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Postprandial regulation of hepatic microRNAs predicted to target the insulin pathway in rainbow trout.

Mennigen JA, Panserat S, Larquier M, Plagnes-Juan E, Medale F, Seiliez I, Skiba-Cassy S - PLoS ONE (2012)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: UMR1067 Nutrition, Métabolisme, Aquaculture, Institut National de la Recherche Agronomique, Saint-Pée-sur-Nivelle, Pyrénées-Atlantiques, France.

ABSTRACT
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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Postprandial expression profiles of hepatic omy-miRNA involved predicted to be involved in glucose metabolism(A) and lipid metabolism (B). Means and S.E. of n = 6 samples per group, are shown. Data were analysed using a one-way ANOVA, followed by the Newman-Keuls post-hoc test. Different letters indicate a significant difference at p<0.05.
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pone-0038604-g002: Postprandial expression profiles of hepatic omy-miRNA involved predicted to be involved in glucose metabolism(A) and lipid metabolism (B). Means and S.E. of n = 6 samples per group, are shown. Data were analysed using a one-way ANOVA, followed by the Newman-Keuls post-hoc test. Different letters indicate a significant difference at p<0.05.

Mentions: Time had a significant effect on the expression of omy-miRNAs whose mammalian homologues are implicated in the regulation of the insulin signaling cascade, particularly with respect to the regulation of glucose metabolism (Fig. 2A–G). The expression of omy-miRNA-21 (df = 6; F = 4.54; p<0.01), omy-miRNA-22 (df = 6; F = 5.46; p<0.01), omy-miRNA-29a (df = 6; F = 4.35; p<0.01), omy-miRNA-103 (df = 6; F = 8.06; p<0.01), omy-miRNA-107 (df = 6; F = 5.59; p<0.01); omy-miRNA-143 (df = 6; F = 3.79; p<0.05) exhibited significant postprandial changes. A significant increase in expression of several of these miRNAs was observed at 4 h after refeeding when compared to other time points (Fig. 2B–G), the exceptions being omy-miRNA-103 and to some extent omy-miRNA-29a and omy-miRNA-107, which exhibited an additional second increase in expression after 24 h which was not significantly different from the elevated expression observed 4 h after the meal (Fig. 2D–E). No significant postprandial changes in gene expression were observed for omy-miRNA-126a (df = 6; F = 1.51; p>0.05). Of the miRNAs, whose mammalian homologues are primarily involved in lipid metabolism, the expression of omy-miRNA-33 (df = 6; F = 3.41; p<0.05) revealed an increased expression 4 h after the meal when compared to the time of the meal (Fig. 2H). Hepatic expression of the highly expressed omy-miRNA-122b (df = 6; F = 3.05; p<0.05), but not of omy-miRNA-122a (df = 6; F = 0.41; p>0.05), exhibited significant postprandial changes. A significantly higher expression of omy-miRNA-122b compared to the time of feeding was observed 4 h after refeeding (Fig. 2I).


Postprandial regulation of hepatic microRNAs predicted to target the insulin pathway in rainbow trout.

Mennigen JA, Panserat S, Larquier M, Plagnes-Juan E, Medale F, Seiliez I, Skiba-Cassy S - PLoS ONE (2012)

Postprandial expression profiles of hepatic omy-miRNA involved predicted to be involved in glucose metabolism(A) and lipid metabolism (B). Means and S.E. of n = 6 samples per group, are shown. Data were analysed using a one-way ANOVA, followed by the Newman-Keuls post-hoc test. Different letters indicate a significant difference at p<0.05.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3368902&req=5

pone-0038604-g002: Postprandial expression profiles of hepatic omy-miRNA involved predicted to be involved in glucose metabolism(A) and lipid metabolism (B). Means and S.E. of n = 6 samples per group, are shown. Data were analysed using a one-way ANOVA, followed by the Newman-Keuls post-hoc test. Different letters indicate a significant difference at p<0.05.
Mentions: Time had a significant effect on the expression of omy-miRNAs whose mammalian homologues are implicated in the regulation of the insulin signaling cascade, particularly with respect to the regulation of glucose metabolism (Fig. 2A–G). The expression of omy-miRNA-21 (df = 6; F = 4.54; p<0.01), omy-miRNA-22 (df = 6; F = 5.46; p<0.01), omy-miRNA-29a (df = 6; F = 4.35; p<0.01), omy-miRNA-103 (df = 6; F = 8.06; p<0.01), omy-miRNA-107 (df = 6; F = 5.59; p<0.01); omy-miRNA-143 (df = 6; F = 3.79; p<0.05) exhibited significant postprandial changes. A significant increase in expression of several of these miRNAs was observed at 4 h after refeeding when compared to other time points (Fig. 2B–G), the exceptions being omy-miRNA-103 and to some extent omy-miRNA-29a and omy-miRNA-107, which exhibited an additional second increase in expression after 24 h which was not significantly different from the elevated expression observed 4 h after the meal (Fig. 2D–E). No significant postprandial changes in gene expression were observed for omy-miRNA-126a (df = 6; F = 1.51; p>0.05). Of the miRNAs, whose mammalian homologues are primarily involved in lipid metabolism, the expression of omy-miRNA-33 (df = 6; F = 3.41; p<0.05) revealed an increased expression 4 h after the meal when compared to the time of the meal (Fig. 2H). Hepatic expression of the highly expressed omy-miRNA-122b (df = 6; F = 3.05; p<0.05), but not of omy-miRNA-122a (df = 6; F = 0.41; p>0.05), exhibited significant postprandial changes. A significantly higher expression of omy-miRNA-122b compared to the time of feeding was observed 4 h after refeeding (Fig. 2I).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: UMR1067 Nutrition, Métabolisme, Aquaculture, Institut National de la Recherche Agronomique, Saint-Pée-sur-Nivelle, Pyrénées-Atlantiques, France.

ABSTRACT
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.

Show MeSH