Viscoelastic properties of vimentin originate from nonequilibrium conformational changes

Johanna Block; Hannes Witt; Andrea Candelli; Jordi Cabanas Danes; Erwin J.G. Peterman; Gijs J.L. Wuite; Andreas Janshoff; Sarah Köster

doi:10.1126/sciadv.aat1161

Viscoelastic properties of vimentin originate from nonequilibrium conformational changes

Johanna Block
, Hannes Witt
, Andrea Candelli
, Jordi Cabanas Danes
, Erwin J.G. Peterman
, Gijs J.L. Wuite
, Andreas Janshoff^*
, Sarah Köster

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Structure and dynamics of living matter rely on design principles fundamentally different from concepts of traditional material science. Specialized intracellular filaments in the cytoskeleton permit living systems to divide, migrate, and grow with a high degree of variability and durability. Among the three filament systems, microfilaments, microtubules, and intermediate filaments (IFs), the physical properties of IFs and their role in cellular mechanics are the least well understood. We use optical trapping of individual vimentin filaments to investigate energy dissipation, strain history dependence, and creep behavior of stretched filaments. By stochastic and numerical modeling, we link our experimental observations to the peculiar molecular architecture of IFs. We find that individual vimentin filaments display tensile memory and are able to dissipate more than 70% of the input energy. We attribute these phenomena to distinct nonequilibrium folding and unfolding of a helices in the vimentin monomers constituting the filaments.

Original language	English
Article number	eaat1161
Journal	Science Advances
Volume	4
Issue number	6
DOIs	https://doi.org/10.1126/sciadv.aat1161
Publication status	Published - 13 Jun 2018

Funding

We are thankful for the discussions and technical support by S. Bauch, A. Schepers, J. Kraxner, F. Savić, and B. Geil. This project has received funding from the European Research Council under the European Union’s Horizon 2020 research and innovation program (Consolidator grant agreement no. 724932 and Laserlab-Europe grant agreement no. 654148). The work was further financially supported by the Deutsche Forschungsgemeinschaft in the framework of SFB755 (project B7) and SFB937 (project A17), as well as the Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences (grant no. GSC 226/2).

Funders	Funder number
Horizon 2020 Framework Programme	654148, 724932
European Research Council
Deutsche Forschungsgemeinschaft	SFB755, SFB937
Göttinger Graduiertenschule für Neurowissenschaften, Biophysik und Molekulare Biowissenschaften	GSC 226/2

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This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 7 Affordable and Clean Energy

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10.1126/sciadv.aat1161

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title = "Viscoelastic properties of vimentin originate from nonequilibrium conformational changes",

abstract = "Structure and dynamics of living matter rely on design principles fundamentally different from concepts of traditional material science. Specialized intracellular filaments in the cytoskeleton permit living systems to divide, migrate, and grow with a high degree of variability and durability. Among the three filament systems, microfilaments, microtubules, and intermediate filaments (IFs), the physical properties of IFs and their role in cellular mechanics are the least well understood. We use optical trapping of individual vimentin filaments to investigate energy dissipation, strain history dependence, and creep behavior of stretched filaments. By stochastic and numerical modeling, we link our experimental observations to the peculiar molecular architecture of IFs. We find that individual vimentin filaments display tensile memory and are able to dissipate more than 70\% of the input energy. We attribute these phenomena to distinct nonequilibrium folding and unfolding of a helices in the vimentin monomers constituting the filaments.",

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AU - Block, Johanna

AU - Witt, Hannes

AU - Candelli, Andrea

AU - Danes, Jordi Cabanas

AU - Peterman, Erwin J.G.

AU - Wuite, Gijs J.L.

AU - Janshoff, Andreas

AU - Köster, Sarah

PY - 2018/6/13

Y1 - 2018/6/13

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AB - Structure and dynamics of living matter rely on design principles fundamentally different from concepts of traditional material science. Specialized intracellular filaments in the cytoskeleton permit living systems to divide, migrate, and grow with a high degree of variability and durability. Among the three filament systems, microfilaments, microtubules, and intermediate filaments (IFs), the physical properties of IFs and their role in cellular mechanics are the least well understood. We use optical trapping of individual vimentin filaments to investigate energy dissipation, strain history dependence, and creep behavior of stretched filaments. By stochastic and numerical modeling, we link our experimental observations to the peculiar molecular architecture of IFs. We find that individual vimentin filaments display tensile memory and are able to dissipate more than 70% of the input energy. We attribute these phenomena to distinct nonequilibrium folding and unfolding of a helices in the vimentin monomers constituting the filaments.

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Viscoelastic properties of vimentin originate from nonequilibrium conformational changes

Abstract

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UN SDGs

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