Multiple kinesins induce tension for smooth cargo transport
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 multiple mammalian kinesin-1 (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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.
Article and author information
Author details
Funding
National Institutes of Health (GM108578)
- Paul R Selvin
National Science Foundation (1430124)
- Paul R Selvin
National Institutes of Health (GM078097)
- Kathleen M Trybus
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Taekjip Ha, Johns Hopkins University, United States
Version history
- Received: August 9, 2019
- Accepted: October 31, 2019
- Accepted Manuscript published: October 31, 2019 (version 1)
- Version of Record published: December 10, 2019 (version 2)
- Version of Record updated: March 13, 2020 (version 3)
Copyright
© 2019, Tjioe et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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