Remodelling epithelial tubes through cell rearrangements: from cells to molecules

Neumann, Marc; Affolter, Markus

doi:10.1038/sj.embor.7400597

Cited by 27 publications

(23 citation statements)

References 38 publications

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“…The elongation of the dorsal branch does not occur in the absence of Dpp signaling (Chen et al, 1998), because, by itself, Bnl/FGF only induces filopodial extensions (Ribeiro et al, 2002). Dpp signaling is required to suppress Spalt (Sal) in the DBs, enabling the formation of a unicellular tube through cell intercalation (Ribeiro et al, 2004;Neumann and Affolter, 2006).…”

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confidence: 99%

A cellular process that includes asymmetric cytokinesis remodels the dorsal tracheal branches in Drosophila larvae

2015

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Tubular networks are central to the structure and function of many organs, such as the vertebrate lungs or the Drosophila tracheal system. Their component epithelial cells are able to proliferate and to undergo complex morphogenetic movements, while maintaining their barrier function. Little is known about the details of the mitotic process in tubular epithelia. Our study presents a comprehensive model of cellular remodeling and proliferation in the dorsal branches of third-instar Drosophila larvae. Through a combination of immunostaining and novel live imaging techniques, we identify the key steps in the transition from a unicellular to a multicellular tube. Junctional remodeling precedes mitosis and, as the cells divide, new junctions are formed through several variations of what we refer to as 'asymmetric cytokinesis'. Depending on the spacing of cells along the dorsal branch, mitosis can occur either before or after the transition to a multicellular tube. In both instances, cell separation is accomplished through asymmetric cytokinesis, a process that is initiated by the ingression of the cytokinetic ring. Unequal cell compartments are a possible but rare outcome of completing mitosis through this mechanism. We also found that the Dpp signaling pathway is required but not sufficient for cell division in the dorsal branches.

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Section: Introductionmentioning

confidence: 99%

A cellular process that includes asymmetric cytokinesis remodels the dorsal tracheal branches in Drosophila larvae

2015

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“…size, length or diameter) were described (Beitel and Krasnow, 2000). The identification and cloning of the genes affected in these and other mutants has shed light on how the specialized apical secretion of ECM material contributes to tube expansion and tube length control.Although the observed size differences between distinct tracheal branches is probably controlled by those genes that regulate branch identity (for example, by the presence or absence of Sal in the cells of the dorsal trunk and the dorsal branches, respectively) (Ribeiro et al, 2004;Neumann and Affolter, 2006; Casanova, 2007), the diameter of certain tubes expands rapidly in a relatively short time frame. The uniform expansion of tube diameter requires the formation of a transient luminal chitin-based matrix (Araujo et al, 2005;Moussian et al, 2006;Tonning et al, 2005;Devine et al, 2005) (reviewed by Swanson and Beitel, 2006) (see Fig.…”

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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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“…The tracheae are the respiratory organ of Drosophila and genes have been identified that are required for each step of tracheole branching morphogenesis (Samakovlis et al 1996;Petit et al 2002;Neumann and Affolter 2006). These studies identify several signaling pathways conserved in humans, including the GF, TGF-b, Wnt, and Hh pathways.…”

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“…Within the moving cell there are directional changes in actin/myosin polymerization and endocytic shuttling of membrane components to the leading edge. Cell intercalation additionally requires changes in the number and location of ''adherens junctions,'' which are specialized connections between epithelial cells involving catenins, cadherins, and the actin cytoskeleton (Neumann and Affolter 2006). GTPases such as Rho and nucleoside kinases including nm23 (awd) act downstream of Wnt and other pathways to directly regulate cytoskeleton organization and membrane dynamics in the moving cell (Palacios et al 2002;Dammai et al 2003).…”

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Conditional Switches for Extracellular Matrix Patterning inDrosophila melanogaster

et al. 2008

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An F 1 mutagenesis strategy was developed to identify conditional mutations affecting extracellular matrix (ECM) patterning. Tubulogenesis requires coordinated movement of epithelial cells and deposition of a multilayered ECM. In the Drosophila ovary, an epithelium of follicle cells creates the eggshells, including the paired tubular dorsal appendages (DAs) that act as breathing tubes for the embryo. A P-element mutagenesis strategy allowed for conditional overexpression of hundreds of genes in follicle cells. Conditional phenotypes were scored at the level of individual mutant (F 1 ) female flies. ECM pattern regulators were readily identified including MAPK signaling gene ets domain lacking (fused DAs), Wnt pathway genes frizzled 3 and osa (long DAs), Hh pathway gene debra (branched DAs), and transcription factor genes sima/HIF-1a, ush, lilli, Tfb1, broad, and foxo. In moving cells the ½Ca 21 /calcineurin pathway can regulate adhesion to ECM while adherens junctions link cells together. Accordingly, thin eggshell and DA phenotypes were identified for the calcineurin regulator calreticulin and the adherens junction component arc. Finally a tubulogenesis defect phenotype was identified for the gene pterodactyl, homologous to the mammalian serine/threonine receptorassociated protein (STRAP) that integrates the TGF-b and PI3K/AKT signaling pathways. Because phenotypes can be scored in each mutant fly before and after gene induction, this F 1 conditional mutagenesis strategy should allow for increased scale in screens for mutations affecting repeated (reiterated) events in adult animals, including gametogenesis, movement, behavior, and learning.

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Remodelling epithelial tubes through cell rearrangements: from cells to molecules

Cited by 27 publications

References 38 publications

A cellular process that includes asymmetric cytokinesis remodels the dorsal tracheal branches in Drosophila larvae

A cellular process that includes asymmetric cytokinesis remodels the dorsal tracheal branches in Drosophila larvae

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

Conditional Switches for Extracellular Matrix Patterning inDrosophila melanogaster

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