1. Cell Biology
  2. Physics of Living Systems
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Concerted action of kinesins KIF5B and KIF13B promotes efficient secretory vesicle transport to microtubule plus ends

  1. Andrea Serra-Marques
  2. Maud Martin
  3. Eugene A Katrukha
  4. Ilya Grigoriev
  5. Cathelijn AE Peeters
  6. Qingyang Liu
  7. Peter Jan Hooikaas
  8. Yao Yao
  9. Veronika Solianova
  10. Ihor Smal
  11. Lotte B Pedersen
  12. Erik Meijering
  13. Lukas C Kapitein
  14. Anna Akhmanova  Is a corresponding author
  1. University of California, San Francisco, United States
  2. Utrecht University, Netherlands
  3. Erasmus University Medical Center, Netherlands
  4. University of Copenhagen, Denmark
  5. University of New South Wales, Australia
Research Article
  • Cited 5
  • Views 1,547
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Cite this article as: eLife 2020;9:e61302 doi: 10.7554/eLife.61302

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

  1. Andrea Serra-Marques

    Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4215-3024
  2. Maud Martin

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0048-6437
  3. Eugene A Katrukha

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
  4. Ilya Grigoriev

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
  5. Cathelijn AE Peeters

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
  6. Qingyang Liu

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
  7. Peter Jan Hooikaas

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9849-9193
  8. Yao Yao

    Medical Informatics and Radiology, Erasmus University Medical Center, Rotterdam, Netherlands
    Competing interests
    No competing interests declared.
  9. Veronika Solianova

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
  10. Ihor Smal

    Medical Informatics and Radiology, Erasmus University Medical Center, Rotterdam, Netherlands
    Competing interests
    No competing interests declared.
  11. Lotte B Pedersen

    Department of Biology, University of Copenhagen, Copenhagen, Denmark
    Competing interests
    Lotte B Pedersen, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9749-3758
  12. Erik Meijering

    Computer Science and Engineering, University of New South Wales, Sydney, Australia
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8015-8358
  13. Lukas C Kapitein

    Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9418-6739
  14. Anna Akhmanova

    Department of Biology, Utrecht University, Utrecht, Netherlands
    For correspondence
    a.akhmanova@uu.nl
    Competing interests
    Anna Akhmanova, Deputy editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9048-8614

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

  1. Kassandra M Ori-McKenney, University of California, United States

Publication history

  1. Received: July 21, 2020
  2. Accepted: November 10, 2020
  3. Accepted Manuscript published: November 11, 2020 (version 1)
  4. 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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