Understanding the factors that direct tissue organization during development is one of the most fundamental goals in developmental biology. Various hypotheses explain cell sorting and tissue organization on the basis of the adhesive and mechanical properties of the constituent cells1. However, validating these hypotheses has been difficult due to the lack of appropriate tools to measure these parameters. Here we use atomic force microscopy (AFM) to quantify the adhesive and mechanical properties of individual ectoderm, mesoderm and endoderm progenitor cells from gastrulating zebrafish embryos. Combining these data with tissue self-assembly in vitro and the sorting behaviour of progenitors in vivo, we have shown that differential actomyosin-dependent cell-cortex tension, regulated by Nodal/TGFβ-signalling (transforming growth factor β), constitutes a key factor that directs progenitor-cell sorting. These results demonstrate a previously unrecognized role for Nodal-controlled cell-cortex tension in germ-layer organization during gastrulation.
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We thank Pierre Bongrand, Wayne Brodland, Jonne Helenius, Mathias Köppen, Andy Oates, Ewa Paluch, Laurel Rohde, Erik Schäffer, Clemens Franz, Sylvia Schneider, Petra Stockinger, Anna Taubenberger, Florian Ulrich and Simon Wilkins for fruitful discussions; Stan Marée for sharing the simulation code for the Cellular-Potts-Model; Lara Carvalho for sharing unpublished results; JPK Instruments for technical support; Jonne Helenius for supporting data analysis procedures and the fifth floor seminar club for vibrant discussions. This work was supported by grants from the Boehringer Ingelheim Fonds to M. K., Deutsch-Französische Hochschule to M. K. and P. H. P. and the Deutsche Forschungsgemeinschaft to C. P. H.
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Krieg, M., Arboleda-Estudillo, Y., Puech, PH. et al. Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 10, 429–436 (2008). https://doi.org/10.1038/ncb1705
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