Force measurements of Myosin II waves at the yolk surface during Drosophila dorsal closure

Selvaggi, Lara; Ackermann, Mathias; Pasakarnis, Laurynas; Brunner, Damian; Aegerter, Christof M.

doi:10.1016/j.bpj.2021.12.038

Cited by 4 publications

(8 citation statements)

References 35 publications

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“…To induce epithelial tissue curvature for furrowing, Drosophila constricts apical cell surfaces using actomyosin networks. Similar actomyosin networks were recently measured by magnetic tweezers to exert forces T myo ∼ 1-1.5 nN during Drosophila dorsal closure 69 . Elastic resistance cannot compete with such forces: the elastic constant for apical cell deformation was measured to be k = 7 pN μm −1 using magnetic beads during late Drosophila cellularization 19 , so even for complete apical constriction (cell width decrease Δ L ∼ 7 μm), the elastic resistance k Δ L ∼50 pN is over 20-fold smaller.…”

Section: Discussionsupporting

confidence: 77%

“…( 3) Using ܶ ୫୷୭ ‫כ‬ ~ 1.5 nN from ref. 20 and the above values of ߦ and ‫ݓ‬ ‫כ‬ , we obtain estimated values for the external drag coefficient ߣ~6 pN s nm ିଵ , and for the intracellular viscosity ߤ~36 pN s nm ିଵ (Table 1). For details, see Supplementary Information.…”

Section: Methodsmentioning

confidence: 99%

“…S1). (3) Using from ref 20 . and the above values of ξ and w *, we obtain estimated values for the external drag coefficient λ ∼ 6 pN s nm-1, and for the intracellular viscosity μ ∼ 36 pN s nm-1 (Table 1).…”

Section: Methodsmentioning

confidence: 99%

“…We now argue the elastic term is small and can be discarded. A recent magnetic tweezers study measured single cell apical myosin contractile stresses 𝑇 myo ~ 1-1.5 nN during Drosophila dorsal closure 20 . For the elastic constant we use 𝑘 = 7 pN μm −1 measured in the experiments of ref.…”

Section: 𝑇 Myo (𝑛 + 1) − 𝑇 Myo (𝑛 − 1) − 𝜇[𝑤(𝑛 + 1) − 𝑤(𝑛 − 1)] + 𝑘[∆...mentioning

confidence: 99%

“…These elasticity-based models predict collective cell contraction and furrowing, but have serious shortcomings. First, the experimentally reported elastic constant for apical cell constriction is ~ 7 pN µm ିଵ 19 , far too small to resist the myosin contractile forces of ~ 1-1.5 nN exerted by a Drosophila apical network 20 . Second, in wild type embryos the myosin profile during VFF has no curvature in the anterior-posterior direction, and cells do not contract in that direction 7 .…”

Section: Introductionmentioning

confidence: 99%

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Actomyosin pulsing rescues embryonic tissue folding from disruption by myosin fluctuations

Zhu

O’Shaughnessy

2023

Preprint

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During early development, myosin II mechanically reshapes and folds embryo tissue. A much-studied example is ventral furrow formation in Drosophila, marking the onset of gastrulation. Furrowing is driven by contraction of actomyosin networks on apical cell surfaces, but how the myosin patterning encodes tissue shape is unclear, and elastic models failed to reproduce essential features of experimental cell contraction profiles. The myosin patterning exhibits substantial cell-to-cell fluctuations with pulsatile time-dependence, a striking but unexplained feature of morphogenesis in many organisms. Here, using biophysical modeling we find viscous forces offer the principle resistance to actomyosin-driven apical constriction. In consequence, tissue shape is encoded in the direction-dependent curvature of the myosin patterning which orients an anterior-posterior furrow. Tissue contraction is highly sensitive to cell-to-cell myosin fluctuations, explaining furrowing failure in genetically perturbed embryos whose fluctuations are temporally persistent. In wild-type embryos, this catastrophic outcome is averted by pulsatile myosin time-dependence, a time-averaging effect that rescues furrowing. This low pass filter mechanism may underlie the usage of actomyosin pulsing in diverse morphogenetic processes across many organisms.

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Section: Discussionsupporting

confidence: 77%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: 𝑇 Myo (𝑛 + 1) − 𝑇 Myo (𝑛 − 1) − 𝜇[𝑤(𝑛 + 1) − 𝑤(𝑛 − 1)] + 𝑘[∆...mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Actomyosin pulsing rescues embryonic tissue folding from disruption by myosin fluctuations

Zhu

O’Shaughnessy

2023

Preprint

View full text Add to dashboard Cite

show abstract

Actomyosin pulsing rescues embryonic tissue folding from disruption by myosin fluctuations

Zhu,

O'Shaughnessy

2023

Preprint

View full text Add to dashboard Cite

During early development, myosin II mechanically reshapes and folds embryo tissue. A much-studied example is ventral furrow formation in Drosophila, marking the onset of gastrulation. Furrowing is driven by contraction of actomyosin networks on apical cell surfaces, but how the myosin patterning encodes tissue shape is unclear, and elastic models failed to reproduce essential features of experimental cell contraction profiles. The myosin patterning exhibits substantial cell-to-cell fluctuations with pulsatile time-dependence, a striking but unexplained feature of morphogenesis in many organisms. Here, using biophysical modeling we find viscous forces offer the principal resistance to actomyosin-driven apical constriction. In consequence, tissue shape is encoded in the direction-dependent curvature of the myosin patterning which orients an anterior-posterior furrow. Tissue contraction is highly sensitive to cell-to-cell myosin fluctuations, explaining furrowing failure in genetically perturbed embryos whose fluctuations are temporally persistent. In wild-type embryos this disastrous outcome is averted by pulsatile myosin time-dependence, which rescues furrowing by eliminating high frequencies in the fluctuation power spectrum. This low pass filter mechanism may underlie the usage of actomyosin pulsing in diverse morphogenetic processes across many organisms.

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A Markov chain Monte Carlo model of mechanical-feedback-driven progressive apical constrictions captures the fluctuating collective cell dynamics in the Drosophila embryo

Gao

Holcomb²,

Thomas³

et al. 2022

Front. Phys.

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Communication via mechanical stress feedback is believed to play an important role in the intercellular coordination of collective cellular movements. One such movement is ventral furrow formation (VFF) in the Drosophila melanogaster embryo. We previously introduced an active granular fluid (AGF) model, which demonstrated that cellular constriction chains observed during the initial phase of VFF are likely the result of intercellular coordination by tensile-stress feedback. Further observation of individual cellular dynamics motivated us to introduce progressive constrictions and Markov chain Monte Carlo based fluctuation of particle radii to our AGF model. We use a novel stress-based Voronoi tessellation method to translate the anisotropic network of highly polydisperse, axisymmetric force centers into a confluent cellular layer. This allows us to apply a similar means of analysis to both live and simulated embryos. We find that our enhanced AGF model, which combines tensile mechanical stress feedback and individual cellular fluctuations, successfully captures collective cell dynamics.

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Force measurements of Myosin II waves at the yolk surface during Drosophila dorsal closure

Cited by 4 publications

References 35 publications

Actomyosin pulsing rescues embryonic tissue folding from disruption by myosin fluctuations

Actomyosin pulsing rescues embryonic tissue folding from disruption by myosin fluctuations

Actomyosin pulsing rescues embryonic tissue folding from disruption by myosin fluctuations

A Markov chain Monte Carlo model of mechanical-feedback-driven progressive apical constrictions captures the fluctuating collective cell dynamics in the Drosophila embryo

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