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

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Article numbere50974
JournaleLife
Volume8
DOIs
StatePublished - Oct 2019

Fingerprint

Kinesin
Microtubules
Assays
Molecules

ASJC Scopus subject areas

  • Neuroscience(all)
  • Immunology and Microbiology(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Tjioe, M., Shukla, S., Vaidya, R., Troitskaia, A., Bookwalter, C., Trybus, K. M., ... Selvin, P. R. (2019). Multiple kinesins induce tension for smooth cargo transport. eLife, 8, [e50974]. https://doi.org/10.7554/eLife.50974

Multiple kinesins induce tension for smooth cargo transport. / Tjioe, Marco; Shukla, Saurabh; Vaidya, Rohit; Troitskaia, Alice; Bookwalter, Carol; Trybus, Kathleen M.; Chemla, Yann R.; Selvin, Paul R.

In: eLife, Vol. 8, e50974, 10.2019.

Research output: Contribution to journalArticle

Tjioe, M, Shukla, S, Vaidya, R, Troitskaia, A, Bookwalter, C, Trybus, KM, Chemla, YR & Selvin, PR 2019, 'Multiple kinesins induce tension for smooth cargo transport', eLife, vol. 8, e50974. https://doi.org/10.7554/eLife.50974
Tjioe M, Shukla S, Vaidya R, Troitskaia A, Bookwalter C, Trybus KM et al. Multiple kinesins induce tension for smooth cargo transport. eLife. 2019 Oct;8. e50974. https://doi.org/10.7554/eLife.50974
Tjioe, Marco ; Shukla, Saurabh ; Vaidya, Rohit ; Troitskaia, Alice ; Bookwalter, Carol ; Trybus, Kathleen M. ; Chemla, Yann R. ; Selvin, Paul R. / Multiple kinesins induce tension for smooth cargo transport. In: eLife. 2019 ; Vol. 8.
@article{31355f1fe72f468abb5007d4837f65b7,
title = "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.",
author = "Marco Tjioe and Saurabh Shukla and Rohit Vaidya and Alice Troitskaia and Carol Bookwalter and Trybus, {Kathleen M.} and Chemla, {Yann R.} and Selvin, {Paul R.}",
year = "2019",
month = "10",
doi = "10.7554/eLife.50974",
language = "English (US)",
volume = "8",
journal = "eLife",
issn = "2050-084X",
publisher = "eLife Sciences Publications",

}

TY - JOUR

T1 - Multiple kinesins induce tension for smooth cargo transport

AU - Tjioe, Marco

AU - Shukla, Saurabh

AU - Vaidya, Rohit

AU - Troitskaia, Alice

AU - Bookwalter, Carol

AU - Trybus, Kathleen M.

AU - Chemla, Yann R.

AU - Selvin, Paul R.

PY - 2019/10

Y1 - 2019/10

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85074472366&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85074472366&partnerID=8YFLogxK

U2 - 10.7554/eLife.50974

DO - 10.7554/eLife.50974

M3 - Article

C2 - 31670658

AN - SCOPUS:85074472366

VL - 8

JO - eLife

JF - eLife

SN - 2050-084X

M1 - e50974

ER -