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Multiple Kinesins Induce Tension for Smooth Cargo Transport

View ORCID ProfileMarco Tjioe, Saurabh Shukla, Rohit Vaidya, Alice Troitskaia, Carol Bookwalter, Kathleen M. Trybus, Yann R. Chemla, Paul R. Selvin
doi: https://doi.org/10.1101/544080
Marco Tjioe
1Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
2Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
3Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
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  • ORCID record for Marco Tjioe
Saurabh Shukla
2Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
4Department of Chemical and Biomolecular Engineering, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
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Rohit Vaidya
1Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
2Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
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Alice Troitskaia
1Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
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Carol Bookwalter
5Department of Molecular Physiology and Biophysics, University of Vermont, Burlington, VT 05405
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Kathleen M. Trybus
5Department of Molecular Physiology and Biophysics, University of Vermont, Burlington, VT 05405
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Yann R. Chemla
1Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
2Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
3Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
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Paul R. Selvin
1Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
2Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
3Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
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  • For correspondence: [email protected]
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ABSTRACT

How cargoes move within a crowded cell—over long distances and at speeds nearly the same as when moving on unimpeded pathway—has long been mysterious. Through an in vitro force-gliding assay, which involves measuring nanometer displacement and piconewtons of force, we show that kinesins (from 2-8) communicate in a team by inducing tension (up to 4 pN) on the cargo. Kinesins adopt two distinct states, with one-third slowing down the microtubule and two-thirds speeding it up. Resisting kinesins tend to come off more rapidly than, and speed up when pulled by driving kinesins, implying an asymmetric tug-of-war. Furthermore, kinesins dynamically interact to overcome roadblocks, occasionally combining their forces. Consequently, multiple kinesins acting as a team may play a significant role in facilitating smooth cargo motion in a dense environment. This is one of few cases in which single molecule behavior can be connected to ensemble behavior of multiple motors.

Footnotes

  • There are corrections on negative cooperativity and more discussions on the relevance of the study to cellular systems.

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Posted October 01, 2019.
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Multiple Kinesins Induce Tension for Smooth Cargo Transport
Marco Tjioe, Saurabh Shukla, Rohit Vaidya, Alice Troitskaia, Carol Bookwalter, Kathleen M. Trybus, Yann R. Chemla, Paul R. Selvin
bioRxiv 544080; doi: https://doi.org/10.1101/544080
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Multiple Kinesins Induce Tension for Smooth Cargo Transport
Marco Tjioe, Saurabh Shukla, Rohit Vaidya, Alice Troitskaia, Carol Bookwalter, Kathleen M. Trybus, Yann R. Chemla, Paul R. Selvin
bioRxiv 544080; doi: https://doi.org/10.1101/544080

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