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Vesicles driven by dynein and kinesin exhibit directional reversals without external regulators

View ORCID ProfileAshwin I. D’Souza, View ORCID ProfileRahul Grover, Gina A. Monzon, View ORCID ProfileLudger Santen, View ORCID ProfileStefan Diez
doi: https://doi.org/10.1101/2022.09.27.509758
Ashwin I. D’Souza
1B CUBE - Center for Molecular Bioengineering, TU Dresden, Dresden, Germany
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  • ORCID record for Ashwin I. D’Souza
Rahul Grover
1B CUBE - Center for Molecular Bioengineering, TU Dresden, Dresden, Germany
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Gina A. Monzon
1B CUBE - Center for Molecular Bioengineering, TU Dresden, Dresden, Germany
2Center for Biophysics, Department of Physics, Saarland University, Saarbrücken, Germany
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Ludger Santen
2Center for Biophysics, Department of Physics, Saarland University, Saarbrücken, Germany
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  • For correspondence: l.santen@mx.uni-saarland.de stefan.diez@tu-dresden.de
Stefan Diez
1B CUBE - Center for Molecular Bioengineering, TU Dresden, Dresden, Germany
3Cluster of Excellence Physics of Life, TU Dresden, Dresden, Germany
4Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
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  • For correspondence: l.santen@mx.uni-saarland.de stefan.diez@tu-dresden.de
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Abstract

Intracellular transport along cytoskeletal filaments propelled by molecular motors ensures the targeted delivery of cargoes to their destinations. Such transport is rarely unidirectional but rather bidirectional, including intermittent pauses and directional reversals owing to the simultaneous presence of opposite-polarity motors. It has been unclear whether such a complex motility pattern results from the sole mechanical interplay between opposite-polarity motors or requires external regulators. Here, we addressed this outstanding question by reconstituting cargo motility along microtubules in vitro by attaching purified Dynein-Dynactin-BICD2 (DDB) and kinesin-3 (KIF16B) to large unilamellar vesicles. Strikingly, we found that this minimal system is sufficient to recapitulate runs, pauses and reversals similar to in vivo cargo motility. In our experiments, reversals were always preceded by vesicle pausing and the transport directionality could be tuned by the relative numbers of opposite-polarity motors on the vesicles. Unexpectedly, during all runs the vesicle velocity was not influenced by the presence of the opposing motors. To gain mechanistic insight into bidirectional transport, we developed a mathematical model which predicts that low numbers of engaged motors are critical to transition between runs and pauses. Taken together, our results suggest that motors diffusively anchored to membranous cargo transiently engage in a tug-of-war during pauses where stochastic motor attachment and detachment events can lead to directional reversals without the necessity of external regulators.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 28, 2022.
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Vesicles driven by dynein and kinesin exhibit directional reversals without external regulators
Ashwin I. D’Souza, Rahul Grover, Gina A. Monzon, Ludger Santen, Stefan Diez
bioRxiv 2022.09.27.509758; doi: https://doi.org/10.1101/2022.09.27.509758
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Vesicles driven by dynein and kinesin exhibit directional reversals without external regulators
Ashwin I. D’Souza, Rahul Grover, Gina A. Monzon, Ludger Santen, Stefan Diez
bioRxiv 2022.09.27.509758; doi: https://doi.org/10.1101/2022.09.27.509758

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