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Edited by David A. Weitz, Harvard University, Cambridge, MA, and approved January 10, 2017 (received for review September 28, 2016)
Significance
The interior of biological cells is composed of soft, macromolecular-based materials. The semiflexible biopolymer actin cross-links into networks and bundles with diverse architectures to form the actin cytoskeleton. Actin networks have been traditionally thought to be viscoelastic gels, whose rigidity controls cell morphogenesis. Here we demonstrate that cross-linked actin filaments also form liquid droplets. Because these liquids are composed of rod-like polymers, they form anisotropic liquid droplets with a spindle-like shape, whose morphology can be controlled by cross-link concentration. Actin-based liquid bundles also display shape instabilities characteristic of fluids. These shape dynamics reveal a mechanism to control subcellular compartmentalization and dynamics, with implications for mitotic spindle shape and molecular motor-independent contractility.
Abstract
The actin cytoskeleton is a critical regulator of cytoplasmic architecture and mechanics, essential in a myriad of physiological processes. Here we demonstrate a liquid phase of actin filaments in the presence of the physiological cross-linker, filamin. Filamin condenses short actin filaments into spindle-shaped droplets, or tactoids, with shape dynamics consistent with a continuum model of anisotropic liquids. We find that cross-linker density controls the droplet shape and deformation timescales, consistent with a variable interfacial tension and viscosity. Near the liquid–solid transition, cross-linked actin bundles show behaviors reminiscent of fluid threads, including capillary instabilities and contraction. These data reveal a liquid droplet phase of actin, demixed from the surrounding solution and dominated by interfacial tension. These results suggest a mechanism to control organization, morphology, and dynamics of the actin cytoskeleton.
Footnotes
- ↵1To whom correspondence should be addressed. Email: gardel{at}uchicago.edu.
Author contributions: K.L.W., S.B., S.V., and M.L.G. designed research; K.L.W. performed experiments; S.B. and K.D. developed the model; K.L.W., S.B., K.D., T.A.W., S.V., and M.L.G. contributed new reagents/analytic tools; K.L.W., S.B., and K.D. analyzed data; and K.L.W., S.B., K.D., S.V., and M.L.G. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1616133114/-/DCSupplemental.
Liquid behavior of cross-linked actin bundles
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- Experimental Assay
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- Filament Length, Mesh Size, and Filament Spacing
- Fluorescence Recovery After Photobleaching and Viscosity Estimate
- Continuum Theory of Elongated Droplets
- Equilibrium Droplet Shapes
- Size Dependence of Tactoid Aspect Ratio
- Droplet Shape Dynamics
- Capillary Instabilities in Long Droplets
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