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Tension and Robustness in Multitasking Cellular Networks

Cellular networks multitask by exhibiting distinct, context-dependent dynamics. However, network states (parameters) that generate a particular dynamic are often sub-optimal for others, defining a source of “tension” between them. Though multitasking is pervasive, it is not clear where tension arise...

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Detalles Bibliográficos
Autores principales: Wong, Jeffrey V., Li, Bochong, You, Lingchong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3343128/
https://www.ncbi.nlm.nih.gov/pubmed/22577355
http://dx.doi.org/10.1371/journal.pcbi.1002491
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author Wong, Jeffrey V.
Li, Bochong
You, Lingchong
author_facet Wong, Jeffrey V.
Li, Bochong
You, Lingchong
author_sort Wong, Jeffrey V.
collection PubMed
description Cellular networks multitask by exhibiting distinct, context-dependent dynamics. However, network states (parameters) that generate a particular dynamic are often sub-optimal for others, defining a source of “tension” between them. Though multitasking is pervasive, it is not clear where tension arises, what consequences it has, and how it is resolved. We developed a generic computational framework to examine the source and consequences of tension between pairs of dynamics exhibited by the well-studied RB-E2F switch regulating cell cycle entry. We found that tension arose from task-dependent shifts in parameters associated with network modules. Although parameter sets common to distinct dynamics did exist, tension reduced both their accessibility and resilience to perturbation, indicating a trade-off between “one-size-fits-all” solutions and robustness. With high tension, robustness can be preserved by dynamic shifting of modules, enabling the network to toggle between tasks, and by increasing network complexity, in this case by gene duplication. We propose that tension is a general constraint on the architecture and operation of multitasking biological networks. To this end, our work provides a framework to quantify the extent of tension between any network dynamics and how it affects network robustness. Such analysis would suggest new ways to interfere with network elements to elucidate the design principles of cellular networks.
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spelling pubmed-33431282012-05-10 Tension and Robustness in Multitasking Cellular Networks Wong, Jeffrey V. Li, Bochong You, Lingchong PLoS Comput Biol Research Article Cellular networks multitask by exhibiting distinct, context-dependent dynamics. However, network states (parameters) that generate a particular dynamic are often sub-optimal for others, defining a source of “tension” between them. Though multitasking is pervasive, it is not clear where tension arises, what consequences it has, and how it is resolved. We developed a generic computational framework to examine the source and consequences of tension between pairs of dynamics exhibited by the well-studied RB-E2F switch regulating cell cycle entry. We found that tension arose from task-dependent shifts in parameters associated with network modules. Although parameter sets common to distinct dynamics did exist, tension reduced both their accessibility and resilience to perturbation, indicating a trade-off between “one-size-fits-all” solutions and robustness. With high tension, robustness can be preserved by dynamic shifting of modules, enabling the network to toggle between tasks, and by increasing network complexity, in this case by gene duplication. We propose that tension is a general constraint on the architecture and operation of multitasking biological networks. To this end, our work provides a framework to quantify the extent of tension between any network dynamics and how it affects network robustness. Such analysis would suggest new ways to interfere with network elements to elucidate the design principles of cellular networks. Public Library of Science 2012-04-26 /pmc/articles/PMC3343128/ /pubmed/22577355 http://dx.doi.org/10.1371/journal.pcbi.1002491 Text en Wong et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Wong, Jeffrey V.
Li, Bochong
You, Lingchong
Tension and Robustness in Multitasking Cellular Networks
title Tension and Robustness in Multitasking Cellular Networks
title_full Tension and Robustness in Multitasking Cellular Networks
title_fullStr Tension and Robustness in Multitasking Cellular Networks
title_full_unstemmed Tension and Robustness in Multitasking Cellular Networks
title_short Tension and Robustness in Multitasking Cellular Networks
title_sort tension and robustness in multitasking cellular networks
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3343128/
https://www.ncbi.nlm.nih.gov/pubmed/22577355
http://dx.doi.org/10.1371/journal.pcbi.1002491
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