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Entropy rectifies the Brownian steps of kinesin

Nature Chemical Biology volume 1, pages 342–347 (2005)Cite this article

Abstract

Kinesin is a stepping motor that successively produces forward and backward 8-nm steps along microtubules. Under physiological conditions, the steps powering kinesin's motility are biased in one direction and drive various biological motile processes. The physical mechanism underlying the unidirectional bias of the kinesin steps is not fully understood. Here we explored the mechanical kinetics and thermodynamics of forward and backward kinesin steps by analyzing their temperature and load dependence. Results show that the frequency asymmetry between forward and backward steps is produced by entropy. Furthermore, the magnitude of the entropic asymmetry is 6 kBT, more than three times greater than expected from a current model, in which a mechanical conformational change within the kinesin molecular structure directly biases the kinesin steps forward. We propose that the stepping direction of kinesin is preferably caused by an entropy asymmetry resulting from the compatibility between the kinesin and microtubule interaction based on their polar structures.

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Figure 1: Nanometry of single kinesin molecules.
Figure 2: Load dependence of the proportion (mean ± s.e.m.) of forward steps (pf, blue), backward steps (pb, red) and detachments (pd, green).
Figure 3: Dwell time at various loads and temperatures.
Figure 4: Kinetic analysis for kinesin steps.
Figure 5: Thermodynamic analysis for kinesin steps (a) Free-energy landscape for kinesin steps.
Figure 6: A model for the rectifying mechanism of stepping direction.

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Acknowledgements

We thank F. Oosawa, T. Kodama, K. Sekimoto, H. Higuchi, A. Ishijima, H. Kojima, T. Ariga and colleagues at Osaka University and Japan Science and Technology Agency for valuable discussions and P. Karagiannis and J. West for carefully revising the manuscript.

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Authors and Affiliations

  1. Soft Nanomachine Project, Japan Science and Technology Agency, 1-3, Yamadaoka, Suita, Osaka, 565-0871, Japan

    Yuichi Taniguchi, Yoshiharu Ishii & Toshio Yanagida

  2. Department of Mechanical Science and Bioengineering, Graduate School of Engineering Science, Osaka University, 1-3, Machikaneyama, Toyonaka, Osaka, 560-8531, Japan

    Yuichi Taniguchi

  3. Department of Chemistry, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502, Japan

    Masayoshi Nishiyama

  4. Laboratories for Nanobiology, Graduate School of Frontier Biosciences, Osaka University, 1-3, Yamadaoka

    Toshio Yanagida

  5. Department of Physiology and Biosignaling, Graduate School of Medicine, Osaka University, 2-2, Yamadaoka, Suita, Osaka, 565-0871, Japan

    Toshio Yanagida

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  1. Yuichi Taniguchi
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Correspondence to Toshio Yanagida.

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Supplementary information

Supplementary Fig. 1

Step size and direction of kinesin steps. (PDF 38 kb)

Supplementary Fig. 2

Distribution of dwell times of the forward (blue) and backward (red) steps. T = 35 °C. (PDF 31 kb)

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Taniguchi, Y., Nishiyama, M., Ishii, Y. et al. Entropy rectifies the Brownian steps of kinesin. Nat Chem Biol 1, 342–347 (2005). https://doi.org/10.1038/nchembio741

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