A wave of EGFR signaling determines cell alignment and intercalation in the<i>Drosophila</i>tracheal placode

Nishimura, Mayuko; Inoue, Yoshiko; Hayashi, Shigeo

doi:10.1242/dev.010397

Cited by 94 publications

(115 citation statements)

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“…Previous work examining tracheal morphogenesis in the fly has demonstrated that interfaces between cells with low levels versus high levels of EGFR signalling correlate with MyoIIdependent AJ remodelling in the tracheal placode (Nishimura et al, 2007). This situation resembles that which we describe here in the wake of the MF.…”

Section: Research Articlesupporting

confidence: 80%

“…Supra-cellular cables of MyoII have been previously associated with cell alignment in various epithelia (Nishimura et al, 2007;Simone and DiNardo, 2010;Walters et al, 2006) and have also been observed at the boundary of sorted clones, whereby cells align at a MyoII-enriched interface (Chang et al, 2011;Le Borgne et al, 2002;Wei et al, 2005). Interestingly, we find that the actomyosin cable defining the posterior boundary of the MF is also preferentially enriched for Rok, a component of the T1, MyoIIpositive AJ in the ventral epidermis (Simoes Sde et al, 2010).…”

Section: Compartment Boundary and Cell Intercalation During Retina Mosupporting

confidence: 72%

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Atonal and EGFR signalling orchestraterok- andDrak-dependent adherens junction remodelling during ommatidia morphogenesis

et al. 2012

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SUMMARYMorphogenesis of epithelial tissues relies on the interplay between cell division, differentiation and regulated changes in cell shape, intercalation and sorting. These processes are often studied individually in relatively simple epithelia that lack the complexity found during organogenesis when these processes might all coexist simultaneously. To address this issue, we are making use of the developing fly retinal neuroepithelium. Retinal morphogenesis relies on a coordinated sequence of interdependent morphogenetic events that includes apical cell constriction, localized alignment of groups of cells and ommatidia morphogenesis coupled to neurogenesis. Here, we use live imaging to document the sequence of adherens junction (AJ) remodelling events required to generate the fly ommatidium. In this context, we demonstrate that the kinases Rok and Drak function redundantly during Myosin II-dependent cell constriction, subsequent multicellular alignment and AJ remodelling. In addition, we show that early multicellular patterning characterized by cell alignment is promoted by the conserved transcription factor Atonal (Ato). Further ommatidium patterning requires the epidermal growth factor receptor (EGFR) signalling pathway, which transcriptionally governs rok-and Drakdependent AJ remodelling while also promoting neurogenesis. In conclusion, our work reveals an important role for Drak in regulating AJ remodelling during retinal morphogenesis. It also sheds new light on the interplay between Ato, EGFR-dependent transcription and AJ remodelling in a system in which neurogenesis is coupled with cell shape changes and regulated steps of cell intercalation.

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Section: Research Articlesupporting

confidence: 80%

Section: Compartment Boundary and Cell Intercalation During Retina Mosupporting

confidence: 72%

Atonal and EGFR signalling orchestraterok- andDrak-dependent adherens junction remodelling during ommatidia morphogenesis

et al. 2012

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“…Actomyosin cables are also characteristic of additional processes, e.g. dorsal closure and germband extension in the Drosophila embryo Blankenship et al, 2006), tracheal tube invagination and neural plate bending and elongation (Nishimura et al, 2007;Nishimura and Takeichi, 2008), and wound healing (Martin and Lewis, 1992;Wood et al, 2002). During Drosophila germ band extension, it has been shown that mechanical tension is higher at cell bonds that are part of an actomyosin cable compared with isolated cell bonds, indicating that cell bond tension is influenced by higher-order cellular organization during this process (Fernandez-Gonzalez et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

A local difference in Hedgehog signal transduction increases mechanical cell bond tension and biases cell intercalations along the Drosophila anteroposterior compartment boundary

et al. 2015

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Tissue organization requires the interplay between biochemical signaling and cellular force generation. The formation of straight boundaries separating cells with different fates into compartments is important for growth and patterning during tissue development. In the developing Drosophila wing disc, maintenance of the straight anteroposterior (AP) compartment boundary involves a local increase in mechanical tension at cell bonds along the boundary. The biochemical signals that regulate mechanical tension along the AP boundary, however, remain unknown. Here, we show that a local difference in Hedgehog signal transduction activity between anterior and posterior cells is necessary and sufficient to increase mechanical tension along the AP boundary. This difference in Hedgehog signal transduction is also required to bias cell rearrangements during cell intercalations to keep the characteristic straight shape of the AP boundary. Moreover, severing cell bonds along the AP boundary does not reduce tension at neighboring bonds, implying that active mechanical tension is upregulated, cell bond by cell bond. Finally, differences in the expression of the homeodomain-containing protein Engrailed also contribute to the straight shape of the AP boundary, independently of Hedgehog signal transduction and without modulating cell bond tension. Our data reveal a novel link between local differences in Hedgehog signal transduction and a local increase in active mechanical tension of cell bonds that biases junctional rearrangements. The large-scale shape of the AP boundary thus emerges from biochemical signals inducing patterns of active tension on cell bonds.

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“…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.…”

Section: Introductionmentioning

confidence: 99%

“…It is partly suppressed dorsally by the expression of sal (also known as spalt), which encodes a zinc finger transcription factor, leading to the observed asymmetry in invagination along the dorsoventral axis. In addition, the careful examination of cell behaviour and myosin localization during the invagination process has revealed that the Egf pathway is activated in a wave, which extends from the centre of the placode, where cells initially constrict apically, to the outer cells, coordinating the timing and positioning of intrinsic cell internalization activities (Nishimura et al, 2007). Egfr signalling eventually translates into an ordered apical distribution of actin and myosin, which presumably generates the forces that lead to invagination via actomyosin contraction.…”

mentioning

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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A wave of EGFR signaling determines cell alignment and intercalation in theDrosophilatracheal placode

Cited by 94 publications

References 50 publications

Atonal and EGFR signalling orchestraterok- andDrak-dependent adherens junction remodelling during ommatidia morphogenesis

Atonal and EGFR signalling orchestraterok- andDrak-dependent adherens junction remodelling during ommatidia morphogenesis

A local difference in Hedgehog signal transduction increases mechanical cell bond tension and biases cell intercalations along the Drosophila anteroposterior compartment boundary

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

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