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Vesicles driven by dynein and kinesin exhibit directional reversals without regulators

Author

Listed:
  • Ashwin I. D’Souza

    (B CUBE - Center for Molecular Bioengineering)

  • Rahul Grover

    (B CUBE - Center for Molecular Bioengineering)

  • Gina A. Monzon

    (B CUBE - Center for Molecular Bioengineering
    Saarland University)

  • Ludger Santen

    (Saarland University)

  • Stefan Diez

    (B CUBE - Center for Molecular Bioengineering
    Cluster of Excellence Physics of Life
    Max Planck Institute of Molecular Cell Biology and Genetics)

Abstract

Intracellular vesicular transport along cytoskeletal filaments ensures targeted cargo delivery. Such transport is rarely unidirectional but rather bidirectional, with frequent directional reversals owing to the simultaneous presence of opposite-polarity motors. So far, it has been unclear whether such complex motility pattern results from the sole mechanical interplay between opposite-polarity motors or requires regulators. Here, we demonstrate that a minimal system, comprising purified Dynein-Dynactin-BICD2 (DDB) and kinesin-3 (KIF16B) attached to large unilamellar vesicles, faithfully reproduces in vivo cargo motility, including runs, pauses, and reversals. Remarkably, opposing motors do not affect vesicle velocity during runs. Our computational model reveals that the engagement of a small number of motors is pivotal for transitioning between runs and pauses. Taken together, our results suggest that motors bound to vesicular cargo transiently engage in a tug-of-war during pauses. Subsequently, stochastic motor attachment and detachment events can lead to directional reversals without the need for regulators.

Suggested Citation

  • Ashwin I. D’Souza & Rahul Grover & Gina A. Monzon & Ludger Santen & Stefan Diez, 2023. "Vesicles driven by dynein and kinesin exhibit directional reversals without regulators," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42605-8
    DOI: 10.1038/s41467-023-42605-8
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    References listed on IDEAS

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    1. Mark J. Schnitzer & Steven M. Block, 1997. "Kinesin hydrolyses one ATP per 8-nm step," Nature, Nature, vol. 388(6640), pages 386-390, July.
    2. Andrew T. Lombardo & Shane R. Nelson & M. Yusuf Ali & Guy G. Kennedy & Kathleen M. Trybus & Sam Walcott & David M. Warshaw, 2017. "Myosin Va molecular motors manoeuvre liposome cargo through suspended actin filament intersections in vitro," Nature Communications, Nature, vol. 8(1), pages 1-9, August.
    3. Brigette Y. Monroy & Danielle L. Sawyer & Bryce E. Ackermann & Melissa M. Borden & Tracy C. Tan & Kassandra M. Ori-McKenney, 2018. "Competition between microtubule-associated proteins directs motor transport," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    4. Adam R. Fenton & Thomas A. Jongens & Erika L. F. Holzbaur, 2021. "Mitochondrial adaptor TRAK2 activates and functionally links opposing kinesin and dynein motors," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
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