Measurement of cortical elasticity in
            <i>Drosophila melanogaster</i>
            embryos using ferrofluids

Doubrovinski, Konstantin; Swan, M.K.; Polyakov, Oleg Yurievich; Wieschaus, Eric

doi:10.1073/pnas.1616659114

Cited by 111 publications

(185 citation statements)

References 27 publications

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“…This suggests that the initially solid-like tissue may be poised near this transition to allow for rapid cell rearrangement and tissue flow with small changes in cell properties or under small applied forces, while still maintaining tissue integrity. This is possibly consistent with recent ferrofluid droplet and magnetic bead microrheology measurements of tissues in the cellularizing Drosophila embryo prior to axis elongation, which indicated that tissue behavior is predominantly elastic (solid-like) over timescales less than several minutes (45,46). While both studies compared the long-time tissue behavior to fluid-like viscous models, their observations might also be consistent with a weak yield-stress solid, which is solid-like for small stresses but deforms plastically and flows for larger stresses.…”

Section: Discussionsupporting

confidence: 86%

“…Cell stretching along the AP axis also contributes to tissue elongation and coincides with movements of neighboring tissues (26-28, 42, 43), indicating that external forces play an important role in tissue behavior. Despite significant study of this tissue, a comprehensive framework for understanding its mechanical behavior is lacking, in part because direct mechanical measurements inside the Drosophila embryo, and more generally for epithelial tissues in vivo, continue to be a challenge (44)(45)(46).…”

Section: Resultsmentioning

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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Section: Discussionsupporting

confidence: 86%

Section: Resultsmentioning

confidence: 99%

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

Wang

Merkel

Sutter

et al. 2019

Preprint

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“…This generates a Brillouin spectrum where the scattered light displays a frequency shift compared to the illumination light, from which the longitudinal modulus can be measured if the refractive index and density of the material is known. MBs-based methodologies have been used to measure viscoelastic properties of embryonic tissues such as elasticity of the trophectoderm and inner cell mass of the mouse blastocyst and mouse limb bud (preprint: Zhu et al, 2018) and Young modulus, shear viscosity and bulk viscosity of the Drosophila blastoderm during cellularization (Doubrovinski et al, 2017;D'Angelo et al, 2019). In addition, from the linewidth of the Brillouin peaks the viscosity of the tissue can be obtained (preprint: Prevedel et al, 2019).…”

Section: Rheologymentioning

confidence: 99%

“…By monitoring the extend of the bead movement during the application and removal of the magnetic force, the viscoelastic properties of the surrounding tissue can be quantified using simple mechanical models (Savin et al, 2011). MBs-based methodologies have been used to measure viscoelastic properties of embryonic tissues such as elasticity of the trophectoderm and inner cell mass of the mouse blastocyst and mouse limb bud (preprint: Zhu et al, 2018) and Young modulus, shear viscosity and bulk viscosity of the Drosophila blastoderm during cellularization (Doubrovinski et al, 2017;D'Angelo et al, 2019). Similar to the FDs, measuring tissue rheology through MBs at larger scales requires insertion of multiple beads within the tissue and the application of a uniform and strong magnetic field, a non-trivial approach when, e.g., using magnetic tweezers.…”

Section: Rheologymentioning

confidence: 99%

Tissue rheology in embryonic organization

2019

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Tissue morphogenesis in multicellular organisms is brought about by spatiotemporal coordination of mechanical and chemical signals. Extensive work on how mechanical forces together with the well‐established morphogen signalling pathways can actively shape living tissues has revealed evolutionary conserved mechanochemical features of embryonic development. More recently, attention has been drawn to the description of tissue material properties and how they can influence certain morphogenetic processes. Interestingly, besides the role of tissue material properties in determining how much tissues deform in response to force application, there is increasing theoretical and experimental evidence, suggesting that tissue material properties can abruptly and drastically change in development. These changes resemble phase transitions, pointing at the intriguing possibility that important morphogenetic processes in development, such as symmetry breaking and self‐organization, might be mediated by tissue phase transitions. In this review, we summarize recent findings on the regulation and role of tissue material properties in the context of the developing embryo. We posit that abrupt changes of tissue rheological properties may have important implications in maintaining the balance between robustness and adaptability during embryonic development.

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“…Beside the force generating mechanism, the material properties of the embryos (22)(23)(24) may influence the movement of the nuclei. The actin cytoskeleton inhibits short time-scale movements (21) and promotes ordering of the nuclear array (14).…”

Section: Introductionmentioning

confidence: 99%

The emergent Yo-yo movement of nuclei driven by collective cytoskeletal remodeling in pseudo-synchronous mitotic cycles

Rosenbaum

Mohr

et al. 2019

Preprint

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23Many aspects in tissue morphogenesis relay on the collective behavior of 24 participating cells. Despite a good understand of the underlying individual 25 processes, the mechanism for emergence of dynamic tissue behavior is 26 unclear in most cases. Here we reveal how isotropic elongation of mitotic 27 spindles drives an anisotropic collective flow of the nuclear array in syncytial 28Drosophila embryos. We found that the asynchrony of nuclear divisions, which 29is visible as a mitotic wave front sweeping over the embryo, allows elongation 30 of mitotic spindles beyond the average of inter-nuclear distances. As a 31 consequence of this overshooting, adjacent nuclei are pushed apart in early 32interphase. Strikingly, the nuclei anisotropically move several nuclear diameter 33 away from the mitotic wave front, albeit the orientation of spindles was 34 isotropic. Shortly afterwards the nuclei return to their original position in a type 35 of elastic movement. We found that spindle overshooting drove directional 36 nuclear flow and that the elastic back and forth movement was controlled by 37 cortical actin. The nuclear array did not return to its original position in mutants 38 of the formin Dia and moved three times further away without returning in 39 mutants of the Rac activator ELMO. The actin cortex effectively acts as a 40viscoelastic material with an ELMO-depending apparent viscosity and dia-and 41ELMO-dependent apparent elasticity. Our analysis provides insight into the 42 2 molecular mechanism leading to the emergence of a collective flow 43 movement. 44 45

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Measurement of cortical elasticity in Drosophila melanogaster embryos using ferrofluids

Cited by 111 publications

References 27 publications

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

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

Tissue rheology in embryonic organization

The emergent Yo-yo movement of nuclei driven by collective cytoskeletal remodeling in pseudo-synchronous mitotic cycles

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