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Cooperative Accumulation of Dynein-Dynactin at Microtubule Minus-Ends Drives Microtubule Network Reorganization

Ruensern Tan, Peter J. Foster, Daniel J. Needleman, Richard J. McKenney
doi: https://doi.org/10.1101/140392
Ruensern Tan
1Dept. of Molecular and Cellular Biology; University of California – Davis; Davis, CA, 95616; United States
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Peter J. Foster
2John A. Paulson School of Engineering and Applied Sciences, FAS Center for Systems Biology; Harvard University, Cambridge, MA, 02138; United States
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Daniel J. Needleman
2John A. Paulson School of Engineering and Applied Sciences, FAS Center for Systems Biology; Harvard University, Cambridge, MA, 02138; United States
3Department of Molecular and Cellular Biology; Harvard University; Cambridge, MA, 01238; United States
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Richard J. McKenney
1Dept. of Molecular and Cellular Biology; University of California – Davis; Davis, CA, 95616; United States
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Abstract

Summary Cytoplasmic dynein-1 (dynein) is minus-end directed motor protein that transports cargo over long distances and organizes microtubules (MTs) during critical cellular processes such as mitotic spindle assembly. How dynein motor activity is harnessed for these diverse functions remains unknown. Here, we have uncovered a mechanism for how processive dynein-dynactin complexes drive MT-MT sliding, reorganization, and focusing, activities required for mitotic spindle assembly. We find that motors cooperatively accumulate, in limited numbers, at MT minus-ends. Minus-end accumulations drive MT-MT sliding, independent of MT orientation, and this activity always results in the clustering of MT minus-ends. At a mesoscale level, activated dynein-dynactin drives the formation and coalescence of MT asters. Macroscopically, dynein-dynactin activity leads to bulk contraction of millimeter-scale MT networks, demonstrating that minus-end accumulations produce network scale contractile stresses. Our data provides a model for how localized dynein activity is harnessed by cells to produce contractile stresses within the mitotic spindle.

Highlights

  • Processive dynein-dynactin complexes cooperatively form stable accumulations at MT minus-ends.

  • Minus-end accumulations of motors slide MTs without orientation bias, leading to minus-end focusing.

  • Minus-end accumulations of motors organize dynamic MTs into asters.

  • Minus-end accumulations of motors drive bulk contractions of large-scale MT networks.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 19, 2017.
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Cooperative Accumulation of Dynein-Dynactin at Microtubule Minus-Ends Drives Microtubule Network Reorganization
Ruensern Tan, Peter J. Foster, Daniel J. Needleman, Richard J. McKenney
bioRxiv 140392; doi: https://doi.org/10.1101/140392
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Cooperative Accumulation of Dynein-Dynactin at Microtubule Minus-Ends Drives Microtubule Network Reorganization
Ruensern Tan, Peter J. Foster, Daniel J. Needleman, Richard J. McKenney
bioRxiv 140392; doi: https://doi.org/10.1101/140392

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