Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning

  1. Autumn P Pomreinke
  2. Gary H Soh
  3. Katherine W Rogers
  4. Jennifer K Bergmann
  5. Alexander J Bläßle
  6. Patrick Müller  Is a corresponding author
  1. Friedrich Miescher Laboratory of the Max Planck Society, Germany

Abstract

During vertebrate embryogenesis, dorsal-ventral patterning is controlled by the BMP/Chordin activator/inhibitor system. BMP induces ventral fates, whereas Chordin inhibits BMP signaling on the dorsal side. Several theories can explain how the distributions of BMP and Chordin are regulated to achieve patterning, but the assumptions regarding activator/inhibitor diffusion and stability differ between models. Notably, “shuttling” models in which the BMP distribution is modulated by a Chordin-mediated increase in BMP diffusivity have gained recent prominence. Here, we directly test five major models by measuring the biophysical properties of fluorescently tagged BMP2b and Chordin in zebrafish embryos. We found that BMP2b and Chordin diffuse and rapidly form extracellular protein gradients, Chordin does not modulate the diffusivity or distribution of BMP2b, and Chordin is not required to establish peak levels of BMP signaling. Our findings challenge current self-regulating reaction-diffusion and shuttling models and provide support for a graded source-sink mechanism underlying zebrafish dorsal-ventral patterning.

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Author details

  1. Autumn P Pomreinke

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Gary H Soh

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Katherine W Rogers

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5700-2662
  4. Jennifer K Bergmann

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Alexander J Bläßle

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Patrick Müller

    Systems Biology of Development Group, Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, Germany
    For correspondence
    pmueller@tuebingen.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0702-6209

Funding

Max-Planck-Gesellschaft

  • Patrick Müller

Human Frontier Science Program (Career Development Award CDA00031/2013-C)

  • Patrick Müller

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

Copyright

© 2017, Pomreinke 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. Autumn P Pomreinke
  2. Gary H Soh
  3. Katherine W Rogers
  4. Jennifer K Bergmann
  5. Alexander J Bläßle
  6. Patrick Müller
(2017)
Dynamics of BMP signaling and distribution during zebrafish dorsal-ventral patterning
eLife 6:e25861.
https://doi.org/10.7554/eLife.25861

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https://doi.org/10.7554/eLife.25861