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Contribution of cytoplasm viscoelastic properties to mitotic spindle positioning

Jing Xie, Javad Najafi, Rémi Le Borgne, Jean‐Marc Verbavatz, Catherine Pioche‐Durieu, Jérémy Sallé, Nicolas Minc

2022Proceedings of the National Academy of Sciences86 citationsDOIOpen Access PDF

Abstract

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.

Topics & Concepts

CytoplasmMagnetic tweezersMitosisCell biologyOrganelleCell divisionCytoskeletonViscoelasticitySpindle apparatusMicrotubuleBiologyBiophysicsCellPhysicsGeneticsDNAThermodynamicsMicrotubule and mitosis dynamicsCellular Mechanics and InteractionsPhotosynthetic Processes and Mechanisms