Neuronal migration prevents spatial competition in retinal morphogenesis

Mauricio Rocha-Martins (), Elisa Nerli, Jenny Kretzschmar, Martin Weigert, Jaroslav Icha, Eugene W. Myers and Caren Norden ()
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Mauricio Rocha-Martins: Instituto Gulbenkian de Ciência
Elisa Nerli: Instituto Gulbenkian de Ciência
Jenny Kretzschmar: Instituto Gulbenkian de Ciência
Martin Weigert: Max Planck Institute of Molecular Cell Biology and Genetics
Jaroslav Icha: Max Planck Institute of Molecular Cell Biology and Genetics
Eugene W. Myers: Max Planck Institute of Molecular Cell Biology and Genetics
Caren Norden: Instituto Gulbenkian de Ciência

Nature, 2023, vol. 620, issue 7974, 615-624

Abstract: Abstract The concomitant occurrence of tissue growth and organization is a hallmark of organismal development1–3. This often means that proliferating and differentiating cells are found at the same time in a continuously changing tissue environment. How cells adapt to architectural changes to prevent spatial interference remains unclear. Here, to understand how cell movements that are key for growth and organization are orchestrated, we study the emergence of photoreceptor neurons that occur during the peak of retinal growth, using zebrafish, human tissue and human organoids. Quantitative imaging reveals that successful retinal morphogenesis depends on the active bidirectional translocation of photoreceptors, leading to a transient transfer of the entire cell population away from the apical proliferative zone. This pattern of migration is driven by cytoskeletal machineries that differ depending on the direction: microtubules are exclusively required for basal translocation, whereas actomyosin is involved in apical movement. Blocking the basal translocation of photoreceptors induces apical congestion, which hampers the apical divisions of progenitor cells and leads to secondary defects in lamination. Thus, photoreceptor migration is crucial to prevent competition for space, and to allow concurrent tissue growth and lamination. This shows that neuronal migration, in addition to its canonical role in cell positioning4, can be involved in coordinating morphogenesis.

Date: 2023
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DOI: 10.1038/s41586-023-06392-y

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