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Direct observation shows superposition and large scale flexibility within cytoplasmic dynein motors moving along microtubules

Author

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  • Hiroshi Imai

    (School of Molecular and Cellular Biology and Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds
    Present address: Department of Biological Sciences, Faculty of Science and Engineering, Chuo University, 1-13-27 Bunkyo-ku, Tokyo 112-8551, Japan)

  • Tomohiro Shima

    (Quantitative Biology Center
    Present address: Department of Biological Sciences, Graduate School of Science, University of Tokyo, 2-11-16 Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan)

  • Kazuo Sutoh

    (Faculty of Science and Engineering, Waseda University)

  • Matthew L. Walker

    (MLW Consulting)

  • Peter J. Knight

    (School of Molecular and Cellular Biology and Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds)

  • Takahide Kon

    (Graduate School of Science, Osaka University
    Japan Science and Technology Agency, Precursory Research for Embryonic Science and Technology)

  • Stan A. Burgess

    (School of Molecular and Cellular Biology and Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds)

Abstract

Cytoplasmic dynein is a dimeric AAA+ motor protein that performs critical roles in eukaryotic cells by moving along microtubules using ATP. Here using cryo-electron microscopy we directly observe the structure of Dictyostelium discoideum dynein dimers on microtubules at near-physiological ATP concentrations. They display remarkable flexibility at a hinge close to the microtubule binding domain (the stalkhead) producing a wide range of head positions. About half the molecules have the two heads separated from one another, with both leading and trailing motors attached to the microtubule. The other half have the two heads and stalks closely superposed in a front-to-back arrangement of the AAA+ rings, suggesting specific contact between the heads. All stalks point towards the microtubule minus end. Mean stalk angles depend on the separation between their stalkheads, which allows estimation of inter-head tension. These findings provide a structural framework for understanding dynein’s directionality and unusual stepping behaviour.

Suggested Citation

  • Hiroshi Imai & Tomohiro Shima & Kazuo Sutoh & Matthew L. Walker & Peter J. Knight & Takahide Kon & Stan A. Burgess, 2015. "Direct observation shows superposition and large scale flexibility within cytoplasmic dynein motors moving along microtubules," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms9179
    DOI: 10.1038/ncomms9179
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    Cited by:

    1. Marie-France Langelier & Ramya Billur & Aleksandr Sverzhinsky & Ben E. Black & John M. Pascal, 2021. "HPF1 dynamically controls the PARP1/2 balance between initiating and elongating ADP-ribose modifications," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

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