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Theory of branching morphogenesis by local interactions and global guidance

View ORCID ProfileMehmet Can Uçar, Dmitrii Kamenev, Kazunori Sunadome, Dominik Fachet, François Lallemend, Igor Adameyko, Saida Hadjab, View ORCID ProfileEdouard Hannezo
doi: https://doi.org/10.1101/2021.08.30.458198
Mehmet Can Uçar
2Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
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  • ORCID record for Mehmet Can Uçar
  • For correspondence: mehmetcan.ucar@ist.ac.at saida.hadjab@ki.se edouard.hannezo@ist.ac.at
Dmitrii Kamenev
3Department of Neuroscience, Karolinska Institutet, 17177, Stockholm, Sweden
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Kazunori Sunadome
4Department of Physiology and Pharmacology, Karolinska Institutet, 17177, Stockholm, Sweden
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Dominik Fachet
2Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
5IRI Life Sciences, Humboldt-Universität zu Berlin, Berlin, 10115, Germany
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François Lallemend
3Department of Neuroscience, Karolinska Institutet, 17177, Stockholm, Sweden
6Ming-Wai Lau Centre for Reparative Medicine, Stockholm node, Karolinska Institutet, Stockholm, Sweden
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Igor Adameyko
4Department of Physiology and Pharmacology, Karolinska Institutet, 17177, Stockholm, Sweden
7Department of Neuroimmunology, Center for Brain Research, Medical University Vienna, 1090, Vienna, Austria
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Saida Hadjab
3Department of Neuroscience, Karolinska Institutet, 17177, Stockholm, Sweden
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  • For correspondence: mehmetcan.ucar@ist.ac.at saida.hadjab@ki.se edouard.hannezo@ist.ac.at
Edouard Hannezo
2Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
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  • ORCID record for Edouard Hannezo
  • For correspondence: mehmetcan.ucar@ist.ac.at saida.hadjab@ki.se edouard.hannezo@ist.ac.at
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Abstract

Branching morphogenesis governs the formation of many organs such as lung, kidney, and the neurovascular system. Many studies have explored system-specific molecular and cellular regulatory mechanisms, as well as self-organizing rules underlying branching morphogenesis. However, in addition to local cues, branched tissue growth can also be influenced by global guidance. Here, we develop a theoretical framework for a stochastic self-organized branching process in the presence of external cues. Combining analytical theory with numerical simulations, we predict differential signatures of global vs. local regulatory mechanisms on the branching pattern, such as angle distributions, domain size, and space-filling efficiency. We find that branch alignment follows a generic scaling law determined by the strength of global guidance, while local interactions influence the tissue density but not its overall territory. Finally, using zebrafish innervation as a model system, we test these key features of the model experimentally. Our work thus provides quantitative predictions to disentangle the role of different types of cues in shaping branched structures across scales.

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. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 31, 2021.
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Theory of branching morphogenesis by local interactions and global guidance
Mehmet Can Uçar, Dmitrii Kamenev, Kazunori Sunadome, Dominik Fachet, François Lallemend, Igor Adameyko, Saida Hadjab, Edouard Hannezo
bioRxiv 2021.08.30.458198; doi: https://doi.org/10.1101/2021.08.30.458198
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Theory of branching morphogenesis by local interactions and global guidance
Mehmet Can Uçar, Dmitrii Kamenev, Kazunori Sunadome, Dominik Fachet, François Lallemend, Igor Adameyko, Saida Hadjab, Edouard Hannezo
bioRxiv 2021.08.30.458198; doi: https://doi.org/10.1101/2021.08.30.458198

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