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Cellular information dynamics through transmembrane flow of ions

We propose cells generate large transmembrane ion gradients to form information circuits that detect, process, and respond to environmental perturbations or signals. In this model, the specialized gates of transmembrane ion channels function as information detectors that communicate to the cell thro...

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Detalles Bibliográficos
Autores principales: Gatenby, Robert A., Frieden, B. Roy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5678125/
https://www.ncbi.nlm.nih.gov/pubmed/29118414
http://dx.doi.org/10.1038/s41598-017-15182-2
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author Gatenby, Robert A.
Frieden, B. Roy
author_facet Gatenby, Robert A.
Frieden, B. Roy
author_sort Gatenby, Robert A.
collection PubMed
description We propose cells generate large transmembrane ion gradients to form information circuits that detect, process, and respond to environmental perturbations or signals. In this model, the specialized gates of transmembrane ion channels function as information detectors that communicate to the cell through rapid and (usually) local pulses of ions. Information in the ion “puffs” is received and processed by the cell through resulting changes in charge density and/or mobile cation (and/or anion) concentrations alter the localization and function of peripheral membrane proteins. The subsequent changes in protein binding to the membrane or activation of K(+), Ca(2+) or Mg(2+)-dependent enzymes then constitute a cellular response to the perturbation. To test this hypothesis we analyzed ion-based signal transmission as a communication channel operating with coded inputs and decoded outputs. By minimizing the Kullback-Leibler cross entropy [Formula: see text] between concentrations of the ion species inside [Formula: see text] and outside [Formula: see text] the cell membrane, we find signal transmission through transmembrane ion flow forms an optimal Shannon information channel that minimizes information loss and maximizes transmission speed. We demonstrate the ion dynamics in neuronal action potentials described by Hodgkin and Huxley (including the equations themselves) represent a special case of these general information principles.
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spelling pubmed-56781252017-11-17 Cellular information dynamics through transmembrane flow of ions Gatenby, Robert A. Frieden, B. Roy Sci Rep Article We propose cells generate large transmembrane ion gradients to form information circuits that detect, process, and respond to environmental perturbations or signals. In this model, the specialized gates of transmembrane ion channels function as information detectors that communicate to the cell through rapid and (usually) local pulses of ions. Information in the ion “puffs” is received and processed by the cell through resulting changes in charge density and/or mobile cation (and/or anion) concentrations alter the localization and function of peripheral membrane proteins. The subsequent changes in protein binding to the membrane or activation of K(+), Ca(2+) or Mg(2+)-dependent enzymes then constitute a cellular response to the perturbation. To test this hypothesis we analyzed ion-based signal transmission as a communication channel operating with coded inputs and decoded outputs. By minimizing the Kullback-Leibler cross entropy [Formula: see text] between concentrations of the ion species inside [Formula: see text] and outside [Formula: see text] the cell membrane, we find signal transmission through transmembrane ion flow forms an optimal Shannon information channel that minimizes information loss and maximizes transmission speed. We demonstrate the ion dynamics in neuronal action potentials described by Hodgkin and Huxley (including the equations themselves) represent a special case of these general information principles. Nature Publishing Group UK 2017-11-08 /pmc/articles/PMC5678125/ /pubmed/29118414 http://dx.doi.org/10.1038/s41598-017-15182-2 Text en © The Author(s) 2017 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
Gatenby, Robert A.
Frieden, B. Roy
Cellular information dynamics through transmembrane flow of ions
title Cellular information dynamics through transmembrane flow of ions
title_full Cellular information dynamics through transmembrane flow of ions
title_fullStr Cellular information dynamics through transmembrane flow of ions
title_full_unstemmed Cellular information dynamics through transmembrane flow of ions
title_short Cellular information dynamics through transmembrane flow of ions
title_sort cellular information dynamics through transmembrane flow of ions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5678125/
https://www.ncbi.nlm.nih.gov/pubmed/29118414
http://dx.doi.org/10.1038/s41598-017-15182-2
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