Amoeboid-like migration ensures correct horizontal cell layer formation in the developing vertebrate retina

  1. Rana Amini
  2. Archit Bhatnagar
  3. Raimund Schlüßler
  4. Stephanie Möllmert
  5. Jochen Guck
  6. Caren Norden  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. Technische Universität Dresden, Germany
  3. Max Planck Institute for the Science of Light, Germany

Abstract

Migration of cells in the developing brain is integral for the establishment of neural circuits and function of the central nervous system. While migration modes during which neurons employ predetermined directional guidance of either preexisting neuronal processes or underlying cells have been well explored, less is known about how cells featuring multipolar morphology migrate in the dense environment of the developing brain. To address this, we here investigated multipolar migration of horizontal cells in the zebrafish retina. We found that these cells feature several hallmarks of amoeboid-like migration that enable them to tailor their movements to the spatial constraints of the crowded retina. These hallmarks include cell and nuclear shape changes, as well as persistent rearward polarization of stable F-actin. Interference with the organization of the developing retina by changing nuclear properties or overall tissue architecture, hampers efficient horizontal cell migration and layer formation showing that cell-tissue interplay is crucial for this process. In view of the high proportion of multipolar migration phenomena observed in brain development, the here uncovered ameboid-like migration mode might be conserved in other areas of the developing nervous system.

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All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided

Article and author information

Author details

  1. Rana Amini

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3974-5072
  2. Archit Bhatnagar

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Raimund Schlüßler

    Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3752-2382
  4. Stephanie Möllmert

    Max Planck Institute for the Science of Light, Erlangen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Jochen Guck

    Max Planck Institute for the Science of Light, Erlangen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Caren Norden

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    cnorden@igc.gulbenkian.pt
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8835-1451

Funding

H2020 European Research Council (ERC-2018-CoG-81904)

  • Caren Norden

Natural Sciences and Engineering Research Council of Canada (502961)

  • Rana Amini

Fonds de Recherche du Québec - Santé (35510)

  • Rana Amini

Max Planck Institute of Molecular Cell Biology and Genetics (open access funding)

  • Rana Amini

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 animal work was performed in accordance with the European Union (EU) directive 2010/63/EU, as well as the German Animal Welfare act.

Copyright

© 2022, Amini 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. Rana Amini
  2. Archit Bhatnagar
  3. Raimund Schlüßler
  4. Stephanie Möllmert
  5. Jochen Guck
  6. Caren Norden
(2022)
Amoeboid-like migration ensures correct horizontal cell layer formation in the developing vertebrate retina
eLife 11:e76408.
https://doi.org/10.7554/eLife.76408

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https://doi.org/10.7554/eLife.76408