Recruitment of two dyneins to an mRNA-dependent Bicaudal D transport complex
We investigated the role of full-length Drosophila Bicaudal D (BicD) binding partners in dynein-dynactin activation for mRNA transport on microtubules. Full-length BicD robustly activated dynein-dynactin motility only when both the mRNA binding protein Egalitarian (Egl) and K10 mRNA cargo were prese...
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doaj-31c5caaefb134acaa7f972fe1db55b732021-05-05T15:58:46ZengeLife Sciences Publications LtdeLife2050-084X2018-06-01710.7554/eLife.36306Recruitment of two dyneins to an mRNA-dependent Bicaudal D transport complexThomas E Sladewski0Neil Billington1https://orcid.org/0000-0003-2306-0228M Yusuf Ali2Carol S Bookwalter3Hailong Lu4Elena B Krementsova5Trina A Schroer6https://orcid.org/0000-0002-5065-1835Kathleen M Trybus7https://orcid.org/0000-0002-5583-8500Department of Molecular Physiology and Biophysics, University of Vermont, Burlington, United StatesLaboratory of Physiology, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, United StatesDepartment of Molecular Physiology and Biophysics, University of Vermont, Burlington, United StatesDepartment of Molecular Physiology and Biophysics, University of Vermont, Burlington, United StatesDepartment of Molecular Physiology and Biophysics, University of Vermont, Burlington, United StatesDepartment of Molecular Physiology and Biophysics, University of Vermont, Burlington, United StatesDepartment of Biology, Johns Hopkins University, Baltimore, United StatesDepartment of Molecular Physiology and Biophysics, University of Vermont, Burlington, United StatesWe investigated the role of full-length Drosophila Bicaudal D (BicD) binding partners in dynein-dynactin activation for mRNA transport on microtubules. Full-length BicD robustly activated dynein-dynactin motility only when both the mRNA binding protein Egalitarian (Egl) and K10 mRNA cargo were present, and electron microscopy showed that both Egl and mRNA were needed to disrupt a looped, auto-inhibited BicD conformation. BicD can recruit two dimeric dyneins, resulting in faster speeds and longer runs than with one dynein. Moving complexes predominantly contained two Egl molecules and one K10 mRNA. This mRNA-bound configuration makes Egl bivalent, likely enhancing its avidity for BicD and thus its ability to disrupt BicD auto-inhibition. Consistent with this idea, artificially dimerized Egl activates dynein-dynactin-BicD in the absence of mRNA. The ability of mRNA cargo to orchestrate the activation of the mRNP (messenger ribonucleotide protein) complex is an elegant way to ensure that only cargo-bound motors are motile.https://elifesciences.org/articles/36306mRNA transportdyneinBicDdynactinEgalitarian |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Thomas E Sladewski Neil Billington M Yusuf Ali Carol S Bookwalter Hailong Lu Elena B Krementsova Trina A Schroer Kathleen M Trybus |
spellingShingle |
Thomas E Sladewski Neil Billington M Yusuf Ali Carol S Bookwalter Hailong Lu Elena B Krementsova Trina A Schroer Kathleen M Trybus Recruitment of two dyneins to an mRNA-dependent Bicaudal D transport complex eLife mRNA transport dynein BicD dynactin Egalitarian |
author_facet |
Thomas E Sladewski Neil Billington M Yusuf Ali Carol S Bookwalter Hailong Lu Elena B Krementsova Trina A Schroer Kathleen M Trybus |
author_sort |
Thomas E Sladewski |
title |
Recruitment of two dyneins to an mRNA-dependent Bicaudal D transport complex |
title_short |
Recruitment of two dyneins to an mRNA-dependent Bicaudal D transport complex |
title_full |
Recruitment of two dyneins to an mRNA-dependent Bicaudal D transport complex |
title_fullStr |
Recruitment of two dyneins to an mRNA-dependent Bicaudal D transport complex |
title_full_unstemmed |
Recruitment of two dyneins to an mRNA-dependent Bicaudal D transport complex |
title_sort |
recruitment of two dyneins to an mrna-dependent bicaudal d transport complex |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2018-06-01 |
description |
We investigated the role of full-length Drosophila Bicaudal D (BicD) binding partners in dynein-dynactin activation for mRNA transport on microtubules. Full-length BicD robustly activated dynein-dynactin motility only when both the mRNA binding protein Egalitarian (Egl) and K10 mRNA cargo were present, and electron microscopy showed that both Egl and mRNA were needed to disrupt a looped, auto-inhibited BicD conformation. BicD can recruit two dimeric dyneins, resulting in faster speeds and longer runs than with one dynein. Moving complexes predominantly contained two Egl molecules and one K10 mRNA. This mRNA-bound configuration makes Egl bivalent, likely enhancing its avidity for BicD and thus its ability to disrupt BicD auto-inhibition. Consistent with this idea, artificially dimerized Egl activates dynein-dynactin-BicD in the absence of mRNA. The ability of mRNA cargo to orchestrate the activation of the mRNP (messenger ribonucleotide protein) complex is an elegant way to ensure that only cargo-bound motors are motile. |
topic |
mRNA transport dynein BicD dynactin Egalitarian |
url |
https://elifesciences.org/articles/36306 |
work_keys_str_mv |
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