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Multiple kinesins induce tension for smooth cargo transport

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 ki...

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Autores principales: Tjioe, Marco, Shukla, Saurabh, Vaidya, Rohit, Troitskaia, Alice, Bookwalter, Carol S, Trybus, Kathleen M, Chemla, Yann R, Selvin, Paul R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6904222/
https://www.ncbi.nlm.nih.gov/pubmed/31670658
http://dx.doi.org/10.7554/eLife.50974
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author Tjioe, Marco
Shukla, Saurabh
Vaidya, Rohit
Troitskaia, Alice
Bookwalter, Carol S
Trybus, Kathleen M
Chemla, Yann R
Selvin, Paul R
author_facet Tjioe, Marco
Shukla, Saurabh
Vaidya, Rohit
Troitskaia, Alice
Bookwalter, Carol S
Trybus, Kathleen M
Chemla, Yann R
Selvin, Paul R
author_sort Tjioe, Marco
collection PubMed
description 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 to 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.
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spelling pubmed-69042222019-12-12 Multiple kinesins induce tension for smooth cargo transport Tjioe, Marco Shukla, Saurabh Vaidya, Rohit Troitskaia, Alice Bookwalter, Carol S Trybus, Kathleen M Chemla, Yann R Selvin, Paul R eLife Structural Biology and Molecular Biophysics 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 to 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. eLife Sciences Publications, Ltd 2019-10-31 /pmc/articles/PMC6904222/ /pubmed/31670658 http://dx.doi.org/10.7554/eLife.50974 Text en © 2019, Tjioe et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Structural Biology and Molecular Biophysics
Tjioe, Marco
Shukla, Saurabh
Vaidya, Rohit
Troitskaia, Alice
Bookwalter, Carol S
Trybus, Kathleen M
Chemla, Yann R
Selvin, Paul R
Multiple kinesins induce tension for smooth cargo transport
title Multiple kinesins induce tension for smooth cargo transport
title_full Multiple kinesins induce tension for smooth cargo transport
title_fullStr Multiple kinesins induce tension for smooth cargo transport
title_full_unstemmed Multiple kinesins induce tension for smooth cargo transport
title_short Multiple kinesins induce tension for smooth cargo transport
title_sort multiple kinesins induce tension for smooth cargo transport
topic Structural Biology and Molecular Biophysics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6904222/
https://www.ncbi.nlm.nih.gov/pubmed/31670658
http://dx.doi.org/10.7554/eLife.50974
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