Contribution of cytoplasm viscoelastic properties to mitotic spindle positioning.

Contribution of cytoplasm viscoelastic properties to mitotic spindle positioning.
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DOI:
10.1073/pnas.2115593119
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发表时间:
2022-02-22
影响因子:
11.1
通讯作者:
Minc N
Minc N
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Xie J;Najafi J;Le Borgne R;Verbavatz JM;Durieu C;Sallé J;Minc N

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The regulation of mitotic spindle positioning is a key process for tissue architecture, embryo development, and stem cells. To date, most models have assumed that spindles are positioned by forces exerted by polar cytoskeleton networks, like microtubule asters or actomyosin bundles. Here, using in situ magnetic tweezers to apply calibrated forces and torques to mitotic spindles in live dividing sea urchin cells, we found that the viscoelastic properties of the cytoplasm medium in which spindles are embedded can hold spindles in place and move them back if their original position is perturbed. These viscoelastic forces are large and may significantly participate in the force balance that position and orient mitotic spindles in many cell types. Cells are filled with macromolecules and polymer networks that set scale-dependent viscous and elastic properties to the cytoplasm. Although the role of these parameters in molecular diffusion, reaction kinetics, and cellular biochemistry is being increasingly recognized, their contributions to the motion and positioning of larger organelles, such as mitotic spindles for cell division, remain unknown. Here, using magnetic tweezers to displace and rotate mitotic spindles in living embryos, we uncovered that the cytoplasm can impart viscoelastic reactive forces that move spindles, or passive objects with similar size, back to their original positions. These forces are independent of cytoskeletal force generators yet reach hundreds of piconewtons and scale with cytoplasm crowding. Spindle motion shears and fluidizes the cytoplasm, dissipating elastic energy and limiting spindle recoils with functional implications for asymmetric and oriented divisions. These findings suggest that bulk cytoplasm material properties may constitute important control elements for the regulation of division positioning and cellular organization.
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