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Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout

Rainbow trout are carnivorous fish and poor metabolizers of carbohydrates, which established this species as a model organism to study the comparative physiology of insulin. Following the recent characterisation of key roles of several miRNAs in the insulin action on hepatic intermediary metabolism...

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Autores principales: Mennigen, Jan A., Panserat, Stéphane, Larquier, Mélanie, Plagnes-Juan, Elisabeth, Medale, Françoise, Seiliez, Iban, Skiba-Cassy, Sandrine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3368902/
https://www.ncbi.nlm.nih.gov/pubmed/22701681
http://dx.doi.org/10.1371/journal.pone.0038604
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author Mennigen, Jan A.
Panserat, Stéphane
Larquier, Mélanie
Plagnes-Juan, Elisabeth
Medale, Françoise
Seiliez, Iban
Skiba-Cassy, Sandrine
author_facet Mennigen, Jan A.
Panserat, Stéphane
Larquier, Mélanie
Plagnes-Juan, Elisabeth
Medale, Françoise
Seiliez, Iban
Skiba-Cassy, Sandrine
author_sort Mennigen, Jan A.
collection PubMed
description Rainbow trout are carnivorous fish and poor metabolizers of carbohydrates, which established this species as a model organism to study the comparative physiology of insulin. Following the recent characterisation of key roles of several miRNAs in the insulin action on hepatic intermediary metabolism in mammalian models, we investigated the hypothesis that hepatic miRNA expression is postprandially regulated in the rainbow trout and temporally coordinated in the context of insulin-mediated regulation of metabolic gene expression in the liver. To address this hypothesis, we used a time-course experiment in which rainbow trout were fed a commercial diet after short-term fasting. We investigated hepatic miRNA expression, activation of the insulin pathway, and insulin regulated metabolic target genes at several time points. Several miRNAs which negatively regulate hepatic insulin signaling in mammalian model organisms were transiently increased 4 h after the meal, consistent with a potential role in acute postprandial negative feed-back regulation of the insulin pathway and attenuation of gluconeogenic gene expression. We equally observed a transient increase in omy- miRNA-33 and omy-miRNA-122b 4 h after feeding, whose homologues have potent lipogenic roles in the liver of mammalian model systems. A concurrent increase in the activity of the hepatic insulin signaling pathway and the expression of lipogenic genes (srebp1c, fas, acly) was equally observed, while lipolytic gene expression (cpt1a and cpt1b) decreased significantly 4 h after the meal. This suggests lipogenic roles of omy-miRNA-33 and omy-miRNA-122b may be conserved between rainbow trout and mammals and that these miRNAs may furthermore contribute to acute postprandial regulation of de novo hepatic lipid synthesis in rainbow trout. These findings provide a framework for future research of miRNA regulation of hepatic metabolism in trout and will help to further elucidate the metabolic phenotype of rainbow trout.
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spelling pubmed-33689022012-06-13 Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout Mennigen, Jan A. Panserat, Stéphane Larquier, Mélanie Plagnes-Juan, Elisabeth Medale, Françoise Seiliez, Iban Skiba-Cassy, Sandrine PLoS One Research Article Rainbow trout are carnivorous fish and poor metabolizers of carbohydrates, which established this species as a model organism to study the comparative physiology of insulin. Following the recent characterisation of key roles of several miRNAs in the insulin action on hepatic intermediary metabolism in mammalian models, we investigated the hypothesis that hepatic miRNA expression is postprandially regulated in the rainbow trout and temporally coordinated in the context of insulin-mediated regulation of metabolic gene expression in the liver. To address this hypothesis, we used a time-course experiment in which rainbow trout were fed a commercial diet after short-term fasting. We investigated hepatic miRNA expression, activation of the insulin pathway, and insulin regulated metabolic target genes at several time points. Several miRNAs which negatively regulate hepatic insulin signaling in mammalian model organisms were transiently increased 4 h after the meal, consistent with a potential role in acute postprandial negative feed-back regulation of the insulin pathway and attenuation of gluconeogenic gene expression. We equally observed a transient increase in omy- miRNA-33 and omy-miRNA-122b 4 h after feeding, whose homologues have potent lipogenic roles in the liver of mammalian model systems. A concurrent increase in the activity of the hepatic insulin signaling pathway and the expression of lipogenic genes (srebp1c, fas, acly) was equally observed, while lipolytic gene expression (cpt1a and cpt1b) decreased significantly 4 h after the meal. This suggests lipogenic roles of omy-miRNA-33 and omy-miRNA-122b may be conserved between rainbow trout and mammals and that these miRNAs may furthermore contribute to acute postprandial regulation of de novo hepatic lipid synthesis in rainbow trout. These findings provide a framework for future research of miRNA regulation of hepatic metabolism in trout and will help to further elucidate the metabolic phenotype of rainbow trout. Public Library of Science 2012-06-06 /pmc/articles/PMC3368902/ /pubmed/22701681 http://dx.doi.org/10.1371/journal.pone.0038604 Text en Mennigen 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
Mennigen, Jan A.
Panserat, Stéphane
Larquier, Mélanie
Plagnes-Juan, Elisabeth
Medale, Françoise
Seiliez, Iban
Skiba-Cassy, Sandrine
Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout
title Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout
title_full Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout
title_fullStr Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout
title_full_unstemmed Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout
title_short Postprandial Regulation of Hepatic MicroRNAs Predicted to Target the Insulin Pathway in Rainbow Trout
title_sort postprandial regulation of hepatic micrornas predicted to target the insulin pathway in rainbow trout
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3368902/
https://www.ncbi.nlm.nih.gov/pubmed/22701681
http://dx.doi.org/10.1371/journal.pone.0038604
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