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...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2019-10-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/50974 |
| _version_ | 1811202740069597184 |
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| author | Marco Tjioe Saurabh Shukla Rohit Vaidya Alice Troitskaia Carol S Bookwalter Kathleen M Trybus Yann R Chemla Paul R Selvin |
| author_facet | Marco Tjioe Saurabh Shukla Rohit Vaidya Alice Troitskaia Carol S Bookwalter Kathleen M Trybus Yann R Chemla Paul R Selvin |
| author_sort | Marco Tjioe |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-12T02:43:43Z |
| format | Article |
| id | doaj.art-f0cfc80e1764485691084dfbb2a346d0 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:43:43Z |
| publishDate | 2019-10-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-f0cfc80e1764485691084dfbb2a346d02022-12-22T03:51:15ZengeLife Sciences Publications LtdeLife2050-084X2019-10-01810.7554/eLife.50974Multiple kinesins induce tension for smooth cargo transportMarco Tjioe0https://orcid.org/0000-0002-6445-9828Saurabh Shukla1Rohit Vaidya2Alice Troitskaia3Carol S Bookwalter4Kathleen M Trybus5https://orcid.org/0000-0002-5583-8500Yann R Chemla6https://orcid.org/0000-0001-9167-0234Paul R Selvin7https://orcid.org/0000-0002-3658-4218Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United States; Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, United States; Department of Physics, University of Illinois at Urbana-Champaign, Urbana, United StatesCenter for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, United States; Department of Chemical and Biomolecular Engineering, University of Illinois at Urbana-Champaign, Urbana, United StatesCenter for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United States; Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, United StatesCenter for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United StatesDepartment of Molecular Physiology and Biophysics, University of Vermont, Burlington, United StatesDepartment of Molecular Physiology and Biophysics, University of Vermont, Burlington, United StatesCenter for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United States; Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, United States; Department of Physics, University of Illinois at Urbana-Champaign, Urbana, United StatesCenter for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United States; Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, United States; Department of Physics, University of Illinois at Urbana-Champaign, Urbana, United StatesHow 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.https://elifesciences.org/articles/50974kinesinrecombinantsf9 cell purificationmultiple motorsmicrotubules |
| spellingShingle | Marco Tjioe Saurabh Shukla Rohit Vaidya Alice Troitskaia Carol S Bookwalter Kathleen M Trybus Yann R Chemla Paul R Selvin Multiple kinesins induce tension for smooth cargo transport eLife kinesin recombinant sf9 cell purification multiple motors microtubules |
| 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 | kinesin recombinant sf9 cell purification multiple motors microtubules |
| url | https://elifesciences.org/articles/50974 |
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