1. Developmental Biology
  2. Physics of Living Systems

Quantitative analyses reveal extracellular dynamics of Wnt ligands in Xenopus embryos

  1. Yusuke Mii  Is a corresponding author
  2. Kenichi Nakazato
  3. Chan-Gi Pack
  4. Takafumi Ikeda
  5. Yasushi Sako
  6. Atsushi Mochizuki
  7. Masanori Taira  Is a corresponding author
  8. Shinji Takada
  1. National Institute for Basic Biology, Japan
  2. RIKEN, Japan
  3. University of Tokyo, Japan
  4. Kyoto University, Japan
  5. National Institutes of Natural Sciences, Japan
https://doi.org/10.7554/eLife.55108
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Cite this article
  1. Yusuke Mii
  2. Kenichi Nakazato
  3. Chan-Gi Pack
  4. Takafumi Ikeda
  5. Yasushi Sako
  6. Atsushi Mochizuki
  7. Masanori Taira
  8. Shinji Takada
(2021)
Quantitative analyses reveal extracellular dynamics of Wnt ligands in Xenopus embryos
eLife 10:e55108.
https://doi.org/10.7554/eLife.55108
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Abstract

The mechanism of intercellular transport of Wnt ligands is still a matter of debate. To better understand this issue, we examined the distribution and dynamics of Wnt8 in Xenopus embryos. While Venus-tagged Wnt8 was found on the surfaces of cells close to Wnt-producing cells, we also detected its dispersal over distances of 15 cell diameters. A combination of fluorescence correlation spectroscopy and quantitative imaging suggested that only a small proportion of Wnt8 ligands diffuses freely, whereas most Wnt8 molecules are bound to cell surfaces. Fluorescence decay after photoconversion showed that Wnt8 ligands bound on cell surfaces decrease exponentially, suggesting a dynamic exchange of bound forms of Wnt ligands. Mathematical modelling based on this exchange recapitulates a graded distribution of bound, but not free, Wnt ligands. Based on these results, we propose that Wnt distribution in tissues is controlled by a dynamic exchange of its abundant bound and rare free populations.

Data availability

Sequence data for anti-HA IgG genes have been deposited in Genbank/DDBJ under accession codes LC522514 and LC522515.

The following data sets were generated

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Author details

  1. Yusuke Mii

    Department of Developmental Biology, National Institute for Basic Biology, Okazaki, Japan
    For correspondence
    mii@nibb.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1907-5665

  2. Kenichi Nakazato

    Theoretical Biology Laboratory, RIKEN, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.

  3. Chan-Gi Pack

    Cellular Informatics Laboratory, RIKEN, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6578-3099

  4. Takafumi Ikeda

    Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.

  5. Yasushi Sako

    Cellular Informatics Laboratory, RIKEN, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.

  6. Atsushi Mochizuki

    Department of Biosystems Science, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.

  7. Masanori Taira

    Department of Biological Sciences, University of Tokyo, Tokyo, Japan
    For correspondence
    m-taira.183@g.chuo-u.ac.jp
    Competing interests
    The authors declare that no competing interests exist.

  8. Shinji Takada

    Okazaki Institute for Integrative Bioscience, National Institutes of Natural Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4125-6056

Funding

Japan Science and Technology Agency (JPMJPR194B)

  • Yusuke Mii

Japan Society for the Promotion of Science (24870031)

  • Yusuke Mii

Japan Society for the Promotion of Science (15K14532)

  • Yusuke Mii

Japan Society for the Promotion of Science (18K14720)

  • Yusuke Mii

Japan Society for the Promotion of Science (17K19418)

  • Shinji Takada

Japan Society for the Promotion of Science (24657147)

  • Yusuke Mii
  • Masanori Taira

National Institutes of Natural Sciences (1311608,01311801)

  • Yusuke Mii

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments using Xenopus laevis were approved by the Institutional Animal Care and Use Committee, National Institutes of Natural Sciences (Permit Number 18A038, 19A062, 20A053), or the Office for Life Science Research Ethics and Safety, University of Tokyo.

Copyright

© 2021, Mii 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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  1. Yusuke Mii
  2. Kenichi Nakazato
  3. Chan-Gi Pack
  4. Takafumi Ikeda
  5. Yasushi Sako
  6. Atsushi Mochizuki
  7. Masanori Taira
  8. Shinji Takada
(2021)
Quantitative analyses reveal extracellular dynamics of Wnt ligands in Xenopus embryos
eLife 10:e55108.
https://doi.org/10.7554/eLife.55108

Share this article

https://doi.org/10.7554/eLife.55108

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