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Emergent chirality in active solid rotation of pancreas spheres

Tzer Han Tan, View ORCID ProfileAboutaleb Amiri, Irene Seijo-Barandiarán, Michael F. Staddon, Anne Materne, Sandra Tomas, Charlie Duclut, Marko Popović, View ORCID ProfileAnne Grapin-Botton, View ORCID ProfileFrank Jülicher
doi: https://doi.org/10.1101/2022.09.29.510101
Tzer Han Tan
1Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
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Aboutaleb Amiri
1Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
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  • ORCID record for Aboutaleb Amiri
Irene Seijo-Barandiarán
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
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Michael F. Staddon
1Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
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Anne Materne
1Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
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Sandra Tomas
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
5Center for Molecular and Cellular Bioengineering, TU Dresden, Dresden, Germany
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Charlie Duclut
1Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
6Université Paris Cité, Laboratoire Matière et Systèmes Complexes (MSC), UMR 7057 CNRS, Paris, France
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Marko Popović
1Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
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  • For correspondence: julicher@pks.mpg.de botton@mpi-cbg.de mpopovic@pks.mpg.de
Anne Grapin-Botton
2Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
4Cluster of Excellence Physics of Life, TU Dresden, Dresden, Germany
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  • For correspondence: julicher@pks.mpg.de botton@mpi-cbg.de mpopovic@pks.mpg.de
Frank Jülicher
1Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
3Center for Systems Biology Dresden, Dresden, Germany
4Cluster of Excellence Physics of Life, TU Dresden, Dresden, Germany
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  • For correspondence: julicher@pks.mpg.de botton@mpi-cbg.de mpopovic@pks.mpg.de
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Abstract

Collective cell dynamics play a crucial role in many developmental and physiological contexts. While two-dimensional (2D) cell migration has been widely studied, how three-dimensional (3D) geometry and topology interplay with collective cell behavior to determine dynamics and functions remains an open question. In this work, we elucidate the biophysical mechanism underlying rotation in spherical tissues, a phenomenon widely reported both in vivo and in vitro. Using murine pancreas-derived organoids as a model system, we find that epithelial spheres exhibit persistent rotation, rotational axis drift and rotation arrest. Using a 3D vertex model, we demonstrate how the interplay between traction force and polarity alignment can account for these distinct rotational dynamics. Furthermore, our analysis shows that the spherical tissue rotates as an active solid and exhibits spontaneous chiral symmetry breaking. Using a continuum model, we demonstrate how the types and location of topological defects in the polarity field underlie this symmetry breaking process. Altogether, our work shows that tissue chirality can arise via topological defects in the pattern of cell traction forces, with potential implications for left-right symmetry breaking processes in morphogenetic events.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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 September 30, 2022.
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Emergent chirality in active solid rotation of pancreas spheres
Tzer Han Tan, Aboutaleb Amiri, Irene Seijo-Barandiarán, Michael F. Staddon, Anne Materne, Sandra Tomas, Charlie Duclut, Marko Popović, Anne Grapin-Botton, Frank Jülicher
bioRxiv 2022.09.29.510101; doi: https://doi.org/10.1101/2022.09.29.510101
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Emergent chirality in active solid rotation of pancreas spheres
Tzer Han Tan, Aboutaleb Amiri, Irene Seijo-Barandiarán, Michael F. Staddon, Anne Materne, Sandra Tomas, Charlie Duclut, Marko Popović, Anne Grapin-Botton, Frank Jülicher
bioRxiv 2022.09.29.510101; doi: https://doi.org/10.1101/2022.09.29.510101

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