Glucagon regulation of carbohydrate metabolism in rainbow trout: in vivo glucose fluxes and gene expression [RESEARCH ARTICLE]

Johnathon L. I. Forbes, Daniel J. Kostyniuk, Jan A. Mennigen, and Jean-Michel Weber

Glucagon increases fish glycemia, but how it affects glucose fluxes in vivo has never been characterized. The goal of this study was to test the hypothesis that glucagon stimulates hepatic glucose production (Ra) and inhibits disposal (Rd) of rainbow trout. Changes in the mRNA abundance of key proteins involved in glycolysis, gluconeogenesis, and glycogen breakdown were also monitored. Results show that glucagon increases glycemia (+38%) by causing a temporary mismatch between Ra and Rd before both fluxes converge below baseline (-17%). A novel aspect of the regulation of trout gluconeogenesis is also demonstrated: the completely different effects of glucagon on the expression of three Pepck isoforms (stimulation of pck1, inhibition of pck2a, and no response of pck2b). Glycogen phosphorylase was modulated differently among tissues, and muscle upregulated pygb and downregulated pygm. Glucagon failed to activate the cAMP-dependent protein kinase or FoxO1 signalling cascades. We conclude that trout hyperglycemia results from the combination of two responses: (i) an increase in Ra glucose induced by the stimulation of gluconeogenesis through transcriptional activation of pck1 (and possibly glycogen phosphorylase), and (ii) a decrease in Rd glucose via inhibition of glycogen synthase and glycolysis. The observed decrease in glucose fluxes after 4 h of glucagon administration may be caused by a counterregulatory response of insulin, potentially linked to the decrease in pygm transcript abundance. Overall, however, these integrated effects of glucagon only lead to modest changes in glucose fluxes that partly explain why trout seem to be unable to control glycemia very tightly.

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