Light-activated Frizzled7 reveals a permissive role of non-canonical Wnt signaling in mesendoderm cell migration

  1. Daniel Čapek
  2. Michael Smutny
  3. Alexandra-Madelaine Tichy
  4. Maurizio Morri
  5. Harald Janovjak
  6. Carl-Philipp Heisenberg  Is a corresponding author
  1. Institute of Science and Technology Austria, Austria
  2. Monash University, Australia

Abstract

Non-canonical Wnt-signaling plays a central role for coordinated cell polarization and directed migration in metazoan development. While spatiotemporally restricted activation of non-canonical Wnt-signaling drives cell polarization in epithelial tissues, it remains unclear whether such instructive activity is also critical for directed mesenchymal cell migration. Here, we developed a light-activated version of the non-canonical Wnt receptor Frizzled 7 (Fz7) to analyze how restricted activation of non-canonical Wnt-signaling affects directed anterior axial mesendoderm (prechordal plate, ppl) cell migration within the zebrafish gastrula. We found that Fz7 signaling is required for ppl cell protrusion formation and migration, and that spatiotemporally restricted ectopic activation is capable of redirecting their migration. Finally, we show that uniform activation of Fz7 signaling in ppl cells fully rescues defective directed cell migration in fz7 mutant embryos. Together, our findings reveal that in contrast to the situation in epithelial cells, non-canonical Wnt-signaling functions permissively rather than instructively in directed mesenchymal cell migration during gastrulation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1-5, and figure supplements S1, S2, and S4-10

Article and author information

Author details

  1. Daniel Čapek

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  2. Michael Smutny

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5920-9090
  3. Alexandra-Madelaine Tichy

    Faculty of Medicine, Nursing and Health Sciences, Australian Regenerative Medicine Institute (ARMI), Monash University, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Maurizio Morri

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  5. Harald Janovjak

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    Competing interests
    The authors declare that no competing interests exist.
  6. Carl-Philipp Heisenberg

    Institute of Science and Technology Austria, Klosterneuburg, Austria
    For correspondence
    heisenberg@ist.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0912-4566

Funding

European Research Council (742573)

  • Carl-Philipp Heisenberg

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

Ethics

Animal experimentation: Experiments involving zebrafish reported in this study included the creation and maintenance of transgenic mutant lines of zebrafish. In my role as Ethics Officer at IST Austria, I herewith confirm that the use of animals for experimental purposes within the scope of this study does not require the approval of the Ethics Committee at IST Austria. In line with EU directive 2010/63/EU on the protection of animals used for scientific purposes, Austrian legislation requires that the use of animals for scientific purposes has to be approved by the respective unit at the Federal Ministry of Education, Science, and Research. This process includes an ethical evaluation of the planned experiments as part of the harm-benefit analysis. Beyond that no further approval by the Ethics Committee at IST Austria is required. The respective approval number that covers the experiments that were performed is 66.018/0010-WF/II/3b/2014.Yours sincerely,Dr. Verena SeibothEthics Officer

Reviewing Editor

  1. Didier Y Stainier, Max Planck Institute for Heart and Lung Research, Germany

Publication history

  1. Received: September 17, 2018
  2. Accepted: January 14, 2019
  3. Accepted Manuscript published: January 16, 2019 (version 1)
  4. Version of Record published: February 6, 2019 (version 2)

Copyright

© 2019, Čapek 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. Daniel Čapek
  2. Michael Smutny
  3. Alexandra-Madelaine Tichy
  4. Maurizio Morri
  5. Harald Janovjak
  6. Carl-Philipp Heisenberg
(2019)
Light-activated Frizzled7 reveals a permissive role of non-canonical Wnt signaling in mesendoderm cell migration
eLife 8:e42093.
https://doi.org/10.7554/eLife.42093

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