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Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues

View ORCID ProfileGuillermo Martínez-Ara, Núria Taberner, Mami Takayama, Elissavet Sandaltzopoulou, Casandra E. Villava, Nozomu Takata, Mototsugu Eiraku, View ORCID ProfileMiki Ebisuya
doi: https://doi.org/10.1101/2021.04.20.440475
Guillermo Martínez-Ara
1European Molecular Biology Laboratory (EMBL) Barcelona, Dr. Aiguader 88, 08003 Barcelona, Spain
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  • ORCID record for Guillermo Martínez-Ara
Núria Taberner
1European Molecular Biology Laboratory (EMBL) Barcelona, Dr. Aiguader 88, 08003 Barcelona, Spain
2RIKEN Center for Biosystems Dynamics Research (RIKEN BDR), 2-2-3 Minatojima-minamimachi, Chuo-ku, 650-0047 Kobe, Japan
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Mami Takayama
2RIKEN Center for Biosystems Dynamics Research (RIKEN BDR), 2-2-3 Minatojima-minamimachi, Chuo-ku, 650-0047 Kobe, Japan
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Elissavet Sandaltzopoulou
1European Molecular Biology Laboratory (EMBL) Barcelona, Dr. Aiguader 88, 08003 Barcelona, Spain
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Casandra E. Villava
1European Molecular Biology Laboratory (EMBL) Barcelona, Dr. Aiguader 88, 08003 Barcelona, Spain
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Nozomu Takata
2RIKEN Center for Biosystems Dynamics Research (RIKEN BDR), 2-2-3 Minatojima-minamimachi, Chuo-ku, 650-0047 Kobe, Japan
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Mototsugu Eiraku
2RIKEN Center for Biosystems Dynamics Research (RIKEN BDR), 2-2-3 Minatojima-minamimachi, Chuo-ku, 650-0047 Kobe, Japan
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Miki Ebisuya
1European Molecular Biology Laboratory (EMBL) Barcelona, Dr. Aiguader 88, 08003 Barcelona, Spain
2RIKEN Center for Biosystems Dynamics Research (RIKEN BDR), 2-2-3 Minatojima-minamimachi, Chuo-ku, 650-0047 Kobe, Japan
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  • ORCID record for Miki Ebisuya
  • For correspondence: miki.ebisuya@embl.es
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ABSTRACT

During embryonic development, cellular forces synchronize in space and time to generate functional tissue shapes. Apical constriction is one of these force-generating processes, and it is necessary to modulate epithelial curvature in fundamental morphogenetic events, such as neural tube folding. The emerging field of synthetic developmental biology proposes bottom-up approaches to examine the contribution of each cellular process to complex morphogenesis. However, the shortage of tools to manipulate three-dimensional (3D) shapes of mammalian tissues currently hinders the progress of the field. Here we report the development of “OptoShroom3”, a new optogenetic tool that achieves fast spatiotemporal control of apical constriction in mammalian epithelia. Activation of OptoShroom3 through illumination of individual cells in an epithelial cell sheet reduced their apical surface while illumination of groups of cells caused deformation in the adjacent regions. By using OptoShroom3, we further manipulated 3D tissue shapes. Light-induced apical constriction provoked the folding of epithelial cell colonies on soft gels. Its application to murine and human neural organoids led to thickening of neuroepithelia, apical lumen reduction in optic vesicles, and flattening in neuroectodermal tissues. These results show that spatiotemporal control of apical constriction can trigger several types of 3D deformation depending on the initial tissue context.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Minor correction and updates regarding the genetic constructs (Fig 1 and method)

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted April 26, 2022.
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Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
Guillermo Martínez-Ara, Núria Taberner, Mami Takayama, Elissavet Sandaltzopoulou, Casandra E. Villava, Nozomu Takata, Mototsugu Eiraku, Miki Ebisuya
bioRxiv 2021.04.20.440475; doi: https://doi.org/10.1101/2021.04.20.440475
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Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
Guillermo Martínez-Ara, Núria Taberner, Mami Takayama, Elissavet Sandaltzopoulou, Casandra E. Villava, Nozomu Takata, Mototsugu Eiraku, Miki Ebisuya
bioRxiv 2021.04.20.440475; doi: https://doi.org/10.1101/2021.04.20.440475

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