Cytoplasmic dynein crosslinks and slides anti-parallel microtubules using its two motor domains
Cytoplasmic dynein is the predominant minus-end-directed microtubule (MT) motor in most eukaryotic cells. In addition to transporting vesicular cargos, dynein helps to organize MTs within MT networks such as mitotic spindles. How dynein performs such non-canonical functions is unknown. Here we demon...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2013-09-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/00943 |
| _version_ | 1811201083076247552 |
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| author | Marvin E Tanenbaum Ronald D Vale Richard J McKenney |
| author_facet | Marvin E Tanenbaum Ronald D Vale Richard J McKenney |
| author_sort | Marvin E Tanenbaum |
| collection | DOAJ |
| description | Cytoplasmic dynein is the predominant minus-end-directed microtubule (MT) motor in most eukaryotic cells. In addition to transporting vesicular cargos, dynein helps to organize MTs within MT networks such as mitotic spindles. How dynein performs such non-canonical functions is unknown. Here we demonstrate that dynein crosslinks and slides anti-parallel MTs in vitro. Surprisingly, a minimal dimeric motor lacking a tail domain and associated subunits can cause MT sliding. Single molecule imaging reveals that motors pause and frequently reverse direction when encountering an anti-parallel MT overlap, suggesting that the two motor domains can bind both MTs simultaneously. In the mitotic spindle, inward microtubule sliding by dynein counteracts outward sliding generated by kinesin-5, and we show that a tailless, dimeric motor is sufficient to drive this activity in mammalian cells. Our results identify an unexpected mechanism for dynein-driven microtubule sliding, which differs from filament sliding mechanisms described for other motor proteins. |
| first_indexed | 2024-04-12T02:16:01Z |
| format | Article |
| id | doaj.art-bb9de9b4cdf54be881456feb0458cab5 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:16:01Z |
| publishDate | 2013-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-bb9de9b4cdf54be881456feb0458cab52022-12-22T03:52:16ZengeLife Sciences Publications LtdeLife2050-084X2013-09-01210.7554/eLife.00943Cytoplasmic dynein crosslinks and slides anti-parallel microtubules using its two motor domainsMarvin E Tanenbaum0Ronald D Vale1Richard J McKenney2Department Cellular and Molecular Pharmacology, Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesDepartment Cellular and Molecular Pharmacology, Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesDepartment Cellular and Molecular Pharmacology, Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United StatesCytoplasmic dynein is the predominant minus-end-directed microtubule (MT) motor in most eukaryotic cells. In addition to transporting vesicular cargos, dynein helps to organize MTs within MT networks such as mitotic spindles. How dynein performs such non-canonical functions is unknown. Here we demonstrate that dynein crosslinks and slides anti-parallel MTs in vitro. Surprisingly, a minimal dimeric motor lacking a tail domain and associated subunits can cause MT sliding. Single molecule imaging reveals that motors pause and frequently reverse direction when encountering an anti-parallel MT overlap, suggesting that the two motor domains can bind both MTs simultaneously. In the mitotic spindle, inward microtubule sliding by dynein counteracts outward sliding generated by kinesin-5, and we show that a tailless, dimeric motor is sufficient to drive this activity in mammalian cells. Our results identify an unexpected mechanism for dynein-driven microtubule sliding, which differs from filament sliding mechanisms described for other motor proteins.https://elifesciences.org/articles/00943dyneinspindlemicrotubuleEg5cytoskeletonmitosis |
| spellingShingle | Marvin E Tanenbaum Ronald D Vale Richard J McKenney Cytoplasmic dynein crosslinks and slides anti-parallel microtubules using its two motor domains eLife dynein spindle microtubule Eg5 cytoskeleton mitosis |
| title | Cytoplasmic dynein crosslinks and slides anti-parallel microtubules using its two motor domains |
| title_full | Cytoplasmic dynein crosslinks and slides anti-parallel microtubules using its two motor domains |
| title_fullStr | Cytoplasmic dynein crosslinks and slides anti-parallel microtubules using its two motor domains |
| title_full_unstemmed | Cytoplasmic dynein crosslinks and slides anti-parallel microtubules using its two motor domains |
| title_short | Cytoplasmic dynein crosslinks and slides anti-parallel microtubules using its two motor domains |
| title_sort | cytoplasmic dynein crosslinks and slides anti parallel microtubules using its two motor domains |
| topic | dynein spindle microtubule Eg5 cytoskeleton mitosis |
| url | https://elifesciences.org/articles/00943 |
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