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.

  • Letter
  • Published:

Molecular wear of microtubules propelled by surface-adhered kinesins

Nature Nanotechnology volume 10, pages 166–169 (2015)Cite this article

Subjects

Abstract

Wear is the progressive loss of material from a body caused by contact and relative movement and is a major concern in both engineering and biology1,2,3,4. Advances in nanotechnology have allowed the origins of wear processes to be studied at the atomic and molecular scale, but also demand that wear in nanoscale systems can be predicted and controlled5,6,7. Biomolecular systems can undergo a range of active movements at the nanoscale, which are enabled by the transduction of chemical energy into mechanical work by polymerization processes and motor proteins8. The active movements are accompanied by dissipative processes that can be conceptually understood as ‘protein friction’9,10. Here, we show that wear also occurs in an in vitro system consisting of microtubules gliding across a surface coated with kinesin-1 motor proteins, and that energetic considerations suggest a molecule-by-molecule removal of tubulin proteins. The rates of removal show a complex dependence on sliding velocity and kinesin density, which, in contrast to the friction behaviour between microtubules and kinesin-8, cannot be explained by simple chemical reaction kinetics.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Length measurements of gliding microtubules.
Figure 2: Microtubule shrinking rates.

Similar content being viewed by others

References

  1. Ludema, K. C. Friction, Wear, Lubrication: A Textbook in Tribology (CRC Press, 1996).

    Book  Google Scholar 

  2. Norton, R. L. Machine Design: An Integrated Approach (Prentice Hall, 2011).

    Google Scholar 

  3. Hutchings, I. M. Tribology: Friction and Wear of Engineering Materials (CRC Press, 1992).

    Google Scholar 

  4. Erickson, G. M. et al. Complex dental structure and wear biomechanics in hadrosaurid dinosaurs. Science 338, 98–101 (2012).

    Article  CAS  Google Scholar 

  5. Bhushan, B. Nanotribology and nanomechanics in nano/biotechnology. Phil. Trans. R. Soc. Lond. A 366, 1499–1537 (2008).

    Article  CAS  Google Scholar 

  6. Gao, G. T., Mikulski, P. T. & Harrison, J. A. Molecular-scale tribology of amorphous carbon coatings: effects of film thickness, adhesion, and long-range interactions. J. Am. Chem. Soc. 124, 7202–7209 (2002).

    Article  CAS  Google Scholar 

  7. Jacobs, T. D. B. & Carpick, R. W. Nanoscale wear as a stress-assisted chemical reaction. Nature Nanotech. 8, 108–112 (2013).

    Article  CAS  Google Scholar 

  8. Howard, J. Mechanics of Motor Proteins and the Cytoskeleton (Sinauer, 2001).

    Google Scholar 

  9. Bormuth, V., Varga, V., Howard, J. & Schaffer, E. Protein friction limits diffusive and directed movements of kinesin motors on microtubules. Science 325, 870–873 (2009).

    Article  CAS  Google Scholar 

  10. Tawada, K. & Sekimoto, K. Protein friction exerted by motor enzymes through a weak-binding interaction. J. Theor. Biol. 150, 193–200 (1991).

    Article  CAS  Google Scholar 

  11. Varga, V., Leduc, C., Bormuth, V., Diez, S. & Howard, J. Kinesin-8 motors act cooperatively to mediate length-dependent microtubule depolymerization. Cell 138, 1174–1183 (2009).

    Article  CAS  Google Scholar 

  12. Wilson, L. et al. Taxol stabilization of microtubules in vitro—dynamics of tubulin addition and loss at opposite microtubule ends. Biochemistry 24, 5254–5262 (1985).

    Article  CAS  Google Scholar 

  13. Schiff, P. B., Fant, J. & Horwitz, S. B. Promotion of microtubule assembly in vitro by taxol. Nature 277, 665–667 (1979).

    Article  CAS  Google Scholar 

  14. Nitta, T. & Hess, H. Dispersion in active transport by kinesin-powered molecular shuttles. Nano Lett. 5, 1337–1342 (2005).

    Article  CAS  Google Scholar 

  15. Brunner, C., Hess, H., Ernst, K-H. & Vogel, V. Lifetime of biomolecules in hybrid nanodevices. Nanotechnology 15, S540–S548 (2004).

    Article  CAS  Google Scholar 

  16. Ruhnow, F., Zwicker, D. & Diez, S. Tracking single particles and elongated filaments with nanometer precision. Biophys. J. 100, 2820–2828 (2011).

    Article  CAS  Google Scholar 

  17. Vale, R. D., Schnapp, B. J., Reese, T. S. & Sheetz, M. P. Organelle, bead, and microtubule translocations promoted by soluble factors from the squid giant axon. Cell 40, 559–569 (1985).

