Fuel use during glycogenesis in rainbow trout (Oncorhynchus mykissWalbaum) white muscle studiedin vitro

Abstract

SUMMARY The purpose of this study was to examine fuel used during muscle glycogenesis in rainbow trout Oncorhynchus mykiss using an in vitro muscle slice preparation to test the hypothesis that intracellular lactate is the major glycogenic substrate and the muscle relies upon extracellular substrates for oxidation. Fish were exhaustively exercised to reduce muscle glycogen content, muscle slices were taken from exhausted fish and incubated for 1 h in medium containing various substrates at physiological concentrations. 14C-labeled lactate, glycerol or palmitate was added and 14C incorporation into muscle glycogen and/or CO2 was measured. Lactate clearance in the absence of net glycogenesis suggests that when suitable oxidizable extracellular substrates were lacking, intracellular lactate was oxidized. Only muscle incubated in lactate, glycerol or palmitate synthesized glycogen, with the greatest synthesis in muscle incubated in lactate plus glycerol. The major fate of these extracellular substrates was oxidative, with lactate oxidized at rates 10 times that of palmitate and 100 times that of glycerol. Neither extracellular lactate nor glycerol contributed significantly to glycogenesis,with lactate carbon contributing less than 0.1% of the total glycogen synthesized, and glycerol less than 0.01%. There was 100 times more extracellular lactate-carbon incorporated into CO2 than into glycogen. In the presence of extracellular lactate, palmitate or glycerol,intracellular lactate was spared an oxidative fate, allowing it to serve as the primary substrate for in situ glycogenesis, with oxidation of extracellular substrates driving ATP synthesis. The primary fate of extracellular lactate is clearly oxidative, while that of intracellular,glycolytically derived lactate is glycogenic, which suggests intracellular compartmentation of lactate metabolism.

Dietary carbohydrate-to-protein ratio affects TOR signaling and metabolism-related gene expression in the liver and muscle of rainbow trout after a single meal

“…However, the absence of stimulation of expression of glycolytic genes, even the significant inhibition of PK gene expression, tends to refute this hypothesis and suggests that there is very limited use of glucose by the muscle. This is also in agreement with the well-known low rate of glucose phosphorylation by hexokinases in trout muscle compared with mammalian species (10,13,53). This was further confirmed by the stable level of muscle glycogen levels in fasted and refed trout measured in the present study (data not shown).…”

Insulin regulates the expression of several metabolism-related genes in the liver and primary hepatocytes of rainbow trout (Oncorhynchus mykiss)

“…However, findings concerning other metabolic mediators of glucose metabolism suggest the existence of atypical regulation after carbohydrate intake by trout, i.e. a lower capacity for glucose phosphorylation by hexokinases in the muscle of fish than in mammalian species, as confirmed by the poor role of exogenous glucose as a glycogenic substrate in trout muscle (Kam and Milligan, 2006;Kirchner et al, 2005;Wilson, 1994). Moreover, in rainbow trout a carbohydrate-rich diet does not affect the activity or gene expression of key enzymes of gluconeogenesis such as glucose 6-phosphatase (G6Pase), fructose 1,6-bisphosphatase (FBPase) and phosphoenolpyruvate carboxykinase (PEPCK) (Panserat et al, 2001b;Panserat et al, 2000a;Panserat et al, 2001c;Tranulis et al, 1991).…”

Metformin improves postprandial glucose homeostasis in rainbow trout fed dietary carbohydrates: a link with the induction of hepatic lipogenic capacities?

“…For some such as glucokinase (GCK; EC 2.7.1.2) (liver), phosphofructokinase (EC 2.7.1.11) (liver and muscle), and pyruvate kinase (PK; EC 2.7.1.40) (liver and muscle), their induction by dietary carbohydrates is similar to that described in mammalian systems (16,38,41). However, data on other metabolic actors of glucose metabolism suggest the existence of an atypical regulation after carbohydrate intake by trout, including a lower capacity for glucose phosphorylation by hexokinases (HKs) in the muscle of fish than in mammalian species, which was further confirmed by the poor utilization of exogenous glucose as a glycogenic substrate in trout muscle (23,26,55). In addition, carbohydrate-rich diets do not affect the activity or mRNA levels of key enzymes of trout hepatic gluconeogenesis, including glucose-6-phosphatase (G-6-Pase; EC 3.1.3.9), fructose-1,6-bisphosphatase (FBPase; EC 3.1.3.11) or phosphoenolpyruvate carboxykinase (PEPCK; EC 4.1.1.49) (27,39,40,41) in contrast to mammals (12,33,51).…”