Oscillation and Polarity of E-Cadherin Asymmetries Control Actomyosin Flow Patterns during Morphogenesis

Levayer, Romain; Lecuit, Thomas

doi:10.1016/j.devcel.2013.06.020

Cited by 157 publications

(165 citation statements)

References 31 publications

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“…During Drosophila germ-band extension, local forces arising from spatiotemporal dynamics in MyoII levels are required for junctional shrinkage (Bertet et al, 2004;Blankenship et al, 2006;FernandezGonzalez et al, 2009;Levayer and Lecuit, 2013;Rauzi et al, 2008) and subsequent extension (Bardet et al, 2013;Collinet et al, 2015), and act together with global, tissue-scale forces (Butler et al, 2009;Collinet et al, 2015;Etournay et al, 2015;Ray et al, 2015) to drive tissue elongation. Therefore, cell intercalation is a direct consequence of local and tissue-scale forces and is a major cause of tissue elongation in the Drosophila germband.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

confidence: 99%

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

et al. 2017

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“…The rosette subsequently resolves into an array along the AP axis. The planar polarized distribution of cytoskeletal molecules allows shrinkage of AP cell interfaces by two related mechanisms: (1) planar polarized junctional contraction (Fernandez-Gonzalez et al, 2009;Rauzi et al, 2010); and (2) alternating myosin-II flow directed by polarized fluctuations in E-cadherin levels (Levayer and Lecuit, 2013;Rauzi et al, 2010). Notably, another process, the contraction of apically localized myosin-II (also called medial myosin-II), contributes to convergent extension during Drosophila epithelial elongation.…”

Section: Drosophila Epithelial Morphogenesismentioning

confidence: 99%

The roles and regulation of multicellular rosette structures during morphogenesis

2014

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Multicellular rosettes have recently been appreciated as important cellular intermediates that are observed during the formation of diverse organ systems. These rosettes are polarized, transient epithelial structures that sometimes recapitulate the form of the adult organ. Rosette formation has been studied in various developmental contexts, such as in the zebrafish lateral line primordium, the vertebrate pancreas, the Drosophila epithelium and retina, as well as in the adult neural stem cell niche. These studies have revealed that the cytoskeletal rearrangements responsible for rosette formation appear to be conserved. By contrast, the extracellular cues that trigger these rearrangements in vivo are less well understood and are more diverse. Here, we review recent studies of the genetic regulation and cellular transitions involved in rosette formation. We discuss and compare specific models for rosette formation and highlight outstanding questions in the field.

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“…[33][34][35] The PIV algorithm is a correlation-based technique for computing velocity field maps of moving objects-in this case, collective cell and ECM filament motion. 3,18,19,36 Mathematical analysis of biological motion, using PIV, allowed a rigorous, mathematically unbiased, search for underlying morphogenetic motion patterns.…”

Section: Localized Morphogenetic Movements In Isolated Tissue Explantmentioning

confidence: 99%

Identification of emergent motion compartments in the amniote embryo

Loganathan¹,

Little²,

Joshi³

et al. 2014

Organogenesis

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The tissue scale deformations (1mm) required to form an amniote embryo are poorly understood. Here, we studied »400 mm-sized explant units from gastrulating quail embryos. The explants deformed in a reproducible manner when grown using a novel vitelline membrane-based culture method. Time-lapse recordings of latent embryonic motion patterns were analyzed after disk-shaped tissue explants were excised from three specific regions near the primitive streak: 1) anterolateral epiblast, 2) posterolateral epiblast, and 3) the avian organizer (Hensen's node). The explants were cultured for 8 hours-an interval equivalent to gastrulation. Both the anterolateral and the posterolateral epiblastic explants engaged in concentric radial/centrifugal tissue expansion. In sharp contrast, Hensen's node explants displayed Cartesian-like, elongated, bipolar deformations-a pattern reminiscent of axis elongation. Time-lapse analysis of explant tissue motion patterns indicated that both cellular motility and extracellular matrix fiber (tissue) remodeling take place during the observed morphogenetic deformations. As expected, treatment of tissue explants with a selective Rho-Kinase (p160ROCK) signaling inhibitor, Y27632, completely arrested all morphogenetic movements. Microsurgical experiments revealed that lateral epiblastic tissue was dispensable for the generation of an elongated midline axisprovided that an intact organizer (node) is present. Our computational analyses suggest the possibility of delineating tissue-scale morphogenetic movements at anatomically discrete locations in the embryo. Further, tissue deformation patterns, as well as the mechanical state of the tissue, require normal actomyosin function. We conclude that amniote embryos contain tissue-scale, regionalized morphogenetic motion generators, which can be assessed using our novel computational time-lapse imaging approach. These data and future studies-using explants excised from overlapping anatomical positions-will contribute to understanding the emergent tissue flow that shapes the amniote embryo.

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Oscillation and Polarity of E-Cadherin Asymmetries Control Actomyosin Flow Patterns during Morphogenesis

Cited by 157 publications

References 31 publications

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

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

The roles and regulation of multicellular rosette structures during morphogenesis

Identification of emergent motion compartments in the amniote embryo

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