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Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism

Metabolic homeostasis is coordinated through a robust network of signaling pathways acting across all tissues. A key part of this network is insulin-like signaling, which is fundamental for surviving glucose stress. Here, we show that Caenorhabditis elegans fed excess dietary glucose reduce insulin-...

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Detalles Bibliográficos
Autores principales: Handley, Ava, Wu, Qiuli, Sherry, Tessa, Cornell, Rebecca, Pocock, Roger
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9162364/
https://www.ncbi.nlm.nih.gov/pubmed/35594303
http://dx.doi.org/10.1371/journal.pbio.3001655
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author Handley, Ava
Wu, Qiuli
Sherry, Tessa
Cornell, Rebecca
Pocock, Roger
author_facet Handley, Ava
Wu, Qiuli
Sherry, Tessa
Cornell, Rebecca
Pocock, Roger
author_sort Handley, Ava
collection PubMed
description Metabolic homeostasis is coordinated through a robust network of signaling pathways acting across all tissues. A key part of this network is insulin-like signaling, which is fundamental for surviving glucose stress. Here, we show that Caenorhabditis elegans fed excess dietary glucose reduce insulin-1 (INS-1) expression specifically in the BAG glutamatergic sensory neurons. We demonstrate that INS-1 expression in the BAG neurons is directly controlled by the transcription factor ETS-5, which is also down-regulated by glucose. We further find that INS-1 acts exclusively from the BAG neurons, and not other INS-1-expressing neurons, to systemically inhibit fat storage via the insulin-like receptor DAF-2. Together, these findings reveal an intertissue regulatory pathway where regulation of insulin expression in a specific neuron controls systemic metabolism in response to excess dietary glucose.
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spelling pubmed-91623642022-06-03 Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism Handley, Ava Wu, Qiuli Sherry, Tessa Cornell, Rebecca Pocock, Roger PLoS Biol Research Article Metabolic homeostasis is coordinated through a robust network of signaling pathways acting across all tissues. A key part of this network is insulin-like signaling, which is fundamental for surviving glucose stress. Here, we show that Caenorhabditis elegans fed excess dietary glucose reduce insulin-1 (INS-1) expression specifically in the BAG glutamatergic sensory neurons. We demonstrate that INS-1 expression in the BAG neurons is directly controlled by the transcription factor ETS-5, which is also down-regulated by glucose. We further find that INS-1 acts exclusively from the BAG neurons, and not other INS-1-expressing neurons, to systemically inhibit fat storage via the insulin-like receptor DAF-2. Together, these findings reveal an intertissue regulatory pathway where regulation of insulin expression in a specific neuron controls systemic metabolism in response to excess dietary glucose. Public Library of Science 2022-05-20 /pmc/articles/PMC9162364/ /pubmed/35594303 http://dx.doi.org/10.1371/journal.pbio.3001655 Text en © 2022 Handley et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Handley, Ava
Wu, Qiuli
Sherry, Tessa
Cornell, Rebecca
Pocock, Roger
Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism
title Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism
title_full Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism
title_fullStr Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism
title_full_unstemmed Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism
title_short Diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism
title_sort diet-responsive transcriptional regulation of insulin in a single neuron controls systemic metabolism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9162364/
https://www.ncbi.nlm.nih.gov/pubmed/35594303
http://dx.doi.org/10.1371/journal.pbio.3001655
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