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Modulation of transcription factor dynamics allows versatile information transmission

Cells detect changes in their environment and generate responses, often involving changes in gene expression. In this paper we use information theory and a simple transcription model to analyze whether the resulting gene expression serves to identify extracellular stimuli and assess their intensity...

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Autores principales: Givré, Alan, Colman-Lerner, Alejandro, Ponce Dawson, Silvina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9929046/
https://www.ncbi.nlm.nih.gov/pubmed/36788258
http://dx.doi.org/10.1038/s41598-023-29539-3
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author Givré, Alan
Colman-Lerner, Alejandro
Ponce Dawson, Silvina
author_facet Givré, Alan
Colman-Lerner, Alejandro
Ponce Dawson, Silvina
author_sort Givré, Alan
collection PubMed
description Cells detect changes in their environment and generate responses, often involving changes in gene expression. In this paper we use information theory and a simple transcription model to analyze whether the resulting gene expression serves to identify extracellular stimuli and assess their intensity when they are encoded in the amplitude, duration or frequency of pulses of a transcription factor’s nuclear concentration (or activation state). We find, for all cases, that about three ranges of input strengths can be distinguished and that maximum information transmission occurs for fast and high activation threshold promoters. The three input modulation modes differ in the sensitivity to changes in the promoters parameters. Frequency modulation is the most sensitive and duration modulation, the least. This is key for signal identification: there are promoter parameters that yield a relatively high information transmission for duration or amplitude modulation and a much smaller value for frequency modulation. The reverse situation cannot be found with a single promoter transcription model. Thus, pulses of transcription factors can selectively activate the “frequency-tuned” promoter while prolonged nuclear accumulation would activate promoters of all three modes simultaneously. Frequency modulation is therefore highly selective and better suited than the other encoding modes for signal identification without requiring other mediators of the transduction process.
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spelling pubmed-99290462023-02-16 Modulation of transcription factor dynamics allows versatile information transmission Givré, Alan Colman-Lerner, Alejandro Ponce Dawson, Silvina Sci Rep Article Cells detect changes in their environment and generate responses, often involving changes in gene expression. In this paper we use information theory and a simple transcription model to analyze whether the resulting gene expression serves to identify extracellular stimuli and assess their intensity when they are encoded in the amplitude, duration or frequency of pulses of a transcription factor’s nuclear concentration (or activation state). We find, for all cases, that about three ranges of input strengths can be distinguished and that maximum information transmission occurs for fast and high activation threshold promoters. The three input modulation modes differ in the sensitivity to changes in the promoters parameters. Frequency modulation is the most sensitive and duration modulation, the least. This is key for signal identification: there are promoter parameters that yield a relatively high information transmission for duration or amplitude modulation and a much smaller value for frequency modulation. The reverse situation cannot be found with a single promoter transcription model. Thus, pulses of transcription factors can selectively activate the “frequency-tuned” promoter while prolonged nuclear accumulation would activate promoters of all three modes simultaneously. Frequency modulation is therefore highly selective and better suited than the other encoding modes for signal identification without requiring other mediators of the transduction process. Nature Publishing Group UK 2023-02-14 /pmc/articles/PMC9929046/ /pubmed/36788258 http://dx.doi.org/10.1038/s41598-023-29539-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Givré, Alan
Colman-Lerner, Alejandro
Ponce Dawson, Silvina
Modulation of transcription factor dynamics allows versatile information transmission
title Modulation of transcription factor dynamics allows versatile information transmission
title_full Modulation of transcription factor dynamics allows versatile information transmission
title_fullStr Modulation of transcription factor dynamics allows versatile information transmission
title_full_unstemmed Modulation of transcription factor dynamics allows versatile information transmission
title_short Modulation of transcription factor dynamics allows versatile information transmission
title_sort modulation of transcription factor dynamics allows versatile information transmission
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9929046/
https://www.ncbi.nlm.nih.gov/pubmed/36788258
http://dx.doi.org/10.1038/s41598-023-29539-3
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