Multi-cellular logistics of collective cell migration.

During development, the formation of biological networks (such as organs and neuronal networks) is controlled by multicellular transportation phenomena based on cell migration. In multi-cellular systems, cellular locomotion is restricted by physical interactions with other cells in a crowded space,...

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Autores principales: Masataka Yamao, Honda Naoki, Shin Ishii
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Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2011
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Acceso en línea:https://doaj.org/article/176b8967f52b4fde87419b9e65415dd9
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spelling oai:doaj.org-article:176b8967f52b4fde87419b9e65415dd92021-11-18T07:31:47ZMulti-cellular logistics of collective cell migration.1932-620310.1371/journal.pone.0027950https://doaj.org/article/176b8967f52b4fde87419b9e65415dd92011-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22205934/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203During development, the formation of biological networks (such as organs and neuronal networks) is controlled by multicellular transportation phenomena based on cell migration. In multi-cellular systems, cellular locomotion is restricted by physical interactions with other cells in a crowded space, similar to passengers pushing others out of their way on a packed train. The motion of individual cells is intrinsically stochastic and may be viewed as a type of random walk. However, this walk takes place in a noisy environment because the cell interacts with its randomly moving neighbors. Despite this randomness and complexity, development is highly orchestrated and precisely regulated, following genetic (and even epigenetic) blueprints. Although individual cell migration has long been studied, the manner in which stochasticity affects multi-cellular transportation within the precisely controlled process of development remains largely unknown. To explore the general principles underlying multicellular migration, we focus on the migration of neural crest cells, which migrate collectively and form streams. We introduce a mechanical model of multi-cellular migration. Simulations based on the model show that the migration mode depends on the relative strengths of the noise from migratory and non-migratory cells. Strong noise from migratory cells and weak noise from surrounding cells causes "collective migration," whereas strong noise from non-migratory cells causes "dispersive migration." Moreover, our theoretical analyses reveal that migratory cells attract each other over long distances, even without direct mechanical contacts. This effective interaction depends on the stochasticity of the migratory and non-migratory cells. On the basis of these findings, we propose that stochastic behavior at the single-cell level works effectively and precisely to achieve collective migration in multi-cellular systems.Masataka YamaoHonda NaokiShin IshiiPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 12, p e27950 (2011)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Masataka Yamao
Honda Naoki
Shin Ishii
Multi-cellular logistics of collective cell migration.
description During development, the formation of biological networks (such as organs and neuronal networks) is controlled by multicellular transportation phenomena based on cell migration. In multi-cellular systems, cellular locomotion is restricted by physical interactions with other cells in a crowded space, similar to passengers pushing others out of their way on a packed train. The motion of individual cells is intrinsically stochastic and may be viewed as a type of random walk. However, this walk takes place in a noisy environment because the cell interacts with its randomly moving neighbors. Despite this randomness and complexity, development is highly orchestrated and precisely regulated, following genetic (and even epigenetic) blueprints. Although individual cell migration has long been studied, the manner in which stochasticity affects multi-cellular transportation within the precisely controlled process of development remains largely unknown. To explore the general principles underlying multicellular migration, we focus on the migration of neural crest cells, which migrate collectively and form streams. We introduce a mechanical model of multi-cellular migration. Simulations based on the model show that the migration mode depends on the relative strengths of the noise from migratory and non-migratory cells. Strong noise from migratory cells and weak noise from surrounding cells causes "collective migration," whereas strong noise from non-migratory cells causes "dispersive migration." Moreover, our theoretical analyses reveal that migratory cells attract each other over long distances, even without direct mechanical contacts. This effective interaction depends on the stochasticity of the migratory and non-migratory cells. On the basis of these findings, we propose that stochastic behavior at the single-cell level works effectively and precisely to achieve collective migration in multi-cellular systems.
format article
author Masataka Yamao
Honda Naoki
Shin Ishii
author_facet Masataka Yamao
Honda Naoki
Shin Ishii
author_sort Masataka Yamao
title Multi-cellular logistics of collective cell migration.
title_short Multi-cellular logistics of collective cell migration.
title_full Multi-cellular logistics of collective cell migration.
title_fullStr Multi-cellular logistics of collective cell migration.
title_full_unstemmed Multi-cellular logistics of collective cell migration.
title_sort multi-cellular logistics of collective cell migration.
publisher Public Library of Science (PLoS)
publishDate 2011
url https://doaj.org/article/176b8967f52b4fde87419b9e65415dd9
work_keys_str_mv AT masatakayamao multicellularlogisticsofcollectivecellmigration
AT hondanaoki multicellularlogisticsofcollectivecellmigration
AT shinishii multicellularlogisticsofcollectivecellmigration
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