Cargando…

Small-world connectivity dictates collective endothelial cell signaling

Every blood vessel is lined by a single layer of highly specialized, yet adaptable and multifunctional endothelial cells. These cells, the endothelium, control vascular contractility, hemostasis, and inflammation and regulate the exchange of oxygen, nutrients, and waste products between circulating...

Descripción completa

Detalles Bibliográficos
Autores principales: Lee, Matthew D., Buckley, Charlotte, Zhang, Xun, Louhivuori, Lauri, Uhlén, Per, Wilson, Calum, McCarron, John G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9170162/
https://www.ncbi.nlm.nih.gov/pubmed/35482920
http://dx.doi.org/10.1073/pnas.2118927119
_version_ 1784721354531012608
author Lee, Matthew D.
Buckley, Charlotte
Zhang, Xun
Louhivuori, Lauri
Uhlén, Per
Wilson, Calum
McCarron, John G.
author_facet Lee, Matthew D.
Buckley, Charlotte
Zhang, Xun
Louhivuori, Lauri
Uhlén, Per
Wilson, Calum
McCarron, John G.
author_sort Lee, Matthew D.
collection PubMed
description Every blood vessel is lined by a single layer of highly specialized, yet adaptable and multifunctional endothelial cells. These cells, the endothelium, control vascular contractility, hemostasis, and inflammation and regulate the exchange of oxygen, nutrients, and waste products between circulating blood and tissue. To control each function, the endothelium processes endlessly arriving requests from multiple sources using separate clusters of cells specialized to detect specific stimuli. A well-developed but poorly understood communication system operates between cells to integrate multiple lines of information and coordinate endothelial responses. Here, the nature of the communication network has been addressed using single-cell Ca(2+) imaging across thousands of endothelial cells in intact blood vessels. Cell activities were cross-correlated and compared to a stochastic model to determine network connections. Highly correlated Ca(2+) activities occurred in scattered cell clusters, and network communication links between them exhibited unexpectedly short path lengths. The number of connections between cells (degree distribution) followed a power-law relationship revealing a scale-free network topology. The path length and degree distribution revealed an endothelial network with a “small-world” configuration. The small-world configuration confers particularly dynamic endothelial properties including high signal-propagation speed, stability, and a high degree of synchronizability. Local activation of small clusters of cells revealed that the short path lengths and rapid signal transmission were achieved by shortcuts via connecting extensions to nonlocal cells. These findings reveal that the endothelial network design is effective for local and global efficiency in the interaction of the cells and rapid and robust communication between endothelial cells in order to efficiently control cardiovascular activity.
format Online
Article
Text
id pubmed-9170162
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-91701622022-06-07 Small-world connectivity dictates collective endothelial cell signaling Lee, Matthew D. Buckley, Charlotte Zhang, Xun Louhivuori, Lauri Uhlén, Per Wilson, Calum McCarron, John G. Proc Natl Acad Sci U S A Biological Sciences Every blood vessel is lined by a single layer of highly specialized, yet adaptable and multifunctional endothelial cells. These cells, the endothelium, control vascular contractility, hemostasis, and inflammation and regulate the exchange of oxygen, nutrients, and waste products between circulating blood and tissue. To control each function, the endothelium processes endlessly arriving requests from multiple sources using separate clusters of cells specialized to detect specific stimuli. A well-developed but poorly understood communication system operates between cells to integrate multiple lines of information and coordinate endothelial responses. Here, the nature of the communication network has been addressed using single-cell Ca(2+) imaging across thousands of endothelial cells in intact blood vessels. Cell activities were cross-correlated and compared to a stochastic model to determine network connections. Highly correlated Ca(2+) activities occurred in scattered cell clusters, and network communication links between them exhibited unexpectedly short path lengths. The number of connections between cells (degree distribution) followed a power-law relationship revealing a scale-free network topology. The path length and degree distribution revealed an endothelial network with a “small-world” configuration. The small-world configuration confers particularly dynamic endothelial properties including high signal-propagation speed, stability, and a high degree of synchronizability. Local activation of small clusters of cells revealed that the short path lengths and rapid signal transmission were achieved by shortcuts via connecting extensions to nonlocal cells. These findings reveal that the endothelial network design is effective for local and global efficiency in the interaction of the cells and rapid and robust communication between endothelial cells in order to efficiently control cardiovascular activity. National Academy of Sciences 2022-04-28 2022-05-03 /pmc/articles/PMC9170162/ /pubmed/35482920 http://dx.doi.org/10.1073/pnas.2118927119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Lee, Matthew D.
Buckley, Charlotte
Zhang, Xun
Louhivuori, Lauri
Uhlén, Per
Wilson, Calum
McCarron, John G.
Small-world connectivity dictates collective endothelial cell signaling
title Small-world connectivity dictates collective endothelial cell signaling
title_full Small-world connectivity dictates collective endothelial cell signaling
title_fullStr Small-world connectivity dictates collective endothelial cell signaling
title_full_unstemmed Small-world connectivity dictates collective endothelial cell signaling
title_short Small-world connectivity dictates collective endothelial cell signaling
title_sort small-world connectivity dictates collective endothelial cell signaling
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9170162/
https://www.ncbi.nlm.nih.gov/pubmed/35482920
http://dx.doi.org/10.1073/pnas.2118927119
work_keys_str_mv AT leematthewd smallworldconnectivitydictatescollectiveendothelialcellsignaling
AT buckleycharlotte smallworldconnectivitydictatescollectiveendothelialcellsignaling
AT zhangxun smallworldconnectivitydictatescollectiveendothelialcellsignaling
AT louhivuorilauri smallworldconnectivitydictatescollectiveendothelialcellsignaling
AT uhlenper smallworldconnectivitydictatescollectiveendothelialcellsignaling
AT wilsoncalum smallworldconnectivitydictatescollectiveendothelialcellsignaling
AT mccarronjohng smallworldconnectivitydictatescollectiveendothelialcellsignaling