Physiological regulation of glucose transporter (GLUT4) protein content in brown trout (Salmo trutta) skeletal muscle

Abstract

SUMMARY In brown trout, red and white skeletal muscle express the insulin-regulatable glucose transporter 4 (btGLUT4). We have previously shown that the mRNA expression of btGLUT4 in red muscle, but not white muscle, is altered under experimental conditions designed to cause changes in the plasma levels of insulin, such as fasting, insulin and arginine administration. In order to determine whether changes of btGLUT4 expression at the mRNA level are correlated with changes at the protein level, we performed in vivoexperiments to alter blood insulin concentrations and determined the abundance of btGLUT4 protein in trout red and white skeletal muscle by immunoblotting using an antibody to salmon GLUT4. In the present study we show that btGLUT4 protein content in red muscle decreases after fasting and increases after insulin administration. By contrast, btGLUT4 protein content in white muscle decreases after fasting but is not affected by insulin treatment. Our results show a good correlation between the changes observed in btGLUT4 protein and the previously reported changes in mRNA levels in response to alterations in circulating insulin, indicating that the regulation of btGLUT4 in brown trout takes place predominantly in the red skeletal muscle.

Expression of rainbow trout glucose transporters GLUT1 and GLUT4 during in vitro muscle cell differentiation and regulation by insulin and IGF-I

“…The observed ability of insulin to stimulate GLUT4 mRNA expression in vitro in trout muscle cells is consistent with the results of a previous in vivo study from our group that established a relationship between insulin plasma levels and GLUT4 mRNA levels in skeletal muscle in trout (8). More recently, we have shown that insulin and arginine administration increase, whereas fasting decreases GLUT4 protein content in trout skeletal muscle (12), supporting the notion that circulating insulin may regulate the expression of GLUT4, both at the mRNA and protein levels, in skeletal muscle. Therefore, the present study provides the first evidence in fish (and in nonmammalian vertebrates) that insulin is able to regulate GLUT4 mRNA content in trout skeletal muscle by exerting its function directly on muscle cells.…”

“…Nevertheless, little is known about the regulation of the expression of fish GLUT4 by insulin or IGF-I. Previous in vivo studies from our laboratory have shown a direct correlation between blood insulin levels and mRNA and protein expression levels of GLUT4 in trout red skeletal muscle (8,12). In contrast to GLUT4, GLUT1 mRNA expression in both white and red trout skeletal muscle remained invariable to the changes in plasma insulin (8).…”

“…To date, four members of the family of facilitated glucose transporters (GLUT1-4) have been cloned and identified in different species of teleost fish (7, 20 -22, 27, 35, 44, 45, 49). In particular, GLUT1 and GLUT4 are expressed in fish skeletal muscle (8,12,22,35,43). Functional studies of fish GLUT1 and GLUT4 homologs expressed in Xenopus oocytes have demonstrated that these transporters are indeed able to transport glucose and that they differ in their affinity for glucose, since that for GLUT4 is higher than that for GLUT1, albeit lower than that of their mammalian counterparts (7,43).…”

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

“…Glucose uptake mediated by the facilitative insulin-regulated glucose transporter GLUT4 homologue in white muscle and fat tissues and by GLUT2 in the liver has been reported in trout (Capilla et al, 2002;Diaz et al, 2007a;Diaz et al, 2007b;Krasnov et al, 2001). Fish glucose transporters GLUT2 and GLUT4 are characterized by a lower affinity for glucose, which may at least partly explain the persistent post-prandial hyperglycemia observed in trout fed with carbohydrates (Capilla et al, 2004a;Krasnov et al, 2001).…”

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

“…In rainbow trout, a system similar to that proposed in mammals involved in the detection of changes in circulating glucose levels by pancreatic ␤-cells and glucose-excited neurons in the hypothalamus and the brain stem appears to be functional and inducible (48,49). Glucose uptake mediated by the facilitative insulin-regulated glucose transporter GLUT4 homolog in white muscle and fat tissues and by GLUT2 in liver are observed in trout (6,9,10,30). At the metabolic level, most key enzymes involved in carbohydrate metabolism are described in fish (7).…”