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Dynein arms are oscillating force generators

Nature volume 393, pages 711–714 (1998)Cite this article

Abstract

Eukaryotic flagella beat rhythmically1. Dynein is a protein that powers flagellar motion, and oscillation may be inherent to this protein2,3,4,5. Here we determine whether oscillation is a property of dynein arms themselves or whether oscillation requires an intact axoneme6, which is the central core of the flagellum and consists ofa regular array of microtubules. Using optical trapping nanometry7,8, we measured the force generated by a few dynein arms on an isolated doublet microtubule. When the dynein arms on the doublet microtubule contact a singlet microtubule and are activated by photolysis of caged ATP8, they generate a peak force of ∼6 pN and move the singlet microtubule over the doublet microtubule in a processive manner. The force and displacement oscillate with a peak-to-peak force and amplitude of ∼2 pN and ∼30 nm, respectively. The geometry of the interaction indicates that very few (possibly one) dynein arms are needed to generate the oscillation. The maximum frequency of the oscillation at 0.75 mM ATP is ∼70 Hz; this frequency decreases as the ATP concentration decreases. A similar oscillatory force is also generated by inner dynein arms alone on doublet microtubules that are depleted of outer dynein arms. The oscillation of the dynein arm may be a basic mechanism underlying flagellar beating.

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Figure 1: Interactions of singlet microtubules with dynein arms present on doublet microtubules.
Figure 2: Force generation by dynein arms.
Figure 3: Force oscillations of dynein arms.

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Acknowledgements

We thank K. Takahashi and R. A. Thornhill for discussion and critical reading of the manuscript, and E. Muto and Y. Inoue for suggestions about the preparation of microtubules. This work was supported by a Kurata Research Grant and a Grant from Nissan Science Foundation (to C.S.).

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Author notes

  1. Hideo Higuchi

    Present address: Department of Metallurgy, Faculty of Engineering, Tohoku University, Aramaki-aza-Aoba, Sendai, 980-8579, Japan

Authors and Affiliations

  1. Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo, 113-0033, Tokyo, Japan

    Chikako Shingyoji & Misako Yoshimura

  2. Yanagida BioMotron Project, ERATO, JRDC, Senba-Higashi 2-4-14, Mino, 562-0035, Osaka, Japan

    Hideo Higuchi & Toshio Yanagida

  3. Department of Fine Morphology, Institute of Medical Science, University of Tokyo, Minato-ku, 108-0071, Tokyo, Japan

    Eisaku Katayama

  4. Department of Physiology, Osaka University Medical School, Suita, 565-0871, Osaka, Japan

    Toshio Yanagida

Authors
  1. Chikako Shingyoji
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Correspondence to Chikako Shingyoji.

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Shingyoji, C., Higuchi, H., Yoshimura, M. et al. Dynein arms are oscillating force generators. Nature 393, 711–714 (1998). https://doi.org/10.1038/31520

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