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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 of genes involved in lipogenesis (A,B) and lipolysis (C) 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-g005: Postprandial expression of genes involved in lipogenesis (A,B) and lipolysis (C) 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: The expression of genes involved in hepatic lipid metabolism increased postprandially for lipogenic genes (Fig. 5A,B), including srebp1c (df = 6; F = 7.13; p<0.01), fas (df = 6; F = 4.41; p<0.01), and acly (df = 6; F = 3.74; p<0.01), but not g6pdh (df = 6; F = 1.13; p = 0.37). Post-hoc analysis reveals significant increases in the expression of srebp1c between 2–4 h after refeeding compared to expression at feeding time, with a second, smaller increase in expression after 16 h that is not significantly different from the expression observed between 2 h and 4 h (Fig. 5A). Expression of fas increases significantly after 4 h and exhibits a second peak in expression between 16–24 h that is not significantly different from the expression observed 4 h after refeeding (Fig. 5B). The postprandial expression of acly is significantly increased 24 h after refeeding; however, this increase is preceded by a smaller, first peak in expression between 2–4 h that is not significantly different from the expression observed 24 h after refeeding. The expression of the lipolytic genes (Fig. 5C), cpt1a (df = 6; F = 5.30; p<0.01) and cpt1b (df = 6; F = 4.11; p<0.01), exhibited postprandial decreases in expression. Both isoforms, cpt1a, and cpt1b, were significantly decreased 4 h and 16 h after refeeding compared to the expression level at the time of refeeding (Fig. 5C).


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 of genes involved in lipogenesis (A,B) and lipolysis (C) 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-g005: Postprandial expression of genes involved in lipogenesis (A,B) and lipolysis (C) 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: The expression of genes involved in hepatic lipid metabolism increased postprandially for lipogenic genes (Fig. 5A,B), including srebp1c (df = 6; F = 7.13; p<0.01), fas (df = 6; F = 4.41; p<0.01), and acly (df = 6; F = 3.74; p<0.01), but not g6pdh (df = 6; F = 1.13; p = 0.37). Post-hoc analysis reveals significant increases in the expression of srebp1c between 2–4 h after refeeding compared to expression at feeding time, with a second, smaller increase in expression after 16 h that is not significantly different from the expression observed between 2 h and 4 h (Fig. 5A). Expression of fas increases significantly after 4 h and exhibits a second peak in expression between 16–24 h that is not significantly different from the expression observed 4 h after refeeding (Fig. 5B). The postprandial expression of acly is significantly increased 24 h after refeeding; however, this increase is preceded by a smaller, first peak in expression between 2–4 h that is not significantly different from the expression observed 24 h after refeeding. The expression of the lipolytic genes (Fig. 5C), cpt1a (df = 6; F = 5.30; p<0.01) and cpt1b (df = 6; F = 4.11; p<0.01), exhibited postprandial decreases in expression. Both isoforms, cpt1a, and cpt1b, were significantly decreased 4 h and 16 h after refeeding compared to the expression level at the time of refeeding (Fig. 5C).

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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