Abstract

The relative glucose intolerance of carnivorous fish species is often proposed to be a result of poor peripheral insulin action or possibly insulin resistance. In the present study, data from aortic cannulated rainbow trout receiving bovine insulin (75 mIU kg(-1)) injections show for the first time their ability to clear glucose in a very efficient manner. In another set of experiments, mRNA transcripts and protein phosphorylation status of proteins controlling glycaemia and glucose-related metabolism were studied during both acute and chronic treatment with bovine insulin. Our results show that fasted rainbow trout are well adapted at the molecular level to respond to increases in circulating insulin levels, and that this hormone is able to potentially improve glucose distribution and uptake by peripheral tissues. After acute insulin administration we found that to counter-regulate the insulin-induced hypoglycaemia, trout metabolism is strongly modified. This short-term, efficient response to hypoglycaemia includes a rapid, coordinated response involving the reorganization of muscle and liver metabolism. During chronic insulin treatment some of the functions traditionally attributed to insulin actions in mammals were observed, including increased mRNA levels of glucose transporters and glycogen storage (primarily in the muscle) as well as decreased mRNA levels of enzymes involved in de novo glucose production (in the liver). Finally, we show that the rainbow trout demonstrates most of the classic metabolic adjustments employed by mammals to efficiently utilize glucose in the appropriate insulin context.

Highlights

  • Carnivorous fish species like rainbow trout (Oncorhynchus mykiss) are traditionally considered as glucose intolerant (Moon, 2001; Wilson, 1994) due primarily to the prolonged hyperglycaemia experienced after a glucose load or intake of carbohydrate-enriched meals (Bergot, 1979; Palmer and Ryman, 1972)

  • Transcript levels of glucose transporter type 2 (GLUT2; Fig. 4A) and hexokinase (HK; Fig. 4B) over the short term were up-regulated in insulin-injected fish, transcript levels of other glycolytic enzymes remained unaffected by the hormone

  • Taken together, the results obtained in the present study indicate that the fasted rainbow trout is well adapted to respond to both acute and chronic increases in circulating insulin levels, and that this hormone is able to improve glucose distribution and uptake by peripheral tissues, enhancing the capacity of the animal to deal with a glucose load

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Summary

Introduction

Carnivorous fish species like rainbow trout (Oncorhynchus mykiss) are traditionally considered as glucose intolerant (Moon, 2001; Wilson, 1994) due primarily to the prolonged hyperglycaemia experienced after a glucose load or intake of carbohydrate-enriched meals (Bergot, 1979; Palmer and Ryman, 1972). Initially the basis for this poor metabolic glucose utilization was though to be a deficiency in insulin secretion (Furuichi and Yone, 1981; Palmer and Ryman, 1972), later hormone titration in several fish species demonstrated that plasma insulin levels in piscine species are even higher than in mammals (Mommsen and Plisetskaya, 1991). The most prominent response to exogenous insulin injection is hypoglycaemia (Ince, 1983b) Both the magnitude and duration of this hypoglycaemic effect are dependent on several factors, including insulin type and dose level, route of injection, season, nutritional state and previous nutritional history (Ince, 1983b; Mommsen and Plisetskaya, 1991)

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