Glucose and lipid metabolism in the pancreas of rainbow trout is regulated at the molecular level by nutritional status and carbohydrate intake

Abstract

Glucose and lipid metabolism in pancreatic islet organs is poorly characterized. In the present study, using as a model the carnivorous rainbow trout, a glucose-intolerant fish, we assessed mRNA expression levels of several genes involved in glucose and lipid metabolism (including ATP-citrate lyase; carnitine palmitoyltransferase-1 isoforms, CPT; the mitochondrial isoform of the phosphoenolpyrutave carboxykinase, mPEPCK and pyruvate kinase, PK) and glucosensing (glucose transporter type 2, Glut2; glucokinase, GK and the potassium channel, K(ATP)) in Brockmann bodies. We evaluated the response of these parameters to changes in feeding status (food deprived vs. fed fish) as well as to changes in the amount of carbohydrate (dextrin) in the diet. A general inhibition of the glycolytic (including the glucosensing marker GK) and β-oxidation pathways was found when comparing fed versus food-deprived fish. When comparing fish feeding on either low- or high-carbohydrate diets, we found that some genes related to lipid metabolism were more controlled by the feeding status than by the carbohydrate content (fatty acid synthase, CPTs). Findings are discussed in the context of pancreatic regulation of glucose and lipid metabolism in fish, and show that while trout pancreatic metabolism can partially adapt to a high-carbohydrate diet, some of the molecular actors studied seem to be poorly regulated (K(ATP)) and may contribute to the glucose intolerance observed in this species when fed high-carbohydrate diets.

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

“…Although few, some genes involved in glycolysis, lipogenesis and energy production pathways were enhanced: GK and FAS (by stimulus 1), G6PDH (by stimulus 2) and 6PFK-L, PK and CS genes (by stimulus 3). These data are similar to the postprandial induction of gene expression observed in rainbow trout, gilthead seabream and zebrafish, after a high carbohydrate intake (Enes et al, 2008b;Kamalam et al, 2012;Meton et al, 2004;Panserat et al, 2000;Polakof et al, 2012b;Seiliez et al, 2013), comparable to what occurs in mammals (Kersten, 2001;Pilkis and Granner, 1992;Yamada and Noguchi, 1999). Moreover, a similar short-term regulation for higher expression of GK and HK1 glycolytic enzymes was observed in rainbow trout and zebrafish fed at first-feeding with a high level (50 to 65%) of dietary carbohydrates (Fang et al, 2014;Geurden et al, 2007Geurden et al, , 2014.…”

Hepatic fatty acid biosynthesis is more responsive to protein than carbohydrate in rainbow trout during acute stimulations

“…These results are consistent with previous demonstrations in rainbow trout (60,61,75,82), showing that high-carbohydrate diets induced hyperglycemia and reduced plasma AA levels. These plasma parameters clearly confirmed the efficiency of controlled feeding method.…”

“…Interestingly, rapamycin also enhanced plasma FAA levels 8 h after controlled feeding. This elevated FAA level was negatively associated with the reduced glycemia, which is consistent with previous observations in trout (60,61,75,82). Given that AAs, especially gluconeogenic AAs, can promote glucose production through hepatic gluconeogenic pathway (5, 15), we presume that both the elevated FAA levels and the reduced glycemia by rapamycin may be related to the suppressed hepatic gluconeogenesis, as previously demonstrated (16), implicating the importance of hepatic gluconeogenesis in modulating glucose homeostasis.…”

Comparison of Glucose and Lipid Metabolic Gene Expressions between Fat and Lean Lines of Rainbow Trout after a Glucose Load

“…In mammals, high carbohydrate availability reduces fatty acid oxidation via an increase in plasma insulin and decreased free fatty acid availability [25], [26]. On the contrary, in rainbow trout, regulation of enzymes involved in fatty acid oxidation was not dependent on the carbohydrate content of the diet [16], [27], [28]. Even conversely, glucose treatment was found to stimulate the rate of hepatic lipolysis by increasing the activity of hepatic lipase activity in rainbow trout [29].…”