Teleost fishes represent a highly diverse group consisting of more than 20,000 species living across all aquatic environments. This group has significant economical, societal and environmental impacts, yet research efforts have concentrated primarily on salmonid and cyprinid species. This review examines carbohydrate/glucose metabolism and its regulation in these model species including the role of hormones and diet. Over the past decade, molecular tools have been used to address some of the downstream components of these processes and these are incorporated to better understand the roles played by carbohydrates and their regulatory paths. Glucose metabolism remains a contentious area as many fish species are traditionally considered glucose intolerant and, therefore, one might expect that the use and storage of glucose would be considered of minor importance. However, the actual picture is not so clear since the apparent intolerance of fish to carbohydrates is not evident in herbivorous and omnivorous species and even in carnivorous species, glucose is important for specific tissues and/or for specific activities. Thus, our aim is to up-date carbohydrate metabolism in fish, placing it to the context of these new experimental tools and its relationship to dietary intake. Finally, we suggest that new research directions ultimately will lead to a better understanding of these processes.
The aim of this study was to evaluate the existence of a glucosensor in different regions of the brain and in the Brockmann bodies (BB) of the rainbow trout, Oncorhynchus mykiss. Five groups (n = 12) of trout were injected intraperitoneally with saline alone (control) or saline-containing bovine glucagon (100 mug/kg), bovine insulin (4 mg/kg), 2-deoxy-d-glucose (100 mg/kg), or d-glucose (500 mg/kg) to promote hyperglycemia (glucagon, d-glucose, 2-deoxy-d-glucose) or hypoglycemia (insulin). Six hours after injection, samples from four brain regions (hypothalamus, telencephalon, hindbrain, and midbrain) and the entire BB were taken. Our results demonstrate within the BB and both the hypothalamus and hindbrain a metabolic response different to that observed in other tissues (midbrain, telencephalon) but similar to that described in tissues known to be glucosensors in mammals. The metabolic responses of these areas to changes in plasma glycemia were characterized by parallel changes in GLUT-2 expression, hexokinase-IV, or glucokinase activity and expression, glycolytic potential, and levels of glycogen and glucose. These changes are similar to those reported in mammalian pancreatic beta-cells and glucose-excited (GE) neurons, two cell types containing glucosensors. This study provides evidence for the presence of glucosensors responsive to hyper- and hypoglycemia in rainbow trout BB, hypothalamus, and hindbrain.
Carnivorous fish are poor users of dietary carbohydrates and are considered to be glucose intolerant. In this context, we have tested, for the first time in rainbow trout, metformin, a common anti-diabetic drug, known to modify muscle and liver metabolism and to control hyperglycemia in mammals. In the present study, juvenile trout were fed with very high levels of carbohydrates (30% of the diet) for this species during 10 days followed by feeding with pellets supplemented with metformin (0.25% of the diet) for three additional days. Dietary metformin led to a significant reduction in postprandial glycemia in trout, demonstrating unambiguously the hypoglycemic effect of this drug. No effect of metformin was detected on mRNA levels for glucose transporter type 4 (GLUT4), or enzymes involved in glycolysis, mitochondrial energy metabolism, or on glycogen level in the white muscle. Expected inhibition of hepatic gluconeogenic (glucose-6-phosphatase, fructose-1,6-bisphosphatase, and phosphoenolpyruvate carboxykinase) mRNA levels was not found, showing instead paradoxically higher mRNA levels for these genes after drug treatment. Finally, metformin treatment was associated with higher mRNA levels and activities for lipogenic enzymes (fatty acid synthase and glucose-6-phosphate dehydrogenase). Overall, this study strongly supports that the induction of hepatic lipogenesis by dietary glucose may permit a more efficient control of postprandial glycemia in carnivorous fish fed with high carbohydrate diets.
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