Polarized Cortical Tension drives Zebrafish Epiboly Movements (original) (raw)

Regulated tissue fluidity steers zebrafish body elongation

Development, 2013

The tailbud is the posterior leading edge of the growing vertebrate embryo and consists of motile progenitors of the axial skeleton, musculature and spinal cord. We measure the 3D cell flow field of the zebrafish tailbud and identify changes in tissue fluidity revealed by reductions in the coherence of cell motion without alteration of cell velocities. We find a directed posterior flow wherein the polarization between individual cell motion is high, reflecting ordered collective migration. At the posterior tip of the tailbud, this flow makes sharp bilateral turns facilitated by extensive cell mixing due to increased directional variability of individual cell motions. Inhibition of Wnt or Fgf signaling or cadherin 2 function reduces the coherence of the flow but has different consequences for trunk and tail extension. Modeling and additional data analyses suggest that the balance between the coherence and rate of cell flow determines whether body elongation is linear or whether congestion forms within the flow and the body axis becomes contorted.

Kinematic analysis of cell lineage reveals coherent and robust mechanical deformation patterns in zebrafish gastrulation

2016

Digital cell lineages reconstructed from 3D+time imaging data provide unique information to unveil mechanical cues and their role in morphogenetic processes. Our methodology based on a kinematic analysis of cell lineage data reveals deformation patterns and quantitative morphogenetic landmarks for a new type of developmental table. The characteristic spatial and temporal length scales of mechanical deformation patterns derived from a continuous approximation of cell displacements indicate a compressible fluid-like behavior of zebrafish gastrulating tissues. The instantaneous deformation rate at the mesoscopic level of the cell's neighborhood is spatially and temporally heterogeneous. The robustness of mechanical patterns results from their cumulative history along cell trajectories. Unsupervised classification of mechanical descriptor profiles was used to assess the homogeneity of biomechanical cues in cell populations. Further clustering of cell trajectories according to their ...

Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain

eLife, 2019

Tissue mechanics is important for development; however, the spatio-temporal dynamics of in vivo tissue stiffness is still poorly understood. We here developed tiv-AFM, combining time-lapse in vivo atomic force microscopy with upright fluorescence imaging of embryonic tissue, to show that during development local tissue stiffness changes significantly within tens of minutes. Within this time frame, a stiffness gradient arose in the developing Xenopus brain, and retinal ganglion cell axons turned to follow this gradient. Changes in local tissue stiffness were largely governed by cell proliferation, as perturbation of mitosis diminished both the stiffness gradient and the caudal turn of axons found in control brains. Hence, we identified a close relationship between the dynamics of tissue mechanics and developmental processes, underpinning the importance of time-resolved stiffness measurements.

Contractility, Differential Tension and Membrane Removal direct zebrafish Epiboly Biomechanics

2017

ABSTRACTPrecise tissue remodeling during development is essential for shaping embryos and for optimal organ function. Epiboly is an early gastrulation event by which the blastoderm expands around the yolk to engulf it. Three different layers are involved, an epithelial layer (the enveloping layer, EVL), the embryo proper, constituted by the deep cells (DCs), and the yolk cell. Although teleost epiboly has been studied for many years, a clear understanding of its mechanics was still missing. Here we present new information on the cellular, molecular and mechanical elements involved in epiboly that, together with some other recent data and upon comparison with previous biomechanical models, lets conclude that the expansion of the epithelia is passive and driven by cortical contraction and membrane removal in the adjacent layer, the External Yolk Syncytial Layer (E-YSL). The isotropic actomyosin contraction of the E-YSL generates an anisotropic stress pattern and a directional net move...

Strain maps characterize the symmetry of convergence and extension patterns during Zebrafish gastrulation

During gastrulation of the zebrafish embryo, the cap of blastoderm cells organizes into the axial body plan of the embryo with left-right symmetry and head-tail, dorsal-ventral polarities. Our labs have been interested in the mechanics of early development and have investigated whether these large-scale cells movements can be described as tissue-level mechanical strain by a tectonics-based approach. The first step is to image the positions of all nuclei from mid-epiboy to early segmentation by digital sheet light microscopy (DSLM), organize the surface of the embryo into multi-cell spherical domains, construct velocity fields from the movements of these domains and extract 3D strain rate maps. Tensile/expansive and compressive strains in the axial and equatorial directions are detected during gastrulation as anterior and posterior expansion along the anterior-posterior axis and medial-lateral compression across the dorsal-ventral axis corresponding to convergence and extension. In l...

A multi-tiered mechanical mechanism shapes the early neural plate

The formation of complex tissues during embryonic development requires an intricate spatiotemporal coordination of local mechanical processes regulating global tissue morphogenesis. Here, we uncover a novel mechanism that mechanically regulates the shape of the anterior neural plate (ANP), a vital forebrain precursor, during zebrafish gastrulation. Combiningin vivoandin silicoapproaches we reveal that the ANP is shaped by global tissue flows regulated by distinct force generating processes. We show that mesendoderm migration and E-cadherin-dependent differential tissue interactions control distinct flow regimes in the neuroectoderm. Initial opposing flows lead to progressive tissue folding and neuroectoderm internalisation which in turn provide forces driving ANP tissue reshaping. We find that convergent extension is dispensable for internalisation but required for ANP tissue extension. Our results highlight how spatiotemporal regulation and coupling of different mechanical processe...

Quantifying mechanical forces during vertebrate morphogenesis

2022

Morphogenesis, the establishment of rudimentary organ structures, requires embryonic cells to generate forces and perform mechanical work to shape their tissues. Incorrect functioning of these force fields can lead to congenital malformations including neural tube defects. The understanding of these dynamic processes requires quantification and profiling of three-dimensional mechanics during evolving vertebrate morphogenesis, which is not tractable with current technology. We fabricated elastic spring-like force sensors with micron-level resolution directly into specific three-dimensional domains of the closing neural tubes of growing chicken embryos through intravital three-dimensional bioprinting. Integration of calibrated sensor readouts with computational mechanical modelling allows direct quantification of forces and work performed by embryonic tissues. The two halves of the closing neural tube at the embryonic midline reach over a hundred nano-Newton compression during neural ...

Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis

2019

Mechanical forces are critical for the emergence of diverse three-dimensional morphologies of multicellular systems. However, it remains unclear what kind of mechanical parameters at cellular level substantially contribute to tissue morphologies. This is largely due to technical limitations of live measurements of cellular forces. Here we developed a framework for inferring and modeling mechanical forces of cell–cell interactions. First, by analogy to coarse-grained models in molecular and colloidal sciences, we approximated cells as particles, where mean forces (i.e. effective forces) of pairwise cell–cell interactions are considered. Then, the forces were statistically inferred by fitting the mathematical model to cell tracking data. This method was validated by using synthetic cell tracking data resembling variousin vivosituations. Application of our method to the cells in the early embryos of mice and the nematodeCaenorhabditis elegansrevealed that cell–cell interaction forces c...