Drosophila
Current Biology, 2004
Klingelbergstrasse 70 into a coordinated response [1]. Epithelial sheets are often remodeled into tubular net-CH-4056 Basel Switzerland works, allowing for an efficient exchange of fluids or gases with surrounding tissues [2, 3]. A particularly wellstudied example of such a remodeling process occurs during the development of the tracheal system in the Summary Drosophila embryo [4, 5]. The larval tracheal system consists of hundreds of interconnected tubes that trans-Background: Branching morphogenesis transforms an port oxygen and other gases throughout the body. Traepithelial sheet into a tubular network with distinct feacheal branches are simple tubes consisting of an epithetures regarding the length and diameter of individual lial monolayer wrapped around a central lumen. The tubes. Branching is controlled by several signaling pathdevelopment of the trachea is initiated in the early emways, but the molecular consequences of these pathbryo upon the determination of ten bilaterally symmetriways in the responding cells are poorly understood. cal clusters of approximately 80 tracheal precursor cells. Results: We have undertaken a detailed characteriza-Each cluster, called a tracheal placode, subsequently tion of cell rearrangements during tracheal branching undergoes a similar sequence of developmental events morphogenesis in Drosophila embryos with a GFP futo generate one segment of the network in the absence sion protein labeling the adherens junctions (AJs) and of further cell divisions.
Compensatory branching morphogenesis in the Drosophila tracheal system
2015
Compensatory Branching Morphogenesis in the Drosophila Tracheal System Deanne Francis Amin Ghabrial Most organs and glands are composed of interconnected networks of tubes. Tubes carryout many important functions throughout the body, such as homeostasis, nutrient and oxygen transport. Surprisingly, given the importance of interconnected tubular networks, how connections between different tubes are maintained remains undetermined. To address this question we used the Drosophila tracheal system as a model to study tube connectivity. The Drosophila trachea is composed of multi-cellular, auto-cellular and seamless tubes. Multi-cellular tubes are composed of multiple interconnected cells, auto-cellular tubes form by wrapping and membrane self-adhesion, while seamless tubes form entirely intracellularly. In all epithelial tube types, the cell apical domain faces the lumen. In this work, I focused on the connection between the auto-cellular tube in the stalk cell and the seamless tube in t...
Echinoid regulates tracheal morphology and fusion cell fate in Drosophila
Developmental Dynamics, 2010
Morphogenesis of the Drosophila embryonic trachea involves a stereotyped pattern of epithelial tube branching and fusion. Here, we report unexpected phenotypes resulting from maternal and zygotic (M/Z) loss of the homophilic cell adhesion molecule Echinoid (Ed), as well as the subcellular localization of Ed in the trachea. ed M/Z embryos have convoluted trachea reminiscent of septate junction (SJ) and luminal matrix mutants. However, Ed does not localize to SJs, and ed M/Z embryos have intact SJs and show normal luminal accumulation of the matrix-modifying protein Vermiform. Surprisingly, tracheal length is not increased in ed M/Z mutants, but a previously undescribed combination of reduced intersegmental spacing and deep epidermal grooves produces a convoluted tracheal phenotype. In addition, ed M/Z mutants have unique fusion defects involving supernumerary fusion cells, ectopic fusion events and atypical branch breaks. Tracheal-specific expression of Ed rescues these fusion defects, indicating that Ed acts in trachea to control fusion cell fate.
