Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming

article Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming published yes Diana C Nunes Pinheiro author 2E839F16-F248-11E8-B48F-1D18A9856A870000-0003-4333-7503 Roland Kardos author 4039350E-F248-11E8-B48F-1D18A9856A87 Edouard B Hannezo author 3A9DB764-F248-11E8-B48F-1D18A9856A870000-0001-6005-1561 Carl-Philipp J Heisenberg author 39427864-F248-11E8-B48F-1D18A9856A870000-0002-0912-4566 CaHe department EdHa department Coordination of mesendoderm cell fate specification and internalization during zebrafish gastrulation project Coordination of mesendoderm cell fate specification and internalization during zebrafish gastrulation project Design Principles of Branching Morphogenesis project Interaction and feedback between cell mechanics and fate specification in vertebrate gastrulation project Embryo development requires biochemical signalling to generate patterns of cell fates and active mechanical forces to drive tissue shape changes. However, how these processes are coordinated, and how tissue patterning is preserved despite the cellular flows occurring during morphogenesis, remains poorly understood. Gastrulation is a crucial embryonic stage that involves both patterning and internalization of the mesendoderm germ layer tissue. Here we show that, in zebrafish embryos, a gradient in Nodal signalling orchestrates pattern-preserving internalization movements by triggering a motility-driven unjamming transition. In addition to its role as a morphogen determining embryo patterning, graded Nodal signalling mechanically subdivides the mesendoderm into a small fraction of highly protrusive leader cells, able to autonomously internalize via local unjamming, and less protrusive followers, which need to be pulled inwards by the leaders. The Nodal gradient further enforces a code of preferential adhesion coupling leaders to their immediate followers, resulting in a collective and ordered mode of internalization that preserves mesendoderm patterning. Integrating this dual mechanical role of Nodal signalling into minimal active particle simulations quantitatively predicts both physiological and experimentally perturbed internalization movements. This provides a quantitative framework for how a morphogen-encoded unjamming transition can bidirectionally couple tissue mechanics with patterning during complex three-dimensional morphogenesis. https://research-explorer.ista.ac.at/download/12209/12412/2022_NaturePhysics_Pinheiro.pdf application/pdfno https://creativecommons.org/licenses/by/4.0/ Springer Nature2022 eng General Physics and Astronomy Nature Physics 1745-2473 1745-2481 00087131990000210.1038/s41567-022-01787-6 18121482-1493 Nunes Pinheiro, Diana C., et al. “Morphogen Gradient Orchestrates Pattern-Preserving Tissue Morphogenesis via Motility-Driven Unjamming.” Nature Physics, vol. 18, no. 12, Springer Nature, 2022, pp. 1482–93, doi:<a href="https://doi.org/10.1038/s41567-022-01787-6">10.1038/s41567-022-01787-6</a>. Nunes Pinheiro, Diana C, Roland Kardos, Edouard B Hannezo, and Carl-Philipp J Heisenberg. “Morphogen Gradient Orchestrates Pattern-Preserving Tissue Morphogenesis via Motility-Driven Unjamming.” Nature Physics. Springer Nature, 2022. <a href="https://doi.org/10.1038/s41567-022-01787-6">https://doi.org/10.1038/s41567-022-01787-6</a>. D. C. Nunes Pinheiro, R. Kardos, E. B. Hannezo, and C.-P. J. Heisenberg, “Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming,” Nature Physics, vol. 18, no. 12. Springer Nature, pp. 1482–1493, 2022. Nunes Pinheiro DC, Kardos R, Hannezo EB, Heisenberg C-PJ. 2022. Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming. Nature Physics. 18(12), 1482–1493. Nunes Pinheiro DC, Kardos R, Hannezo EB, Heisenberg C-PJ. Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming. Nature Physics. 2022;18(12):1482-1493. doi:<a href="https://doi.org/10.1038/s41567-022-01787-6">10.1038/s41567-022-01787-6</a> D.C. Nunes Pinheiro, R. Kardos, E.B. Hannezo, C.-P.J. Heisenberg, Nature Physics 18 (2022) 1482–1493. Nunes Pinheiro, D. C., Kardos, R., Hannezo, E. B., & Heisenberg, C.-P. J. (2022). Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming. Nature Physics. Springer Nature. <a href="https://doi.org/10.1038/s41567-022-01787-6">https://doi.org/10.1038/s41567-022-01787-6</a> 122092023-01-16T09:45:19Z2025-04-14T07:46:59Z