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Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns

In vertebrate embryos, somites, the precursor of vertebrae, form from the presomitic mesoderm (PSM), which is composed of cells displaying signaling oscillations. Cellular oscillatory activity leads to periodic wave patterns in the PSM. Here, we address the origin of such complex wave patterns. We e...

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Detalles Bibliográficos
Autores principales: Tsiairis, Charisios D., Aulehla, Alexander
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4752819/
https://www.ncbi.nlm.nih.gov/pubmed/26871631
http://dx.doi.org/10.1016/j.cell.2016.01.028
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author Tsiairis, Charisios D.
Aulehla, Alexander
author_facet Tsiairis, Charisios D.
Aulehla, Alexander
author_sort Tsiairis, Charisios D.
collection PubMed
description In vertebrate embryos, somites, the precursor of vertebrae, form from the presomitic mesoderm (PSM), which is composed of cells displaying signaling oscillations. Cellular oscillatory activity leads to periodic wave patterns in the PSM. Here, we address the origin of such complex wave patterns. We employed an in vitro randomization and real-time imaging strategy to probe for the ability of cells to generate order from disorder. We found that, after randomization, PSM cells self-organized into several miniature emergent PSM structures (ePSM). Our results show an ordered macroscopic spatial arrangement of ePSM with evidence of an intrinsic length scale. Furthermore, cells actively synchronize oscillations in a Notch-signaling-dependent manner, re-establishing wave-like patterns of gene activity. We demonstrate that PSM cells self-organize by tuning oscillation dynamics in response to surrounding cells, leading to collective synchronization with an average frequency. These findings reveal emergent properties within an ensemble of coupled genetic oscillators.
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spelling pubmed-47528192016-03-02 Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns Tsiairis, Charisios D. Aulehla, Alexander Cell Article In vertebrate embryos, somites, the precursor of vertebrae, form from the presomitic mesoderm (PSM), which is composed of cells displaying signaling oscillations. Cellular oscillatory activity leads to periodic wave patterns in the PSM. Here, we address the origin of such complex wave patterns. We employed an in vitro randomization and real-time imaging strategy to probe for the ability of cells to generate order from disorder. We found that, after randomization, PSM cells self-organized into several miniature emergent PSM structures (ePSM). Our results show an ordered macroscopic spatial arrangement of ePSM with evidence of an intrinsic length scale. Furthermore, cells actively synchronize oscillations in a Notch-signaling-dependent manner, re-establishing wave-like patterns of gene activity. We demonstrate that PSM cells self-organize by tuning oscillation dynamics in response to surrounding cells, leading to collective synchronization with an average frequency. These findings reveal emergent properties within an ensemble of coupled genetic oscillators. Cell Press 2016-02-11 /pmc/articles/PMC4752819/ /pubmed/26871631 http://dx.doi.org/10.1016/j.cell.2016.01.028 Text en © 2016 The Authors http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Tsiairis, Charisios D.
Aulehla, Alexander
Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns
title Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns
title_full Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns
title_fullStr Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns
title_full_unstemmed Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns
title_short Self-Organization of Embryonic Genetic Oscillators into Spatiotemporal Wave Patterns
title_sort self-organization of embryonic genetic oscillators into spatiotemporal wave patterns
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4752819/
https://www.ncbi.nlm.nih.gov/pubmed/26871631
http://dx.doi.org/10.1016/j.cell.2016.01.028
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