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Self-organization of chemoattractant waves in Dictyostelium depends on F-actin and cell–substrate adhesion

In the social amoeba Dictyostelium discoideum, travelling waves of extracellular cyclic adenosine monophosphate (cAMP) self-organize in cell populations and direct aggregation of individual cells to form multicellular fruiting bodies. In contrast to the large body of studies that addressed how movem...

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Autores principales: Fukujin, Fumihito, Nakajima, Akihiko, Shimada, Nao, Sawai, Satoshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4938087/
https://www.ncbi.nlm.nih.gov/pubmed/27358278
http://dx.doi.org/10.1098/rsif.2016.0233
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author Fukujin, Fumihito
Nakajima, Akihiko
Shimada, Nao
Sawai, Satoshi
author_facet Fukujin, Fumihito
Nakajima, Akihiko
Shimada, Nao
Sawai, Satoshi
author_sort Fukujin, Fumihito
collection PubMed
description In the social amoeba Dictyostelium discoideum, travelling waves of extracellular cyclic adenosine monophosphate (cAMP) self-organize in cell populations and direct aggregation of individual cells to form multicellular fruiting bodies. In contrast to the large body of studies that addressed how movement of cells is determined by spatial and temporal cues encoded in the dynamic cAMP gradients, how cell mechanics affect the formation of a self-generated chemoattractant field has received less attention. Here, we show, by live cell imaging analysis, that the periodicity of the synchronized cAMP waves increases in cells treated with the actin inhibitor latrunculin. Detail analysis of the extracellular cAMP-induced transients of cytosolic cAMP (cAMP relay response) in well-isolated cells demonstrated that their amplitude and duration were markedly reduced in latrunculin-treated cells. Similarly, in cells strongly adhered to a poly-l-lysine-coated surface, the response was suppressed, and the periodicity of the population-level oscillations was markedly lengthened. Our results suggest that cortical F-actin is dispensable for the basic low amplitude relay response but essential for its full amplification and that this enhanced response is necessary to establish high-frequency signalling centres. The observed F-actin dependence may prevent aggregation centres from establishing in microenvironments that are incompatible with cell migration.
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spelling pubmed-49380872016-07-15 Self-organization of chemoattractant waves in Dictyostelium depends on F-actin and cell–substrate adhesion Fukujin, Fumihito Nakajima, Akihiko Shimada, Nao Sawai, Satoshi J R Soc Interface Life Sciences–Physics interface In the social amoeba Dictyostelium discoideum, travelling waves of extracellular cyclic adenosine monophosphate (cAMP) self-organize in cell populations and direct aggregation of individual cells to form multicellular fruiting bodies. In contrast to the large body of studies that addressed how movement of cells is determined by spatial and temporal cues encoded in the dynamic cAMP gradients, how cell mechanics affect the formation of a self-generated chemoattractant field has received less attention. Here, we show, by live cell imaging analysis, that the periodicity of the synchronized cAMP waves increases in cells treated with the actin inhibitor latrunculin. Detail analysis of the extracellular cAMP-induced transients of cytosolic cAMP (cAMP relay response) in well-isolated cells demonstrated that their amplitude and duration were markedly reduced in latrunculin-treated cells. Similarly, in cells strongly adhered to a poly-l-lysine-coated surface, the response was suppressed, and the periodicity of the population-level oscillations was markedly lengthened. Our results suggest that cortical F-actin is dispensable for the basic low amplitude relay response but essential for its full amplification and that this enhanced response is necessary to establish high-frequency signalling centres. The observed F-actin dependence may prevent aggregation centres from establishing in microenvironments that are incompatible with cell migration. The Royal Society 2016-06 /pmc/articles/PMC4938087/ /pubmed/27358278 http://dx.doi.org/10.1098/rsif.2016.0233 Text en © 2016 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Life Sciences–Physics interface
Fukujin, Fumihito
Nakajima, Akihiko
Shimada, Nao
Sawai, Satoshi
Self-organization of chemoattractant waves in Dictyostelium depends on F-actin and cell–substrate adhesion
title Self-organization of chemoattractant waves in Dictyostelium depends on F-actin and cell–substrate adhesion
title_full Self-organization of chemoattractant waves in Dictyostelium depends on F-actin and cell–substrate adhesion
title_fullStr Self-organization of chemoattractant waves in Dictyostelium depends on F-actin and cell–substrate adhesion
title_full_unstemmed Self-organization of chemoattractant waves in Dictyostelium depends on F-actin and cell–substrate adhesion
title_short Self-organization of chemoattractant waves in Dictyostelium depends on F-actin and cell–substrate adhesion
title_sort self-organization of chemoattractant waves in dictyostelium depends on f-actin and cell–substrate adhesion
topic Life Sciences–Physics interface
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4938087/
https://www.ncbi.nlm.nih.gov/pubmed/27358278
http://dx.doi.org/10.1098/rsif.2016.0233
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