Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex

Abstract The Rho family GTPases are molecular switches that regulate cytoskeletal dynamics and cell movement through a complex spatiotemporal organization of their activity. In Patiria miniata (starfish) oocytes under in vitro experimental conditions (with overexpressed Ect2, induced expression of Δ...

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Autores principales:	Siarhei Hladyshau, Mary Kho, Shuyi Nie, Denis Tsygankov
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/ac93049fb393468f99e8ce7da81df15b
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spelling	oai:doaj.org-article:ac93049fb393468f99e8ce7da81df15b2021-12-02T17:37:40ZSpatiotemporal development of coexisting wave domains of Rho activity in the cell cortex10.1038/s41598-021-99029-x2045-2322https://doaj.org/article/ac93049fb393468f99e8ce7da81df15b2021-09-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-99029-xhttps://doaj.org/toc/2045-2322Abstract The Rho family GTPases are molecular switches that regulate cytoskeletal dynamics and cell movement through a complex spatiotemporal organization of their activity. In Patiria miniata (starfish) oocytes under in vitro experimental conditions (with overexpressed Ect2, induced expression of Δ90 cyclin B, and roscovitine treatment), such activity generates multiple co-existing regions of coherent propagation of actin waves. Here we use computational modeling to investigate the development and properties of such wave domains. The model reveals that the formation of wave domains requires a balance between the activation and inhibition in the Rho signaling motif. Intriguingly, the development of the wave domains is preceded by a stage of low-activity quasi-static patterns, which may not be readily observed in experiments. Spatiotemporal patterns of this stage and the different paths of their destabilization define the behavior of the system in the later high-activity (observable) stage. Accounting for a strong intrinsic noise allowed us to achieve good quantitative agreement between simulated dynamics in different parameter regimes of the model and different wave dynamics in Patiria miniata and wild type Xenopus laevis (frog) data. For quantitative comparison of simulated and experimental results, we developed an automated method of wave domain detection, which revealed a sharp reversal in the process of pattern formation in starfish oocytes. Overall, our findings provide an insight into spatiotemporal regulation of complex and diverse but still computationally reproducible cell-level actin dynamics.Siarhei HladyshauMary KhoShuyi NieDenis TsygankovNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-19 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Siarhei Hladyshau Mary Kho Shuyi Nie Denis Tsygankov Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex
description	Abstract The Rho family GTPases are molecular switches that regulate cytoskeletal dynamics and cell movement through a complex spatiotemporal organization of their activity. In Patiria miniata (starfish) oocytes under in vitro experimental conditions (with overexpressed Ect2, induced expression of Δ90 cyclin B, and roscovitine treatment), such activity generates multiple co-existing regions of coherent propagation of actin waves. Here we use computational modeling to investigate the development and properties of such wave domains. The model reveals that the formation of wave domains requires a balance between the activation and inhibition in the Rho signaling motif. Intriguingly, the development of the wave domains is preceded by a stage of low-activity quasi-static patterns, which may not be readily observed in experiments. Spatiotemporal patterns of this stage and the different paths of their destabilization define the behavior of the system in the later high-activity (observable) stage. Accounting for a strong intrinsic noise allowed us to achieve good quantitative agreement between simulated dynamics in different parameter regimes of the model and different wave dynamics in Patiria miniata and wild type Xenopus laevis (frog) data. For quantitative comparison of simulated and experimental results, we developed an automated method of wave domain detection, which revealed a sharp reversal in the process of pattern formation in starfish oocytes. Overall, our findings provide an insight into spatiotemporal regulation of complex and diverse but still computationally reproducible cell-level actin dynamics.
format	article
author	Siarhei Hladyshau Mary Kho Shuyi Nie Denis Tsygankov
author_facet	Siarhei Hladyshau Mary Kho Shuyi Nie Denis Tsygankov
author_sort	Siarhei Hladyshau
title	Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex
title_short	Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex
title_full	Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex
title_fullStr	Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex
title_full_unstemmed	Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex
title_sort	spatiotemporal development of coexisting wave domains of rho activity in the cell cortex
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/ac93049fb393468f99e8ce7da81df15b
work_keys_str_mv	AT siarheihladyshau spatiotemporaldevelopmentofcoexistingwavedomainsofrhoactivityinthecellcortex AT marykho spatiotemporaldevelopmentofcoexistingwavedomainsofrhoactivityinthecellcortex AT shuyinie spatiotemporaldevelopmentofcoexistingwavedomainsofrhoactivityinthecellcortex AT denistsygankov spatiotemporaldevelopmentofcoexistingwavedomainsofrhoactivityinthecellcortex
_version_	1718379901506027520

Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex

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