A gene-expression-based neural code for food abundance that modulates lifespan

How the nervous system internally represents environmental food availability is poorly understood. Here, we show that quantitative information about food abundance is encoded by combinatorial neuron-specific gene-expression of conserved TGFβ and serotonin pathway components in Caenorhabditis elegans...

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Main Authors: Eugeni V Entchev, Dhaval S Patel, Mei Zhan, Andrew J Steele, Hang Lu, QueeLim Ch'ng
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/06259
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spelling doaj-3830d9d787b6426fbf16e47a6667c72e2021-05-04T23:47:32ZengeLife Sciences Publications LtdeLife2050-084X2015-05-01410.7554/eLife.06259A gene-expression-based neural code for food abundance that modulates lifespanEugeni V Entchev0Dhaval S Patel1Mei Zhan2Andrew J Steele3Hang Lu4QueeLim Ch'ng5MRC Centre for Developmental Neurobiology, King's College London, London, United KingdomMRC Centre for Developmental Neurobiology, King's College London, London, United KingdomInterdisciplinary Bioengineering Graduate Program, Georgia Institute of Technology, Atlanta, United States; Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology, Atlanta, United StatesMRC Centre for Developmental Neurobiology, King's College London, London, United KingdomInterdisciplinary Bioengineering Graduate Program, Georgia Institute of Technology, Atlanta, United States; Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology, Atlanta, United States; School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, United StatesMRC Centre for Developmental Neurobiology, King's College London, London, United KingdomHow the nervous system internally represents environmental food availability is poorly understood. Here, we show that quantitative information about food abundance is encoded by combinatorial neuron-specific gene-expression of conserved TGFβ and serotonin pathway components in Caenorhabditis elegans. Crosstalk and auto-regulation between these pathways alters the shape, dynamic range, and population variance of the gene-expression responses of daf-7 (TGFβ) and tph-1 (tryptophan hydroxylase) to food availability. These intricate regulatory features provide distinct mechanisms for TGFβ and serotonin signaling to tune the accuracy of this multi-neuron code: daf-7 primarily regulates gene-expression variability, while tph-1 primarily regulates the dynamic range of gene-expression responses. This code is functional because daf-7 and tph-1 mutations bidirectionally attenuate food level-dependent changes in lifespan. Our results reveal a neural code for food abundance and demonstrate that gene expression serves as an additional layer of information processing in the nervous system to control long-term physiology.https://elifesciences.org/articles/06259neural codedietary restrictionneural circuitgene regulationexpression variability
collection DOAJ
language English
format Article
sources DOAJ
author Eugeni V Entchev
Dhaval S Patel
Mei Zhan
Andrew J Steele
Hang Lu
QueeLim Ch'ng
spellingShingle Eugeni V Entchev
Dhaval S Patel
Mei Zhan
Andrew J Steele
Hang Lu
QueeLim Ch'ng
A gene-expression-based neural code for food abundance that modulates lifespan
eLife
neural code
dietary restriction
neural circuit
gene regulation
expression variability
author_facet Eugeni V Entchev
Dhaval S Patel
Mei Zhan
Andrew J Steele
Hang Lu
QueeLim Ch'ng
author_sort Eugeni V Entchev
title A gene-expression-based neural code for food abundance that modulates lifespan
title_short A gene-expression-based neural code for food abundance that modulates lifespan
title_full A gene-expression-based neural code for food abundance that modulates lifespan
title_fullStr A gene-expression-based neural code for food abundance that modulates lifespan
title_full_unstemmed A gene-expression-based neural code for food abundance that modulates lifespan
title_sort gene-expression-based neural code for food abundance that modulates lifespan
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2015-05-01
description How the nervous system internally represents environmental food availability is poorly understood. Here, we show that quantitative information about food abundance is encoded by combinatorial neuron-specific gene-expression of conserved TGFβ and serotonin pathway components in Caenorhabditis elegans. Crosstalk and auto-regulation between these pathways alters the shape, dynamic range, and population variance of the gene-expression responses of daf-7 (TGFβ) and tph-1 (tryptophan hydroxylase) to food availability. These intricate regulatory features provide distinct mechanisms for TGFβ and serotonin signaling to tune the accuracy of this multi-neuron code: daf-7 primarily regulates gene-expression variability, while tph-1 primarily regulates the dynamic range of gene-expression responses. This code is functional because daf-7 and tph-1 mutations bidirectionally attenuate food level-dependent changes in lifespan. Our results reveal a neural code for food abundance and demonstrate that gene expression serves as an additional layer of information processing in the nervous system to control long-term physiology.
topic neural code
dietary restriction
neural circuit
gene regulation
expression variability
url https://elifesciences.org/articles/06259
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