Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Self-straining of actively crosslinked microtubule networks

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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

Data availability

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

References

  1. Marchetti, M. C. et al. Hydrodynamics of soft active matter. Rev. Mod. Phys. 85, 1143–1189 (2013).

    Article  ADS  Google Scholar 

  2. Needleman, D. & Dogic, Z. Active matter at the interface between materials science and cell biology. Nat. Rev. Mater. 2, 17048 (2017).

    Article  ADS  Google Scholar 

  3. Alberts, B. et al. Molecular Biology of the Cell 4th edn (Garland, 2002).

  4. Kruse, K., Joanny, J.-F., Jülicher, F., Prost, J. & Sekimoto, K. Generic theory of active polar gels: a paradigm for cytoskeletal dynamics. Eur. Phys. J. E 16, 5–16 (2005).

    Article  Google Scholar 

  5. Joanny, J. F., Jülicher, F., Kruse, K. & Prost, J. Hydrodynamic theory for multi-component active polar gels. New J. Phys. 9, 422 (2007).

    Article  ADS  Google Scholar 

  6. Jülicher, F., Grill, S. W. & Salbreux, G. Hydrodynamic theory of active matter. Rep. Prog. Phys. 81, 076601 (2018).

    Article  MathSciNet  ADS  Google Scholar 

  7. Bray, D. Cell Movements: From Molecules to Motility 2nd edn (Garland, 2001).

  8. Naganathan, S. R. et al. Morphogenetic degeneracies in the actomyosin cortex. elife 7, e37677 (2018).

    Article  Google Scholar 

  9. Roostalu, J., Rickman, J., Thomas, C., Nédélec, F. & Surrey, T. Determinants of polar versus nematic organization in networks of dynamic microtubules and mitotic motors. Cell 175, 796–808 (2018).

    Article  Google Scholar 

  10. Foster, P. J., Fürthauer, S., Shelley, M. J. & Needleman, D. J. From cytoskeletal assemblies to living materials. Curr. Opin. Cell Biol. 56, 109–114 (2019).

    Article  Google Scholar 

  11. Mitchison, T. J. Mechanism and function of poleward flux in Xenopus extract meiotic spindles. Phil. Trans. R. Soc. Lond. B 360, 623–629 (2005).

    Article  Google Scholar 

  12. Burbank, K. S., Mitchison, T. J. & Fisher, D. S. Slide-and-cluster models for spindle assembly. Curr. Biol. 17, 1373–1383 (2007).

    Article  Google Scholar 

  13. Yang, G., Cameron, L. A., Maddox, P. S., Salmon, E. D. & Danuser, G. Regional variation of microtubule flux reveals microtubule organization in the metaphase meiotic spindle. J. Cell Biol. 182, 631–639 (2008).

    Article  Google Scholar 

  14. Fürthauer, S., Strempel, M., Grill, S. W. & Jülicher, F. Active chiral fluids. Eur. Phys. J. E 35, 1–13 (2012).

    Article  Google Scholar 

  15. Thampi, S. P., Golestanian, R. & Yeomans, J. M. Velocity correlations in an active nematic. Phys. Rev. Lett. 111, 118101 (2013).

    Article  ADS  Google Scholar 

  16. Salbreux, G., Prost, J. & Joanny, J.-F. Hydrodynamics of cellular cortical flows and the formation of contractile rings. Phys. Rev. Lett. 103, 058102 (2009).

    Article  ADS  Google Scholar 

  17. Mayer, M., Depken, M., Bois, J. S., Jülicher, F. & Grill, S. W. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467, 617–621 (2010).

    Article  ADS  Google Scholar 

  18. Naganathan, S. R., Fürthauer, S., Nishikawa, M., Jülicher, F. & Grill, S. W. Active torque generation by the actomyosin cell cortex drives left–right symmetry breaking. elife 3, e04165 (2014).

    Article  Google Scholar 

  19. Brugués, J. & Needleman, D. Physical basis of spindle self-organization. Proc. Natl Acad. Sci. USA 111, 18496–18500 (2014).

    Article  ADS  Google Scholar 

  20. Kruse, K. & Jülicher, F. Actively contracting bundles of polar filaments. Phys. Rev. Lett. 85, 1778–1781 (2000).

    Article  ADS  Google Scholar 

  21. Aranson, I. S. & Tsimring, L. S. Pattern formation of microtubules and motors: inelastic interaction of polar rods. Phys. Rev. E 71, 050901 (2005).

