Glucose overload in yolk has little effects on the long term modulation of carbohydrate metabolic genes in zebrafish (Danio rerio)

Abstract

Some fish show a low metabolic ability to use dietary carbohydrates. The use of early nutritional stimuli to program metabolic pathways in fish is ill defined. Therefore, studies were undertaken with zebrafish to assess the effect of high glucose levels during the embryonic stage as a lifelong modulator of genes involved in carbohydrate metabolism. Genes related to carbohydrate metabolism were expressed at low levels at 0.2 and 1 day post-fertilization (dpf). However, from 4 dpf onwards there was a significant increase on expression of all genes, suggesting that all analysed pathways were active. By microinjection, we successfully enriched zebrafish egg yolk with glucose (a 43-fold increase of basal levels). Acute effects of glucose injection on gene expression were assessed in larvae up to 10 dpf, and the programming concept was evaluated in juveniles (41 dpf) challenged with a hyperglucidic diet. At 4 dpf, larvae from glucose-enriched eggs showed a downregulation of several genes related to glycolysis, glycogenolysis, lipogenesis and carbohydrate digestion in comparison with control (saline-injected) embryos. This inhibitory regulation was suppressed after 10 dpf. At the juvenile stage, and upon switching from a low to a high digestible carbohydrate diet, early glucose enrichment had no significant effect on most analysed genes. However, these same fish showed altered expression of the genes for cytosolic phosphoenolpyruvate carboxykinase, sodium-dependent glucose cotransporter 1 and glycogen synthase, suggesting changes to the glucose storage capacity in muscle and glucose production and transport in viscera. Overall, supplementation of egg yolk with high glucose levels had little effect on the long-term modulation of carbohydrate metabolic genes in zebrafish.

High-glucose feeding of gilthead seabream (Sparus aurata) larvae: Effects on molecular and metabolic pathways

“…during first-feeding stage). Promising studies upon applying the concept of nutritional programming in fish to improve their capacity to cope with high dietary carbohydrates have been conducted, mostly in fresh water species (Fang et al, 2014;Geurden et al, 2007Geurden et al, , 2014Gong et al, 2015;Rocha et al, 2014Rocha et al, , 2015. In contrast, only few were targeted to marine species (Vagner et al, 2009(Vagner et al, , 2007 of which none was aimed to programme the carbohydrate utilization.…”

“…However, in the past years the number of studies performed in this topic has been growing, as the concept gains more notability for fish nutrition research. Recent studies exploring the short-and long-term effects of carbohydrate stimulus on the modulation of metabolic pathways were performed: at different stages of zebrafish (Danio rerio) embryogenesis through direct supplementation of the embryo yolk reserve (Rocha et al, 2014(Rocha et al, , 2015 and at the onset of exogenous feeding in rainbow trout (Oncorhynchus mykiss) (Geurden et al, 2007, zebrafish (Fang et al, 2014) and Siberian sturgeon (Acipenser baerii) (Gong et al, 2015). With variable extent, all these studies showed some effects at molecular and/or metabolic level related to early nutritional conditioning.…”

Glucose metabolism ontogenesis in rainbow trout (Oncorhynchus mykiss) in the light of the recently sequenced genome: new tools for intermediary metabolism programming

“…However, such an investigation entails considering a non-nutritional stimulus such as hypoxia, known to affect glucose metabolism (Osumek et al, 2014;Zhong and Mostoslavsky, 2010), and having greater understanding of the transcription patterns of glucose metabolism-related genes during ontogenesis and before nutritional transition. Previous studies carried out in zebrafish (Rocha et al, 2013(Rocha et al, , 2015 have revealed that metabolic programming could occur following a nonnutritional stimulus such as nutrient injection, applied during late embryogenesis and before first feeding. The information obtained in this study will thus assist identification of potential windows of plasticity and the timing of application of the environmental stimulus.…”

High or low dietary carbohydrate:protein ratios during first-feeding affect glucose metabolism and intestinal microbiota in juvenile rainbow trout

“…Possible biological mechanisms for 'imprinting' the nutritional event until adulthood in mammalian vertebrates comprise adaptive changes in gene expression pattern or cellular phenotype (epigenetic phenomenon), nutrient-sensitive signalling pathways and adaptive clonal selection, which may be transmitted to future offspring (Lucas, 1998;Symonds et al, 2009;Waterland and Jirtle, 2003;Gut and Verdin, 2013). Experimental data on the concept of nutritional programming in fish are limited and some first knowledge stems from recent studies dealing with the possibility of altering the functioning of long-chain fatty acid desaturation in European seabass (Dicentrarchus labrax) (Vagner et al, 2007;Vagner et al, 2009), the use of dietary carbohydrates in rainbow trout [Oncorhynchus mykiss (Walbaum 1792)] (Geurden et al, 2007) or zebrafish (Danio rerio) (Fang et al, 2014;Rocha et al, 2014) and the acceptance and use of plant-based feed in rainbow trout . Taken together, the results all showed particular long-term effects on molecular markers or on growth, because of the acute early-life exposure to the imposed nutritional stimulus.…”

“…In fish, a nutritional stimulus during stages of high metabolic plasticity, such as embryogenesis or early larval development, can be applied at the egg stage [e.g. egg glucose injection (Rocha et al, 2014) or maternal nutrient transfer (Fernández-Palacios et al, 1995;Fernández-Palacios et al, 1997)] or at the onset of exogenous feeding (Geurden et al, 2007;Vagner et al, 2007;Vagner et al, 2009;Fang et al, 2014). Indeed, a previous study in trout by Geurden et al (Geurden et al, 2007) has shown that a hyperglucidic stimulus at the onset of feeding had a permanent effect on carbohydrate digestive enzymes at the juvenile stage, indicating a positive long-term physiological change induced by the first-feeding stimulus in rainbow trout.…”