Global morphogenetic flow is accurately predicted by the spatial distribution of myosin motors

Streichan, Sebastian J.; Lefebvre, Matthew F; Noll, Nicholas; Wieschaus, Eric; Shraiman, Boris I.

doi:10.7554/elife.27454

Cited by 176 publications

(214 citation statements)

References 42 publications

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“…Collective cellular motion on curved surfaces is ubiquitous in developmental processes, such as morphogenesis and embryonic development [14][15][16], or when cells migrate in the gut [17,18] or on the surface of the growing cornea [19], and it also affects cell division [20]. Recent in vitro work has demonstrated a direct effect of substrate curvature on cytoskeletal alignment and cell motility in epithelial cells [21].…”

Section: Introductionmentioning

confidence: 99%

Topological Sound and Flocking on Curved Surfaces

2017

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Active systems on curved geometries are ubiquitous in the living world. In the presence of curvature, orientationally ordered polar flocks are forced to be inhomogeneous, often requiring the presence of topological defects even in the steady state because of the constraints imposed by the topology of the underlying surface. In the presence of spontaneous flow, the system additionally supports long-wavelength propagating sound modes that get gapped by the curvature of the underlying substrate. We analytically compute the steady-state profile of an active polar flock on a two-sphere and a catenoid, and show that curvature and active flow together result in symmetry-protected topological modes that get localized to special geodesics on the surface (the equator or the neck, respectively). These modes are the analogue of edge states in electronic quantum Hall systems and provide unidirectional channels for information transport in the flock, robust against disorder and backscattering.

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Section: Introductionmentioning

confidence: 99%

Topological Sound and Flocking on Curved Surfaces

2017

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“…The large majority of rearrangements are oriented along the head-to-tail body axis (19,20,40,41,54), and the time period of rapid cell rearrangement (Fig. 1C) coincides with the period of planar polarized myosin (23,25,40). Taken together, these findings suggest that over the 20 min timescale of rapid axis elongation, the Drosophila germband tissue may still behave as a weak yield-stress solid, in which driving forces from planar polarized myosin are required to overcome energy barriers to drive cell rearrangements and tissue flow over these short timescales.…”

Section: Discussionmentioning

confidence: 84%

“…5C), cell rearrangement (Fig. 5D), and endoderm invagination, but still undergo mesoderm invagination (18,20,25,26,28,41).…”

Section: Cell Shape and Cell Shape Alignment Together Indicate A Solimentioning

confidence: 99%

“…1A). Planar polarized myosin is required for cell rearrangements that converge and extend the tissue to rapidly elongate the body and is thought to produce anisotropic tensions in the tissue (19)(20)(21)(22)(23)(24)(25). In addition, the Drosophila germband experiences external forces from neighboring tissues, including the mesoderm and endoderm, which have been linked to cell shape changes in the germband during convergent extension (26)(27)(28) (Fig.…”

Section: Introductionmentioning

confidence: 99%

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Anisotropy links cell shapes to a solid-to-fluid transition during convergent extension

Wang

Merkel

Sutter

et al. 2019

Preprint

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Within developing embryos, tissues flow and reorganize dramatically on timescales as short as minutes. This includes epithelial tissues, which often narrow and elongate in convergent extension movements due to anisotropies in external forces or in internal cell-generated forces. However, the mechanisms that allow or prevent tissue reorganization, especially in the presence of strongly anisotropic forces, remain unclear. We study this question in the converging and extending Drosophila germband epithelium, which displays planar polarized myosin II and experiences anisotropic forces from neighboring tissues, and we show that in contrast to isotropic tissues, cell shape alone is not sufficient to predict the onset of rapid cell rearrangement. From theoretical considerations and vertex model simulations, we predict that in anisotropic tissues two experimentally accessible metrics of cell patterns-the cell shape index and a cell alignment index-are required to determine whether an anisotropic tissue is in a solid-like or fluid-like state. We show that changes in cell shape and alignment over time in the Drosophila germband indicate a solid-to-fluid transition that corresponds to the onset of cell rearrangement and convergent extension in wild-type embryos and are also consistent with more solid-like behavior in bnt mutant embryos. Thus, the onset of cell rearrangement in the germband can be predicted by a combination of cell shape and alignment. These findings suggest that convergent extension is associated with a transition to more fluid-like tissue behavior, which may help accommodate tissue shape changes during rapid developmental events.

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“…During gastrulation of Drosophila, about 6000 cells on the embryonic blastoderm on the embryo surface undergo global morphogenetic flow which induce severe tissue deformation, finally giving rise to the three germ layers. We compute the DM on an "ensemble averaged" cell velocity dataset from 22 wild-type Drosophila melanogaster embryos undergoing gastrulation, developed in [25]. Each velocity dataset is obtained combining in toto light sheet microscopy [11,12] and tissue cartography [26], and consists of coarse-grained velocities averaged with a spatial window of approximately 5 cell size.…”

Section: Gastrulation In the Fly Embryomentioning

confidence: 99%

Dynamic morphoskeletons in development

Serra

Streichan

Mahadevan

2019

Preprint

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Morphogenetic flows in developmental biology are characterized by the coordinated motion of thousands of cells that organize into tissues, naturally raising the question of how this collective organization arises. Using only the Lagrangian kinematics of tissue deformation, which naturally integrates local and global mechanisms along cell paths, we can identifying the Dynamic Morphoskeletons (DM) behind morphogenesis, i.e., the evolving centerpieces of multi-cellular trajectory patterns. The DM is model and parameter-free, frame-invariant, robust to measurement errors, and can be computed from unfiltered cell velocity data. It reveals the spatial attractors and repellers of the embryo, objects that cannot be identified by simple trajectory inspection or Eulerian methods that are local and typically frame-dependent. Computing the DM underlying primitive streak formation in chicken embryo and early gastrulation in the whole fly embryo, we find that the DM captures the early footprint of known morphogenetic features, and reveals new ones, providing a geometric framework to analyze tissue organization.

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Global morphogenetic flow is accurately predicted by the spatial distribution of myosin motors

Cited by 176 publications

References 42 publications

Topological Sound and Flocking on Curved Surfaces

Topological Sound and Flocking on Curved Surfaces

Anisotropy links cell shapes to a solid-to-fluid transition during convergent extension

Dynamic morphoskeletons in development

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