Mechanisms of Development, 2000
The Drosophila tracheal system arises from clusters of ectodermal cells that invaginate and migrate to originate a network of epithelial tubes. Genetic analyses have identi®ed several genes that are speci®cally expressed in the tracheal cells and are required for tracheal development. Among them, trachealess (trh) is able to induce ectopic tracheal pits and therefore it has been suggested that it would act as an inducer of tracheal cell fates; however, this capacity appears to be spatially restricted. Here we analyze the expression of the tracheal speci®c genes in the early steps of tracheal development and their cross-interactions. We ®nd that there is a set of primary genes including trh and ventral veinless (vvl) whose expression does not depend on any other tracheal gene and a set of downstream genes whose expression requires different combinations of the primary genes. We also ®nd that the combined expression of primary genes is suf®cient to induce some downstream genes but not others. These results indicate that there is not a single master gene responsible for the appropriate expression of the tracheal genes and support a model where tracheal cell fates are induced by the co-operation of several factors rather than by the activity of a single tracheal inducer. q
Genetic control of epithelial tube size in the Drosophila tracheal system
Development (Cambridge, England), 2000
The proper size of epithelial tubes is critical for the function of the lung, kidney, vascular system and other organs, but the genetic and cellular mechanisms that control epithelial tube size are unknown. We investigated tube size control in the embryonic and larval tracheal (respiratory) system of Drosophila. A morphometric analysis showed that primary tracheal branches have characteristic sizes that undergo programmed changes during development. Branches grow at different rates and their diameters and lengths are regulated independently: tube length increases gradually throughout development, whereas tube diameter increases abruptly at discrete times in development. Cellular analysis and manipulation of tracheal cell number using cell-cycle mutations demonstrated that tube size is not dictated by the specific number or shape of the tracheal cells that constitute it. Rather, tube size appears to be controlled by coordinately regulating the apical (lumenal) surface of tracheal cel...
Current Biology, 2006
The development of the complex network of epithelial tubes that ultimately forms the Drosophila tracheal system relies on cell migration, cell shape changes, cell rearrangements, cell differentiation, and branch fusion . Most of these events are controlled by a combination of distinct transcription factors and cell-cell signaling molecules, but few proteins that do not fall within these two functional classes have been associated with tracheal development. We show that the MAGUK protein Polychaetoid (Pyd/ZO-1), the Drosophila homolog of the junctional protein ZO-1 [4], plays a dual role in the formation of tracheal tubes. pyd/ZO-1 mutant embryos display branch fusion defects due to the lack of reliable determination of the fusion cell fate. In addition, pyd/ZO-1 mutant embryos show impaired cell intercalation in thin tracheal branches. Pyd/ZO-1 localizes to the adherens junctions (AJs) in tracheal cells and might thus play a direct role in the regulation of the dynamic state of the AJ during epithelial remodeling. Our study suggests that MAGUK proteins might play important roles during AJ remodeling in epithelial morphogenesis.
Genetics, 2009
Insulin-like growth factors (IGFs) control cell and organism growth through evolutionarily conserved signaling pathways. The mammalian acid-labile subunit (ALS) is a secreted protein that complexes with IGFs to modulate their activity. Recent work has shown that a Drosophila homolog of ALS, dALS, can also complex with and modulate the activity of a Drosophila IGF. Here we report the first mutations in the gene encoding dALS. Unexpectedly, we find that these mutations are allelic to a previously described mutation in convoluted (conv), a gene required for epithelial morphogenesis. In conv mutants, the tubes of the Drosophila tracheal system become abnormally elongated without altering tracheal cell number. conv null mutations cause larval lethality, but do not disrupt several processes required for tracheal tube size control, including septate junction formation, deposition of a lumenal/apical extracellular matrix, and lumenal secretion of Vermiform and Serpentine, two putative matrix-modifying proteins. Clearance of lumenal matrix and subcellular localization of clathrin also appear normal in conv mutants. However, we show that Conv/dALS is required for the dynamic organization of the transient lumenal matrix and normal structure of the cuticle that lines the tracheal lumen. These and other data suggest that the Conv/ dALS-dependent tube size control mechanism is distinct from other known processes involved in tracheal tube size regulation. Moreover, we present evidence indicating that Conv/dALS has a novel, IGF-signaling independent function in tracheal morphogenesis.
Cell fate choices in Drosophila tracheal morphogenesis
BioEssays, 2000
The Drosophila tracheal system is a branched tubular structure that supplies air to target tissues. The elaborate tracheal morphology is shaped by two linked inductive processes, one involving the choice of cell fates, and the other a guided cell migration. We will describe the molecular basis for these processes, and the allocation of cell fate decisions to four temporal hierarchies. First, tracheal placodes are specified within the embryonic ectoderm. Subsequently, branch fates are allocated within the tracheal placodes, prior to migration. Localized presentation of the FGF ligand, Branchless, to tracheal cells that express the FGF receptor, Breathless, guides migration. Once cell migration is initiated, distinct cell fates are determined within each migrating branch. Finally, inhibitory feedback mechanisms ensure the correct assignment of these fates. Tracheal cell fate choices are determined by signaling cascades triggered by signals emanating from the tracheal cells, as well as by ligands produced by adjacent tissues.