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Self-straining of actively crosslinked microtubule networks

Nature Physics volume 15, pages 1295–1300 (2019)Cite this article

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Abstract

Cytoskeletal networks are foundational examples of active matter and central to self-organized structures in the cell. In vivo, these networks are active and densely crosslinked. Relating their large-scale dynamics to the properties of their constituents remains an unsolved problem. Here, we study an in vitro active gel made from aligned microtubules and XCTK2 kinesin motors. Using photobleaching, we demonstrate that the gel’s aligned microtubules, driven by motors, continually slide past each other at a speed independent of the local microtubule polarity and motor concentration. This phenomenon is also observed, and remains unexplained, in spindles. We derive a general framework for coarse graining microtubule gels crosslinked by molecular motors from microscopic considerations. Using microtubule–microtubule coupling through a force–velocity relationship for kinesin, this theory naturally explains the experimental results: motors generate an active strain rate in regions of changing polarity, which allows microtubules of opposite polarities to slide past each other without stressing the material.

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Fig. 1: Bleaching of aligned active gels reveals microtubule sliding speed.
Fig. 2: Microtubule sliding speed is independent of polarity and motor concentration.
Fig. 3: Sketch of the microscopic model.

Data availability

Figures 1 and 2 are based on microscopy data. The raw data are available from the authors upon reasonable request.

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Acknowledgements

C.E.W. acknowledges support by NIH R35GM122482. D.J.N. acknowledges the Kavli Institute for Bionano Science and Technology at Harvard University and National Science Foundation grants PHY-1305254, PHY-0847188, DMR-0820484 and DBI-0959721. P.J.F. acknowledges support from the Gordon and Betty Moore Foundation for support as a Physics of Living Systems Fellow through grant no. GBMF4513. M.J.S. acknowledges support from National Science Foundation grants DMR-0820341 (NYU MRSEC), DMS-1463962 and DMS-1620331. Z.D. acknowledges support from NSF MRSEC DMR-1420382.

Author information

Authors and Affiliations

  1. Center for Computational Biology, Flatiron Institute, New York, NY, USA

    Sebastian Fürthauer & Michael J. Shelley

  2. Department of Physics, Harvard University, Cambridge, MA, USA

    Bezia Lemma

  3. Department of Physics, Brandeis University, Waltham, MA, USA

    Bezia Lemma & Zvonimir Dogic

  4. Department of Physics, University of California, Santa Barbara, CA, USA

    Bezia Lemma & Zvonimir Dogic

  5. Physics of Living Systems, Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, USA

    Peter J. Foster

  6. Medical Sciences, Indiana University, Bloomington, IN, USA

    Stephanie C. Ems-McClung & Claire E. Walczak

  7. Department of Electrical and Computer Engineering, University of California, Santa Barbara, CA, USA

    Che-Hang Yu

  8. Paulson School of Engineering & Applied Science and Department of Molecular & Cellular Biology, Harvard University, Cambridge, MA, USA

    Daniel J. Needleman

  9. Courant Institute, New York University, New York, NY, USA

    Michael J. Shelley

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  1. Sebastian Fürthauer
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Contributions

S.F., M.J.S. and D.J.N. developed the theory. B.L., P.J.F., S.C.E.-M., C.-H.Y., C.E.W. and Z.D. performed experiments and provided materials. S.F., B.L., D.J.N. and M.J.S. wrote the paper with input from all authors.

Corresponding author

Correspondence to Sebastian Fürthauer.

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The authors declare no competing interests.

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Peer review information: Nature Physics thanks Karin John, Gijsje Koenderink and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Information, Figs. 1–4 and refs. 1–17.

Reporting Summary

Supplementary Video 1

Fluorescent microtubule material with 0.4 µM XCTK2.

Supplementary Video 2

Fluorescent microtubule material with 0.75 µM XCTK2.

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Fürthauer, S., Lemma, B., Foster, P.J. et al. Self-straining of actively crosslinked microtubule networks. Nat. Phys. 15, 1295–1300 (2019). https://doi.org/10.1038/s41567-019-0642-1

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