Research ArticleBIOPHYSICS

Viscoelastic properties of vimentin originate from nonequilibrium conformational changes

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Science Advances  13 Jun 2018:
Vol. 4, no. 6, eaat1161
DOI: 10.1126/sciadv.aat1161
  • Fig. 1 Experimental setup, vimentin assembly, and comparison of effective two-state model and experimental data.

    (A) Top: Microfluidic chip. Middle: Schematic representation of vimentin assembly. Bottom: Secondary structure of the IF monomer; α-helical rod, subdivided into the three α helices, 1A, 1B, and 2, and intrinsically disordered head and tail domains. (B) Force-strain cycles of single vimentin filaments at different loading rates. (C) Force-strain cycles for different loading rates [color-coded as in (B)] calculated by the effective two-state model. (D) Dissipated energy during individual stretching cycles. (E) Comparison between energy dissipation measured for 75 different filaments at five different velocities between 50 and 2450 nm/s (dark blue dots) and prediction by the two-state model (black); nonequilibrium transition between α helices and β sheets (red); viscous dissipation (light blue). Error bars indicate SD.

  • Fig. 2 Response to repeated strain.

    (A) Top: Distance versus time. Bottom: Force versus strain for a typical filament. (B) Kinetic MC simulations of a simplified vimentin filament that take into account 32 monomers per cross section (inset) reproduce a curve progression resembling the experiment. The force and extension in (B) are given in arbitrary units (a.u.) of force and distance. (C) Fitting the linear regime of the stretching part of every cycle [(A); up to 10% strain] yields the stiffness for each cycle. The progression with cycle number for 77 different filaments is shown. Magenta, average stiffness per cycle. Error bars indicate SEM. (D) Every monomer within the simulated IF is traced by the MC simulation. Transition of the 32 α helices of eight individual ULFs (color-coded) within one filament.

  • Fig. 3 Response of individual vimentin IFs to applied constant force.

    (A and B) Examples of single vimentin filaments responding to a constant force (FC) of 500 and 50 pN, respectively. Top: Constant force versus time. Bottom: Filament extension versus time. Right: Histogram of filament length; power-law fit (red line). (C) Log-log plot of the filament strain versus time for FC experiments on about 100 vimentin filaments at different forces from 50 to 700 pN. The three single curves in orange, green, and magenta show the prediction of the two-state model for a filament responding to a constant force of 50, 100, and 250 pN, respectively. The cartoons illustrate the two elongation mechanisms. Top: Viscous sliding. Bottom: α-β transition. (D) Histogram of all steps. (E) Power-law coefficients found for filaments at 500- and 700-pN FCs.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/4/6/eaat1161/DC1

    fig. S1. Vimentin assembly: IF formation follows a complex and hierarchical scheme.

    fig. S2. Comparison of calculated (two-state model) stretching and relaxation curves for different values of the persistence lengths LP (color-coded; see legend).

    fig. S3. Sketch of the equivalent circuit diagram used for setting up the MC simulations.

    fig. S4. Step size analysis of FC data sets.

    fig. S5. Step size analysis of data sets with filaments covalently bond to beads via malemide chemistry.

    fig. S6. Step size analysis of relaxation data sets.

    fig. S7. Vimentin relaxation experiments starting from different forces.

    fig. S8. Data corresponding to the cycle shown in movie S1.

    fig. S9. Quality control of labeled, assembled vimentin filaments.

    fig. S10. Simulations, cycles, and comparison for different numbers of monomers per ULF.

    movie S1. Epifluorescence video of an example stretching cycle of a single vimentin filament.

    data file S1. Jupyter Notebook for MC simulations.

    Reference (45)

  • Supplementary Materials

    This PDF file includes:

    • fig. S1. Vimentin assembly: IF formation follows a complex and hierarchical scheme.
    • fig. S2. Comparison of calculated (two-state model) stretching and relaxation curves for different values of the persistence lengths LP (color-coded; see legend).
    • fig. S3. Sketch of the equivalent circuit diagram used for setting up the MC simulations.
    • fig. S4. Step size analysis of FC data sets.
    • fig. S5. Step size analysis of data sets with filaments covalently bond to beads via malemide chemistry.
    • fig. S6. Step size analysis of relaxation data sets.
    • fig. S7. Vimentin relaxation experiments starting from different forces.
    • fig. S8. Data corresponding to the cycle shown in movie S1.
    • fig. S9. Quality control of labeled, assembled vimentin filaments.
    • fig. S10. Simulations, cycles, and comparison for different numbers of monomers per ULF.
    • Legend for movie S1
    • Reference (45)

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    Other Supplementary Material for this manuscript includes the following:

    • movie S1 (.avi format). Epifluorescence video of an example stretching cycle of a single vimentin filament.
    • data file S1 (.ipynb format). Jupyter Notebook for MC simulations.

    Files in this Data Supplement:

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