breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells.

Klämbt, Christian; Glazer, Lillian; Shilo, Ben‐Zion

doi:10.1101/gad.6.9.1668

Cited by 400 publications

(293 citation statements)

References 36 publications

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“…FGFs and the control of branching morphogenesis-Mutant analysis in Drosophila has revealed that an FGF ligand (branchless) and its receptor (breathless) regulate tracheal development (Klambt et al 1992;Sutherland et al 1996). In mouse, FGF signaling through FGF-10 and FGFR2-IIIb direct branching morphogenesis of the lungs (Min et al 1998;Shishido et al 1997;Stathopoulos et al 2004), and although mammalian lungs and insect trachea may not be directly homologous, these data suggest a conserved role for FGF signaling in controlling branching morphogenesis in organisms as diverse as flies and mammals.…”

Section: Conserved Roles Of Fgf Signalingmentioning

confidence: 99%

FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian

2007

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The fibroblast growth factor (FGF) signal transduction pathway serves as one of the key regulators of early metazoan development, displaying conserved roles in the specification of endodermal, mesodermal, and neural fates during vertebrate development. FGF signals also regulate gastrulation, in part, by triggering epithelial to mesenchymal transitions in embryos of both vertebrates and invertebrates. Thus, FGF signals coordinate gastrulation movements across many different phyla. To help understand the breadth of FGF signaling deployment across the animal kingdom, we have examined the presence and expression of genes encoding FGF pathway components in the anthozoan cnidarian Nematostella vectensis. We isolated three FGF ligands (NvFGF8A, NvFGF8B, and NvFGF1A), two FGF receptors (NvFGFRa and NvFGFRb), and two orthologs of vertebrate FGF responsive genes, Sprouty (NvSprouty), an inhibitor of FGF signaling, and Churchill (NvChurchill), a Zn finger transcription factor. We found these FGF ligands, receptors, and response gene expressed asymmetrically along the oral/aboral axis during gastrulation and in a developing chemosensory structure of planula stages known as the apical tuft. These results suggest a conserved role for FGF signaling molecules in coordinating both gastrulation and neural induction that predates the Cambrian explosion and the origins of the Bilateria.

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Section: Conserved Roles Of Fgf Signalingmentioning

confidence: 99%

FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian

2007

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“…Tracheal cells express a Fgf receptor, encoded by the breathless (btl) locus (Klambt et al, 1992), as well as a Fgf-specific signalling adaptor protein encoded by downstreamof-Fgfr (dof; also known as stumps) (Vincent et al, 1998;Imam et al, 1999;Petit et al, 2004;Wilson et al, 2004). As for rho and cvc expression (discussed above), btl and dof expression also require the Trh transcription factor, and the accumulation of btl and dof clearly distinguishes tracheal cells from neighbouring, non-tracheal, cells and prepares them for the branching process.…”

Section: The Role Of Cell Migrationmentioning

confidence: 99%

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

2008

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2055Our understanding of the molecular control of morphological processes has increased tremendously over recent years through the development and use of high resolution in vivo imaging approaches, which have enabled cell behaviour to be linked to molecular functions. Here we review how such approaches have furthered our understanding of tracheal branching morphogenesis in Drosophila, during which the control of cell invagination, migration, competition and rearrangement is accompanied by the sequential secretion and resorption of proteins into the apical luminal space, a vital step in the elaboration of the trachea's complex tubular network. We also discuss the similarities and differences between flies and vertebrates in branched organ formation that are becoming apparent from these studies. IntroductionBranching morphogenesis restructures epithelial sheets to give rise to organs of fascinating three-dimensional architecture, as exemplified by the adult lung, the kidney and the vasculature in humans. In Drosophila melanogaster, genetic studies have provided much insight into the regulatory networks that regulate the ordered formation of tracheal branches in the embryo, and into how the different branches coordinate their relative sizes, an issue that is of importance to the physical aspects of branched organ function (Affolter et al., 2003;Ghabrial et al., 2003;Uv et al., 2003). More recently, the development of live-imaging approaches in Drosophila have allowed researchers to take a deeper look at the behaviour of cells during the branching process, and have enabled events at the molecular level to be linked to the behaviour of individual cells or groups of cells.This combination of molecular genetics and live-imaging techniques has provided investigators with a unique opportunity to understand the morphological processes that occur during branching morphogenesis. This review focuses and builds on some of these recent insights, and assesses how they have led to a better understanding of the cellular and molecular processes that contribute to the transformation of simple, two-dimensional epithelial sheets into fascinating, three-dimensional tubular structures that can perform important functions in development and homeostasis. We focus here on the Drosophila tracheal system because several cellular and molecular paradigms, such as cell migration, competition and rearrangement, as well as the elaboration of a complex apical luminal environment, have recently been uncovered in this system that might serve related roles in the formation of other branched organs or tissues; these similarities might help us in the future to gain an even better understanding of how morphogenesis in general is regulated during development. Tracheal development in the fly embryoThe complex structure of the tracheal system consists of interconnected, metameric units of different-sized tubes that extend over the entire embryo shortly before hatching (Samakovlis et al., 1996b) (see Fig. 1, see also Movie 1 in the supplementary material)....

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“…In Drosophila melanogaster, Breathless/fibroblast growth factor receptor (Btl/FGFR) is implicated in the Branchless/FGF (Bnl/FGF)-dependent migration of tracheal cells during the development of the embryonic tracheal system (Klambt et al 1992;Sutherland et al 1996;Affolter et al 2003;Ghabrial et al 2003;Uv et al 2003). Btl/FGFR is expressed in migrating tracheal cells, whereas the Bnl/FGF ligand is expressed in single or groups of ectodermal and mesodermal cells, in a highly dynamic pattern that prefigures tracheal branch outgrowth.…”

mentioning

confidence: 99%

A Genetic Mosaic Analysis With a Repressible Cell Marker Screen to Identify Genes Involved in Tracheal Cell Migration During Drosophila Air Sac Morphogenesis

et al. 2007

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Branching morphogenesis of the Drosophila tracheal system relies on the fibroblast growth factor receptor (FGFR) signaling pathway. The Drosophila FGF ligand Branchless (Bnl) and the FGFR Breathless (Btl/FGFR) are required for cell migration during the establishment of the interconnected network of tracheal tubes. However, due to an important maternal contribution of members of the FGFR pathway in the oocyte, a thorough genetic dissection of the role of components of the FGFR signaling cascade in tracheal cell migration is impossible in the embryo. To bypass this shortcoming, we studied tracheal cell migration in the dorsal air sac primordium, a structure that forms during late larval development. Using a mosaic analysis with a repressible cell marker (MARCM) clone approach in mosaic animals, combined with an ethyl methanesulfonate (EMS)-mutagenesis screen of the left arm of the second chromosome, we identified novel genes implicated in cell migration. We screened 1123 mutagenized lines and identified 47 lines displaying tracheal cell migration defects in the air sac primordium. Using complementation analyses based on lethality, mutations in 20 of these lines were genetically mapped to specific genomic areas. Three of the mutants were mapped to either the Mhc or the stam complementation groups. Further experiments confirmed that these genes are required for cell migration in the tracheal air sac primordium.

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breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells.

Cited by 400 publications

References 36 publications

FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian

FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian

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

A Genetic Mosaic Analysis With a Repressible Cell Marker Screen to Identify Genes Involved in Tracheal Cell Migration During Drosophila Air Sac Morphogenesis

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