Genetic Control of Cell Intercalation during Tracheal Morphogenesis in Drosophila

Ribeiro, Carlos; Neumann, Marc; Affolter, Markus

doi:10.1016/j.cub.2004.11.056

Cited by 140 publications

(171 citation statements)

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“…These studies have shown that highly controlled cell intercalations, which require extensive AJ remodelling, are key to the formation of fine tracheal branches. Based on these studies and on single-cell analysis, a four-step model of tube remodelling has been proposed (Ribeiro et al, 2004) (see Fig. 5).…”

Section: The Role Of Cell Intercalationmentioning

confidence: 99%

“…The dorsal trunk is also the only tracheal tube in which all cells express the zinc finger transcription factor Sal (Kuhnlein and Schuh, 1996). Loss-and gain-of-function genetic studies, including single-cell analyses (Ribeiro et al, 2004), have demonstrated that Sal is indeed responsible for inhibiting cell intercalation and the formation of autocellular AJs in the dorsal trunk, and it can potently and completely inhibit intercalation when ectopically expressed in dorsal branches. How Sal inhibits intercalation remains unknown.…”

Section: The Role Of Cell Intercalationmentioning

confidence: 99%

“…5). To describe these cell rearrangements, a detailed characterization of the formation of the dorsal branch has been undertaken using high-resolution live imaging with a GFP-fusion protein that labels adherens junctions (AJs) (Ribeiro et al, 2004). These studies have shown that highly controlled cell intercalations, which require extensive AJ remodelling, are key to the formation of fine tracheal branches.…”

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confidence: 99%

“…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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Section: The Role Of Cell Intercalationmentioning

confidence: 99%

Section: The Role Of Cell Intercalationmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

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

2008

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“…First, tracheal tip cells (TCs) begin to migrate away from the tracheal sac and pull along several tracheal stalk cells into the developing branch, forming a small bud (Samakovlis et al, 1996). In a second phase, the branches elongate and narrow down due to stalk cell intercalation (SCI) and extensive cell lengthening (Ribeiro et al, 2004) (Fig. S1B).…”

Section: Introductionmentioning

confidence: 99%

Myosin II is not required for Drosophila tracheal branch elongation and cell intercalation

et al. 2017

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The Drosophila tracheal system consists of an interconnected network of monolayered epithelial tubes that ensures oxygen transport in the larval and adult body. During tracheal dorsal branch (DB) development, individual DBs elongate as a cluster of cells, led by tip cells at the front and trailing cells in the rear. Branch elongation is accompanied by extensive cell intercalation and cell lengthening of the trailing stalk cells. Although cell intercalation is governed by Myosin II (MyoII)-dependent forces during tissue elongation in the Drosophila embryo that lead to germ-band extension, it remained unclear whether MyoII plays a similar active role during tracheal branch elongation and intercalation. Here, we have used a nanobody-based approach to selectively knock down MyoII in tracheal cells. Our data show that, despite the depletion of MyoII function, tip cell migration and stalk cell intercalation (SCI) proceed at a normal rate. This confirms a model in which DB elongation and SCI in the trachea occur as a consequence of tip cell migration, which produces the necessary forces for the branching process. ABSTRACTThe Drosophila tracheal system consists of an interconnected network of monolayered epithelial tubes that ensures oxygen transport in the larval and adult body. During tracheal dorsal branch (DB) development, individual DBs elongate as a cluster of cells, led by tip cells at the front and trailing cells in the rear. Branch elongation is accompanied by extensive cell intercalation and cell lengthening of the trailing stalk cells. Although cell intercalation is governed by Myosin II (MyoII)-dependent forces during tissue elongation in the Drosophila embryo that lead to germ-band extension, it remained unclear whether MyoII plays a similar active role during tracheal branch elongation and intercalation. Here, we have used a nanobodybased approach to selectively knock down MyoII in tracheal cells. Our data show that, despite the depletion of MyoII function, tip cell migration and stalk cell intercalation (SCI) proceed at a normal rate. This confirms a model in which DB elongation and SCI in the trachea occur as a consequence of tip cell migration, which produces the necessary forces for the branching process.

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Mechanisms controlling human endothelial lumen formation and tube assembly in three‐dimensional extracellular matrices

Davis

Koh

Stratman

2007

Birth Defects Research Pt C

119

142

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Recent data have revealed new mechanisms that underlie endothelial cell (EC) lumen formation during vascular morphogenic events in development, wound repair, and other disease states. It is apparent that EC interactions with extracellular matrices (ECMs) establish signaling cascades downstream of integrin ligation leading to activation of the Rho GTPases, Cdc42 and Rac1, which are required for lumen formation. In large part, this process is driven by intracellular vacuole formation and coalescence, which rapidly leads to the creation of fluid-filled matrix-free spaces that are then interconnected via EC-EC interactions to create multicellular tube structures. EC vacuoles markedly accumulate in a polarized fashion directly adjacent to the centrosome in a region that strongly accumulates Cdc42 protein as indicated by green fluorescent protein (GFP)-Cdc42 during the lumen formation process. Downstream of Cdc42-mediated signaling, key molecules that have been identified to be required for EC lumen formation include Pak2, Pak4, Par3, Par6, and the protein kinase C (PKC) isoforms zeta and epsilon. Together, these molecules coordinately regulate the critical EC lumen formation process in three-dimensional (3D) collagen matrices. These events also require cell surface proteolysis mediated through membrane type 1 matrix metalloproteinase (MT1-MMP), which is necessary to create vascular guidance tunnels within the 3D matrix environment. These tunnels represent physical spaces within the ECM that are necessary to regulate vascular morphogenic events, including the establishment of interconnected vascular tube networks as well as the recruitment of pericytes to initiate vascular tube maturation (via basement membrane matrix assembly) and stabilization. Current research continues to analyze how specific molecules integrate signaling information in concert to catalyze EC lumen formation, pericyte recruitment, and stabilization processes to control vascular morphogenesis in 3D extracellular matrices.

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Genetic Control of Cell Intercalation during Tracheal Morphogenesis in Drosophila

Cited by 140 publications

References 43 publications

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

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

Myosin II is not required for Drosophila tracheal branch elongation and cell intercalation

Mechanisms controlling human endothelial lumen formation and tube assembly in three‐dimensional extracellular matrices

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