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Coupled organoids reveal that signaling gradients drive traveling segmentation clock waves during human axial morphogenesis

Yusuf Ilker Yaman, Roya Huang, Sharad Ramanathan
doi: https://doi.org/10.1101/2022.05.10.491359
Yusuf Ilker Yaman
1John A. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA
3Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
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  • For correspondence: yyaman@g.harvard.edu sharad@cgr.harvard.edu
Roya Huang
2Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA
3Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
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Sharad Ramanathan
1John A. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA
2Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA
3Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA
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  • For correspondence: yyaman@g.harvard.edu sharad@cgr.harvard.edu
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Summary

Axial development of mammals is a dynamic process involving several coordinated morphogenetic events including axial elongation, somitogenesis, and neural tube formation. How different signals control the dynamics of human axial morphogenesis remains largely unknown. By inducing anteroposterior symmetry breaking of spatially coupled epithelial cysts derived from human pluripotent stem cells, we were able to generate hundreds of axially elongating organoids. Each organoid was composed of a neural tube flanked by presomitic mesoderm that was sequentially segmented into somites. Periodic activation of the somite differentiation gene MESP2 coincided in space and time with anteriorly traveling segmentation clock waves in the presomitic mesoderm of the organoids, recapitulating key aspects of somitogenesis. Through timed perturbations of organoids, we demonstrated that FGF and WNT signaling play distinct roles in axial elongation and somitogenesis, and that the segmentation clock waves are driven by FGF signaling gradients. By generating and perturbing organoids that robustly recapitulate the architecture and dynamics of multiple axial tissues in human embryos, this work offers a means to dissect complex mechanisms underlying human embryogenesis.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 11, 2022.
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Coupled organoids reveal that signaling gradients drive traveling segmentation clock waves during human axial morphogenesis
Yusuf Ilker Yaman, Roya Huang, Sharad Ramanathan
bioRxiv 2022.05.10.491359; doi: https://doi.org/10.1101/2022.05.10.491359
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Coupled organoids reveal that signaling gradients drive traveling segmentation clock waves during human axial morphogenesis
Yusuf Ilker Yaman, Roya Huang, Sharad Ramanathan
bioRxiv 2022.05.10.491359; doi: https://doi.org/10.1101/2022.05.10.491359

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