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Research Article
Mechanical induction of oscillatory movement in demembranated, immotile flagella of sea urchin sperm at very low ATP concentrations
Yasuhide Izawa, Chikako Shingyoji
Journal of Experimental Biology 2020 223: jeb225797 doi: 10.1242/jeb.225797 Published 16 October 2020
Yasuhide Izawa
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo, Tokyo 113-0033, Japan
2Department of Biotechnology and Life Science, Tokyo University of Agriculture and Technology, 2-24-16 Naka-cho, Koganei, Tokyo 184-8588, Japan
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Chikako Shingyoji
1Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo, Tokyo 113-0033, Japan
2Department of Biotechnology and Life Science, Tokyo University of Agriculture and Technology, 2-24-16 Naka-cho, Koganei, Tokyo 184-8588, Japan
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  • ORCID record for Chikako Shingyoji
  • For correspondence: chikako@bs.s.u-tokyo.ac.jp chikako.shingyoji@gmail.com
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ABSTRACT

Oscillation is a characteristic feature of eukaryotic flagellar movement. The mechanism involves the control of dynein-driven microtubule sliding under self-regulatory mechanical feedback within the axoneme. To define the essential factors determining the induction of oscillation, we developed a novel experiment by applying mechanical deformation of demembranated, immotile sea urchin sperm flagella at very low ATP concentrations, below the threshold of ATP required for spontaneous beating. Upon application of mechanical deformation at above 1.5 µmol l−1 ATP, a pair of bends could be induced and was accompanied by bend growth and propagation, followed by switching the bending direction. For an oscillatory, cyclical bending response to occur, the velocity of bend propagation towards the flagellar tip must be kept above certain levels. Continuous formation of new bends at the flagellar base was coupled with synchronized decay of the preceding paired bends. Induction of cyclical bends was initiated in a constant direction relative to the axis of the flagellar 9+2 structure, and resulted in the so-called principal bend. In addition, stoppage of the bending response occasionally occurred during development of a new principal bend, and in this situation, formation of a new reverse bend did not occur. This observation indicates that the reverse bend is always active, opposing the principal bend. The results show that mechanical strain of bending is a central component regulating the bend oscillation, and switching of the bend direction appears to be controlled, in part, by the velocity of wave propagation.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: C.S.; Methodology: C.S., Y.I.; Formal analysis: Y.I.; Investigation: C.S., Y.I.; Data curation: C.S., Y.I.; Writing - original draft: Y.I.; Writing - review & editing: C.S.; Supervision: C.S.; Project administration: C.S.; Funding acquisition: C.S.

  • Funding

    This work was supported by the Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research on Innovative Areas, 26102510 and 16H00752 to C.S.

  • Data availability

    The data obtained in this study will become available through the University of Tokyo Academic Institutional Repository, 6 months after publication.

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.225797.supplemental

  • Received March 31, 2020.
  • Accepted August 6, 2020.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Axonemal dynein
  • Bend initiation
  • Cyclical bending
  • Imposed bending
  • Mechanical signal
  • Microtubule sliding

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Research Article
Mechanical induction of oscillatory movement in demembranated, immotile flagella of sea urchin sperm at very low ATP concentrations
Yasuhide Izawa, Chikako Shingyoji
Journal of Experimental Biology 2020 223: jeb225797 doi: 10.1242/jeb.225797 Published 16 October 2020
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Research Article
Mechanical induction of oscillatory movement in demembranated, immotile flagella of sea urchin sperm at very low ATP concentrations
Yasuhide Izawa, Chikako Shingyoji
Journal of Experimental Biology 2020 223: jeb225797 doi: 10.1242/jeb.225797 Published 16 October 2020

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