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Non-specific adhesive forces between filaments and membraneless organelles

Thomas J. Böddeker, Kathryn A. Rosowski, Doris Berchtold, Leonidas Emmanouilidis, Yaning Han, Frédéric H. T. Allain, Robert W. Style, Lucas Pelkmans, Eric R. Dufresne
doi: https://doi.org/10.1101/2021.07.22.453380
Thomas J. Böddeker
1Department of Materials, ETH Zurich, Zurich, Switzerland
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Kathryn A. Rosowski
1Department of Materials, ETH Zurich, Zurich, Switzerland
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Doris Berchtold
2Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
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Leonidas Emmanouilidis
3Institute of Biochemistry, ETH Zurich, Switzerland
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Yaning Han
3Institute of Biochemistry, ETH Zurich, Switzerland
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Frédéric H. T. Allain
3Institute of Biochemistry, ETH Zurich, Switzerland
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Robert W. Style
1Department of Materials, ETH Zurich, Zurich, Switzerland
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Lucas Pelkmans
2Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
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Eric R. Dufresne
1Department of Materials, ETH Zurich, Zurich, Switzerland
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  • For correspondence: eric.dufresne@mat.ethz.ch
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Abstract

Membraneless organelles are liquid-like domains that form inside living cells by phase-separation. While standard physical models of their formation assume their surroundings to be a simple liquid, the cytoplasm is an active viscoelastic environment. To investigate potential coupling of phase separation with the cytoskeleton, we quantify structural correlations of stress granules and microtubules in a human-derived epithelial cell line. We find that microtubule networks are significantly perturbed in the vicinity of stress granules, and that large stress granules conform to the local pore-structure of the microtubule network. When microtubules are depolymerized by nocodazole, tubulin enrichment is localized near the surface of stress granules. We interpret these data using a thermodynamic model of partitioning of particles to the surface and bulk of droplets. This analysis shows that proteins generically have a non-specific affinity for droplet interfaces, which becomes most apparent when they weakly partition to the bulk of droplets and have a large molecular weight. In this framework, our data is consistent with a weak (≲ kbT) affinity of tubulin sub-units for stress granule interfaces. As microtubules polymerize their affinity for interfaces increases, providing sufficient adhesion to deform droplets and/or the network. We validate this basic physical phenomena in vitro through the interaction of a simple protein-RNA condensate with tubulin and microtubules.

Competing Interest Statement

The authors have declared no competing interest.

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Posted July 23, 2021.
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Non-specific adhesive forces between filaments and membraneless organelles
Thomas J. Böddeker, Kathryn A. Rosowski, Doris Berchtold, Leonidas Emmanouilidis, Yaning Han, Frédéric H. T. Allain, Robert W. Style, Lucas Pelkmans, Eric R. Dufresne
bioRxiv 2021.07.22.453380; doi: https://doi.org/10.1101/2021.07.22.453380
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Non-specific adhesive forces between filaments and membraneless organelles
Thomas J. Böddeker, Kathryn A. Rosowski, Doris Berchtold, Leonidas Emmanouilidis, Yaning Han, Frédéric H. T. Allain, Robert W. Style, Lucas Pelkmans, Eric R. Dufresne
bioRxiv 2021.07.22.453380; doi: https://doi.org/10.1101/2021.07.22.453380

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