    Article  CAS  Google Scholar 

  18. Diaz-Valencia, J. D. et al. Drosophila katanin-60 depolymerizes and severs at microtubule defects. Biophys. J. 100, 2440–2449 (2011).

    Article  CAS  Google Scholar 

  19. Howard, J. & Hyman, A. A. Preparation of marked microtubules for the assay of the polarity of microtubule-based motors by fluorescence microscopy. Methods Cell Biol. 39, 105–113 (1993).

    Article  CAS  Google Scholar 

  20. Aggarwal, T., Materassi, D., Davison, R., Hays, T. & Salapaka, M. Detection of steps in single molecule data. Cell. Mol. Bioeng. 5, 14–31 (2012).

    Article  CAS  Google Scholar 

  21. Dumont, E. L. P., Belmas, H. & Hess, H. Observing the mushroom-to-brush transition for kinesin proteins. Langmuir 29, 15142–15145 (2013).

    Article  CAS  Google Scholar 

  22. Toprak, E., Yildiz, A., Hoffman, M. T., Rosenfeld, S. S. & Selvin, P. R. Why kinesin is so processive. Proc. Natl Acad. Sci. USA 106, 12717–12722 (2009).

    Article  CAS  Google Scholar 

  23. VanBuren, V., Cassimeris, L. & Odde, D. J. Mechanochemical model of microtubule structure and self-assembly kinetics. Biophys. J. 89, 2911–2926 (2005).

    Article  CAS  Google Scholar 

  24. Agarwal, A., Katira, P. & Hess, H. Millisecond curing time of a molecular adhesive causes velocity-dependent cargo-loading of molecular shuttles. Nano Lett. 9, 1170–1175 (2009).

    Article  CAS  Google Scholar 

  25. Neuert, G., Albrecht, C. H. & Gaub, H. E. Predicting the rupture probabilities of molecular bonds in series. Biophys. J. 93, 1215–1223 (2007).

    Article  CAS  Google Scholar 

  26. Bhaskaran, H. et al. Ultralow nanoscale wear through atom-by-atom attrition in silicon-containing diamond-like carbon. Nature Nanotech. 5, 181–185 (2010).

    Article  CAS  Google Scholar 

  27. Gnecco, E., Bennewitz, R. & Meyer, E. Abrasive wear on the atomic scale. Phys. Rev. Lett. 88, 215501 (2002).

    Article  CAS  Google Scholar 

  28. Gotsmann, B. & Lantz, M. A. Atomistic wear in a single asperity sliding contact. Phys. Rev. Lett. 101, 125501 (2008).

    Article  Google Scholar 

  29. Coy, D. L., Hancock, W. O., Wagenbach, M. & Howard, J. Kinesin's tail domain is an inhibitory regulator of the motor domain. Nature Cell Biol. 1, 288–292 (1999).

    Article  CAS  Google Scholar 

  30. Howard, J., Hunt, A. J. & Baek, S. Assay of microtubule movement driven by single kinesin molecules. Methods Cell. Biol. 39, 137–147 (1993).

    Article  CAS  Google Scholar 

  31. Wettermark, G., Borglund, E. & Brolin, S. E. A regenerating system for studies of phosphoryl transfer from ATP. Anal. Biochem. 22, 211–218 (1968).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge financial support from the National Science Foundation (grant CMMI-0926780) and from a Liu Ping fellowship (E.L.P.D.) and thank G. Bachand for providing the kinesin protein. This work was performed, in part, at the Center for Integrated Nanotechnologies, an Office of Science User Facility operated for the US Department of Energy (DOE) Office of Science by Los Alamos National Laboratory (contract DE-AC52-06NA25396) and Sandia National Laboratories (contract DE-AC04-94AL85000).

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, Columbia University, New York, 10027, New York, USA

    Emmanuel L. P. Dumont & Henry Hess

  2. The Jacobs Technion-Cornell Institute at Cornell Tech, 111 8th Avenue #302, New York, 10011, USA, New York

    Emmanuel L. P. Dumont

  3. Institute for Cancer Genetics, Columbia University Medical Center, New York, 10032, New York, USA

    Catherine Do

Authors
  1. Emmanuel L. P. Dumont
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Catherine Do
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Henry Hess
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.L.P.D. and H.H. designed and conceived the experiments. E.L.P.D. performed the experiments. E.L.P.D. and C.D. performed the statistical analysis. E.L.P.D. and H.H. wrote the paper.

Corresponding author

Correspondence to Henry Hess.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary Information (PDF 2878 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dumont, E., Do, C. & Hess, H. Molecular wear of microtubules propelled by surface-adhered kinesins. Nature Nanotech 10, 166–169 (2015). https://doi.org/10.1038/nnano.2014.334

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nnano.2014.334

This article is cited by

Search

Advanced 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