Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing

Etournay, Raphaël; Popović, Marko; Merkel, Matthias; Nandi, Amitabha; Blasse, Corinna; Aigouy, Benoît; Brandl, Holger; Myers, Gene; Salbreux, Guillaume; Jülicher, Frank; Eaton, Suzanne

doi:10.7554/elife.07090

Cited by 326 publications

(529 citation statements)

References 58 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 initial velocity of wound margin retraction or closure after ablation measures the stress-to-viscosity ratio within the tissue. Alternatively, severing a large circle (Bonnet et al, 2012;Etournay et al, 2015) reveals at once the main directions of stress and its anisotropy (Fig. 2Ca,Cb).…”

Section: Laser Ablationmentioning

confidence: 99%

Measuring forces and stressesin situin living tissues

2016

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Development, homeostasis and regeneration of tissues result from a complex combination of genetics and mechanics, and progresses in the former have been quicker than in the latter. Measurements of in situ forces and stresses appear to be increasingly important to delineate the role of mechanics in development. We review here several emerging techniques: contact manipulation, manipulation using light, visual sensors, and non-mechanical observation techniques. We compare their fields of applications, their advantages and limitations, and their validations. These techniques complement measurements of deformations and of mechanical properties. We argue that such approaches could have a significant impact on our understanding of the development of living tissues in the near future.

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“…Another extensively studied system that allows detailed tracking of individual cells is the Drosophila embryo [26][27][28][29][30]. In recent studies that combined experiments with advanced data analysis, it was possible to quantitatively account for shape change of the wing blade by decomposing it into cell divisions, cell rearrangements and cell shape changes [31,32]. Finally, it has recently become possible to track more than 100,000 individual cells in a chick embryo over a period exceeding 24 hours [33].…”

Section: Introductionmentioning

confidence: 99%

Active Vertex Model for Cell-Resolution Description of Epithelial Tissue Mechanics

Barton

Henkes

Weijer

et al. 2016

Preprint

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We introduce an Active Vertex Model (AVM) for cell-resolution studies of the mechanics of confluent epithelial tissues consisting of tens of thousands of cells, with a level of detail inaccessible to similar methods. The AVM combines the Vertex Model for confluent epithelial tissues with active matter dynamics. This introduces a natural description of the cell motion and accounts for motion patterns observed on multiple scales. Furthermore, cell contacts are generated dynamically from positions of cell centres. This not only enables efficient numerical implementation, but provides a natural description of the T1 transition events responsible for local tissue rearrangements. The AVM also includes cell alignment, cellspecific mechanical properties, cell growth, division and apoptosis. In addition, the AVM introduces a flexible, dynamically changing boundary of the epithelial sheet allowing for studies of phenomena such as the fingering instability or wound healing. We illustrate these capabilities with a number of case studies. Author summaryWe present a detailed analysis of the Active Vertex Model to study the mechanics of confluent epithelial tissues and cell monolayers. The model combines the commonly used Vertex Model for describing epithelial tissue mechanics with the active matter dynamics extensively studied in soft matter physics. We utlise an exact mathematical mapping that enables a very efficient numerical implementation using standard methods for simulating particle-based models. System sizes accessible to this model allow us to probe the dynamical motion patterns that occur in tissues over a range of length-and time-scales previously inaccessible to available simulation tools. Our model also includes a number of essential features required to properly describe actual biological systems such as cell growth, cell division and aptotsis, as well as the dynamic boundary of the epithelial sheet. This allows us to study phenomena such as the finger-like protrusions in cell monolayers and processes related to wound healing. The model is implemented into the SAMoS PLOS Computational Biology | https://doi

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Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing

Cited by 326 publications

References 58 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

Measuring forces and stressesin situin living tissues

Active Vertex Model for Cell-Resolution Description of Epithelial Tissue Mechanics

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