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Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development

Propagating waves of cAMP, periodically initiated in the aggregation centre, are known to guide the chemotactic aggregation of hundreds of thousands of starving individual Dictyostelium discoideum cells into multicellular aggregates. Propagating optical density waves, reflecting cell periodic moveme...

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Autores principales: Singer, Gail, Araki, Tsuyoshi, Weijer, Cornelis J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6478855/
https://www.ncbi.nlm.nih.gov/pubmed/31044164
http://dx.doi.org/10.1038/s42003-019-0371-0
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author Singer, Gail
Araki, Tsuyoshi
Weijer, Cornelis J.
author_facet Singer, Gail
Araki, Tsuyoshi
Weijer, Cornelis J.
author_sort Singer, Gail
collection PubMed
description Propagating waves of cAMP, periodically initiated in the aggregation centre, are known to guide the chemotactic aggregation of hundreds of thousands of starving individual Dictyostelium discoideum cells into multicellular aggregates. Propagating optical density waves, reflecting cell periodic movement, have previously been shown to exist in streaming aggregates, mounds and migrating slugs. Using a highly sensitive cAMP-FRET reporter, we have now been able to measure periodically propagating cAMP waves directly in these multicellular structures. In slugs cAMP waves are periodically initiated in the tip and propagate backward through the prespore zone. Altered cAMP signalling dynamics in mutants with developmental defects strongly support a key functional role for cAMP waves in multicellular Dictyostelium morphogenesis. These findings thus show that propagating cAMP not only control the initial aggregation process but continue to be the long range cell-cell communication mechanism guiding cell movement during multicellular Dictyostelium morphogenesis at the mound and slugs stages.
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spelling pubmed-64788552019-05-01 Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development Singer, Gail Araki, Tsuyoshi Weijer, Cornelis J. Commun Biol Article Propagating waves of cAMP, periodically initiated in the aggregation centre, are known to guide the chemotactic aggregation of hundreds of thousands of starving individual Dictyostelium discoideum cells into multicellular aggregates. Propagating optical density waves, reflecting cell periodic movement, have previously been shown to exist in streaming aggregates, mounds and migrating slugs. Using a highly sensitive cAMP-FRET reporter, we have now been able to measure periodically propagating cAMP waves directly in these multicellular structures. In slugs cAMP waves are periodically initiated in the tip and propagate backward through the prespore zone. Altered cAMP signalling dynamics in mutants with developmental defects strongly support a key functional role for cAMP waves in multicellular Dictyostelium morphogenesis. These findings thus show that propagating cAMP not only control the initial aggregation process but continue to be the long range cell-cell communication mechanism guiding cell movement during multicellular Dictyostelium morphogenesis at the mound and slugs stages. Nature Publishing Group UK 2019-04-23 /pmc/articles/PMC6478855/ /pubmed/31044164 http://dx.doi.org/10.1038/s42003-019-0371-0 Text en © The Author(s) 2019 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/.
spellingShingle Article
Singer, Gail
Araki, Tsuyoshi
Weijer, Cornelis J.
Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development
title Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development
title_full Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development
title_fullStr Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development
title_full_unstemmed Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development
title_short Oscillatory cAMP cell-cell signalling persists during multicellular Dictyostelium development
title_sort oscillatory camp cell-cell signalling persists during multicellular dictyostelium development
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6478855/
https://www.ncbi.nlm.nih.gov/pubmed/31044164
http://dx.doi.org/10.1038/s42003-019-0371-0
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