Concerted action of kinesins KIF5B and KIF13B promotes efficient secretory vesicle transport to microtubule plus ends
- University of California, San Francisco, United States
- Utrecht University, Netherlands
- Erasmus University Medical Center, Netherlands
- University of Copenhagen, Denmark
- University of New South Wales, Australia
Abstract
Intracellular transport relies on multiple kinesins, but it is poorly understood which kinesins are present on particular cargos, what their contributions are and whether they act simultaneously on the same cargo. Here, we show that Rab6-positive secretory vesicles are transported from the Golgi apparatus to the cell periphery by kinesin-1 KIF5B and kinesin-3 KIF13B, which determine the location of secretion events. KIF5B plays a dominant role, whereas KIF13B helps Rab6 vesicles to reach freshly polymerized microtubule ends, to which KIF5B binds poorly, likely because its cofactors, MAP7-family proteins, are slow in populating these ends. Sub-pixel localization demonstrated that during microtubule plus-end directed transport, both kinesins localize to the vesicle front and can be engaged on the same vesicle. When vesicles reverse direction, KIF13B relocates to the middle of the vesicle, while KIF5B shifts to the back, suggesting that KIF5B but not KIF13B undergoes a tug-of-war with a minus-end directed motor.
Data availability
The source data that support the conclusions of the paper are included as supplementary files for all figures containing plots (all 8 Main figures and Figure Supplements to Figs 1, 2, 3, 5 and 8). The custom software used for movement tracking and analysis in this manuscript can be found at https://imagescience.org/meijering/software/beta/. All raw and segmented trajectories and corresponding custom source code are available at https://doi.org/10.6084/m9.figshare.c.5177636.v1.
Article and author information
Author details
Andrea Serra-Marques
Peter Jan Hooikaas
Funding
H2020 European Research Council (Synergy grant 609822)
- Anna Akhmanova
H2020 European Research Council (Consolidator grant 819219)
- Lukas C Kapitein
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (ALW Open Program grant 824.15.017)
- Anna Akhmanova
H2020 Marie Skłodowska-Curie Actions (IEF fellowship)
- Maud Martin
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (STW grant OTP13391)
- Erik Meijering
Fundação para a Ciência e a Tecnologia (PhD fellowship)
- Andrea Serra-Marques
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Kassandra M Ori-McKenney, University of California, United States
Version history
- Received: July 21, 2020
- Accepted: November 10, 2020
- Accepted Manuscript published: November 11, 2020 (version 1)
- Version of Record published: December 2, 2020 (version 2)
Copyright
© 2020, Serra-Marques et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Concerted action of kinesins KIF5B and KIF13B promotes efficient secretory vesicle transport to microtubule plus ends
eLife 9:e61302.
https://doi.org/10.7554/eLife.61302
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