Hepatic glucose metabolic responses to digestible dietary carbohydrates in two isogenic lines of rainbow trout

Abstract

Rainbow trout (Oncorhynchus mykiss) was recognized as a typical ‘glucose-intolerant’ fish and poor dietary carbohydrate user. Our first objective was to test the effect of dietary carbohydrates themselves (without modification of dietary protein intake) on hepatic glucose gene expression (taking into account the paralogs). The second aim was to research if two isogenic trout lines had different responses to carbohydrate intake, showing one with a better use dietary carbohydrates. Thus, we used two isogenic lines of rainbow trout (named A32h and AB1h) fed with either a high carbohydrate diet or a low carbohydrate diet for 12 weeks. We analysed the zootechnical parameters, the plasma metabolites, the hepatic glucose metabolism at the molecular level and the hormonal-nutrient sensing pathway. Globally, dietary carbohydrate intake was associated with hyperglycaemia and down regulation of the energy sensor Ampk, but also with atypical regulation of glycolysis and gluconeogenesis in the liver. Indeed, the first steps of glycolysis and gluconeogenesis catalysed by the glucokinase and the phospenolpyruvate carboxykinase are regulated at the molecular level by dietary carbohydrates as expected (i.e. induction of the glycolytic gck and repression of the gluconeogenic pck); by contrast, and surprisingly, for two other key glycolytic enzymes (phosphofructokinase enzyme – pfkl and pyruvate kinase – pk) some of the paralogs (pfklb and pklr) are inhibited by carbohydrates whereas some of the genes coding gluconeogenic enzymes (the glucose-6-phosphatase enzyme g6pcb1b and g6pcb2a gene and the fructose1-6 biphosphatase paralog fbp1a) are induced. On the other hand, some differences for the zootechnical parameters and metabolic genes were also found between the two isogenic lines, confirming the existence of genetic polymorphisms for nutritional regulation of intermediary metabolism in rainbow trout. In conclusion, our study determines some new and unexpected molecular regulations of the glucose metabolism in rainbow trout which may partly lead to the poor utilization of dietary carbohydrates and it underlines the existence of differences in molecular regulation of glucose metabolism between two isogenic lines which provides arguments for future selection of rainbow trout.

Regulations on glucose metabolism affected by dietary carbohydrate in different strains of juvenile gibel carp (Carassius gibelio)

“…In the present study, the mRNA level of pfk encoding for glycolytic enzyme was increased by 30C diet and the mRNA levels of fbp and g6p genes encoding for the key gluconeogenic enzymes were not changed by dietary carbohydrate in three strains. These findings were different with the performance observed in rainbow trout that glycolysis was inhibited whereas gluconeogenesis was induced after feeding with carbohydrate diet (Song et al, ). The typical regulation on glucose use and production related to the low levels of plasma glucose and triglyceride partly explained a better ability of using dietary carbohydrate for gibel carp.…”

“…The strong interaction for lipid biosynthesis may link to the higher whole body lipid content in DT strain. As found in rainbow trout that higher lipogenic ability contributed to decrease postprandial glycaemia and tolerate more dietary carbohydrate (Skiba‐Cassy et al, ; Song et al, ). However, DT strain had higher plasma glucose and poor growth performance suggesting that even though lipogenesis was significantly induced by high carbohydrate diet in DT strain, the limited effects cannot improve carbohydrate utilization, but it need to be tested in the future studies.…”

“…Carbohydrate was an important energy source; excessive dietary carbohydrate always resulted in fatty liver and crude lipid accumulation (Li, ; Song et al, ). In the present study, whole body energy content increased with increasing dietary carbohydrate levels.…”

“…glut2: glucose transporter 2 Light grey bar: DT strain (Dongting strain); Dark grey bar: A strain (gibel carp CAS III); Black bar: F strain (gibel carp CAS V strain). Data were presented as mean ± SD (n = 3 tanks), statistical differences of glut2 were evaluated by two-way ANOVA (p < 0.05, values in bold) DT strain A strain F strain DT strain> A strain, F strain; p = 0.01 inhibited whereas gluconeogenesis was induced after feeding with carbohydrate diet (Song et al, 2018). The typical regulation on glucose use and production related to the low levels of plasma glucose and triglyceride partly explained a better ability of using dietary carbohydrate for gibel carp.…”

Molecular adaptations of glucose and lipid metabolism to different levels of dietary carbohydrates in juvenile Japanese flounderParalichthys olivaceus

“…The present study showed that the increase in glycogen in the liver was correlated with the increase in dietary carbohydrate levels, which could be mediated via increased glycogenic gys2 mRNA levels and reduced glycogenolytic pygl mRNA levels. This is consistent with previously reported studies in silver sea bream ( Sparus sarba ), rainbow trout ( Oncorhynchus mykiss ) and Wuchang bream ( Megalobrama amblycephala ) (Leung & Woo, ; Song, Marandel, Dupont‐Nivet, et al, ; Zhou et al, ). In the present study, intake of 120 g/kg dietary carbohydrates induced higher hepatic mRNA levels of gck and pfkl and HK activity, which are the rate‐limiting genes in glycolysis (Massa, Gagliardino, & Francini, ; Song, Marandel, Skiba‐Cassy, et al, ).…”