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Theory of branching morphogenesis by local interactions and global guidance

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...

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Autores principales: Uçar, Mehmet Can, Kamenev, Dmitrii, Sunadome, Kazunori, Fachet, Dominik, Lallemend, Francois, Adameyko, Igor, Hadjab, Saida, Hannezo, Edouard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8613190/
https://www.ncbi.nlm.nih.gov/pubmed/34819507
http://dx.doi.org/10.1038/s41467-021-27135-5
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author Uçar, Mehmet Can
Kamenev, Dmitrii
Sunadome, Kazunori
Fachet, Dominik
Lallemend, Francois
Adameyko, Igor
Hadjab, Saida
Hannezo, Edouard
author_facet Uçar, Mehmet Can
Kamenev, Dmitrii
Sunadome, Kazunori
Fachet, Dominik
Lallemend, Francois
Adameyko, Igor
Hadjab, Saida
Hannezo, Edouard
author_sort Uçar, Mehmet Can
collection PubMed
description 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.
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spelling pubmed-86131902021-12-01 Theory of branching morphogenesis by local interactions and global guidance Uçar, Mehmet Can Kamenev, Dmitrii Sunadome, Kazunori Fachet, Dominik Lallemend, Francois Adameyko, Igor Hadjab, Saida Hannezo, Edouard Nat Commun Article 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. Nature Publishing Group UK 2021-11-24 /pmc/articles/PMC8613190/ /pubmed/34819507 http://dx.doi.org/10.1038/s41467-021-27135-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Uçar, Mehmet Can
Kamenev, Dmitrii
Sunadome, Kazunori
Fachet, Dominik
Lallemend, Francois
Adameyko, Igor
Hadjab, Saida
Hannezo, Edouard
Theory of branching morphogenesis by local interactions and global guidance
title Theory of branching morphogenesis by local interactions and global guidance
title_full Theory of branching morphogenesis by local interactions and global guidance
title_fullStr Theory of branching morphogenesis by local interactions and global guidance
title_full_unstemmed Theory of branching morphogenesis by local interactions and global guidance
title_short Theory of branching morphogenesis by local interactions and global guidance
title_sort theory of branching morphogenesis by local interactions and global guidance
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8613190/
https://www.ncbi.nlm.nih.gov/pubmed/34819507
http://dx.doi.org/10.1038/s41467-021-27135-5
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