    Article  ADS  Google Scholar 

  22. Liverpool, T. B. & Marchetti, M. C. Bridging the microscopic and the hydrodynamic in active filament solutions. Europhys. Lett. 69, 846–852 (2005).

    Article  ADS  Google Scholar 

  23. Liverpool, T. B. & Marchetti, M. C. in Cell Motility (ed. Lenz, P.) 177–206 (Springer, 2008).

  24. Saintillan, D. & Shelley, M. J. Instabilities and pattern formation in active particle suspensions: kinetic theory and continuum simulations. Phys. Rev. Lett. 100, 178103 (2008).

    Article  ADS  Google Scholar 

  25. Saintillan, D. & Shelley, M. J. Instabilities, pattern formation and mixing in active suspensions. Phys. Fluids 20, 123304 (2008).

    Article  ADS  Google Scholar 

  26. Saintillan, D. & Shelley, M. J. Active suspensions and their nonlinear models. C. R. Phys. 14, 497–517 (2013).

    Article  ADS  Google Scholar 

  27. Foster, P. J., Fürthauer, S., Shelley, M. J. & Needleman, D. J. Active contraction of microtubule networks. eLife 4, e10837 (2015).

    Article  Google Scholar 

  28. Gao, T., Blackwell, R., Glaser, M. A., Betterton, M. D. & Shelley, M. J. Multiscale polar theory of microtubule and motor-protein assemblies. Phys. Rev. Lett. 114, 048101 (2015).

    Article  ADS  Google Scholar 

  29. Heidenreich, S., Dunkel, J., Klapp, S. H. L. & Bär, M. Hydrodynamic length-scale selection in microswimmer suspensions. Phys. Rev. E 94, 020601 (2016).

    Article  ADS  Google Scholar 

  30. Maryshev, I., Marenduzzo, D., Goryachev, A. B. & Morozov, A. Kinetic theory of pattern formation in mixtures of microtubules and molecular motors. Phys. Rev. E 97, 022412 (2018).

    Article  ADS  Google Scholar 

  31. Broedersz, C. P. & MacKintosh, F. C. Modeling semiflexible polymer networks. Rev. Mod. Phys. 86, 995 (2014).

    Article  ADS  Google Scholar 

  32. Ronceray, P. & Lenz, M. Connecting local active forces to macroscopic stress in elastic media. Soft Matter 11, 1597–1605 (2015).

    Article  ADS  Google Scholar 

  33. Ronceray, P., Broedersz, C. P. & Lenz, M. Fiber networks amplify active stress. Proc. Natl Acad. Sci. USA 113, 2827–2832 (2016).

    Article  ADS  Google Scholar 

  34. Belmonte, J. M., Leptin, M. & Nédélec, F. A theory that predicts behaviors of disordered cytoskeletal networks. Mol. Syst. Biol. 13, 941 (2017).

    Article  Google Scholar 

  35. Foster, P. J., Yan, W., Fürthauer, S., Shelley, M. J. & Needleman, D. J. Connecting macroscopic dynamics with microscopic properties in active microtubule network contraction. New J. Phys. 19, 125011 (2017).

    Article  ADS  Google Scholar 

  36. Hentrich, C. & Surrey, T. Microtubule organization by the antagonistic mitotic motors kinesin-5 and kinesin-14. J. Cell Biol. 189, 465–480 (2010).

    Article  Google Scholar 

  37. Yu, C.-H. et al. Measuring microtubule polarity in spindles with second-harmonic generation. Biophys. J. 106, 1578–1587 (2014).

    Article  ADS  Google Scholar 

  38. Brugués, J., Nuzzo, V., Mazur, E. & Needleman, D. J. Nucleation and transport organize microtubules in metaphase spindles. Cell 149, 554–564 (2012).

    Article  Google Scholar 

  39. Kapitein, L. C. et al. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 435, 114–118 (2005).

    Article  ADS  Google Scholar 

  40. Tan, R., Foster, P. J., Needleman, D. J. & McKenney, R. J. Cooperative accumulation of dynein–dynactin at microtubule minus-ends drives microtubule network reorganization. Dev. Cell 44, 233–247 (2018).

    Article  Google Scholar 

Download references

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

Authors

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.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41567-019-0642-1

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing