Gut glucose metabolism in rainbow trout: implications in glucose homeostasis and glucosensing capacity

Abstract

The main objective of the present study was to evaluate the relative contribution of the intestine to glucose homeostasis in rainbow trout. In a first set of in vivo experiments trout were subjected to oral glucose treatments alone or in combination with insulin injections to assess changes in glucose-related enzymes activities, metabolite levels, and mRNA levels. Rainbow trout gut displays an important glucose metabolism that includes the ability to store glucose as glycogen (mostly in the muscle layers) and a large capacity to oxidize glucose. This constitutes a surprising result for a carnivorous fish. In a second set of in vivo experiments, trout received an oral amino acid solution alone or in combination with insulin injection to determine whether other factors besides fasting could regulate gluconeogenesis in intestine. The results confirm the absence of regulation of gluconeogenesis in trout gut, which does not respond to hormones, glucose, lactate, or amino acid changes, either in vivo or in vitro. We also fully characterized gut glucose metabolism in vitro. We observed that a large amount of glucose is oxidized to lactate, supporting the importance of glucose in gut metabolism. Moreover, we corroborated the minor actions of insulin in trout gut, whereas other hormones such as glucagon-like peptide-1 and C-peptide appear to be major hormonal regulators of glucose metabolism in fish gut. Finally, we obtained the first evidence for the existence of a glucosensing mechanism in the midgut of this carnivorous species.

Glycemic and insulin responses in white sea bream Diplodus sargus, after intraperitoneal administration of glucose

“…Peak glucose values were within the range of values observed in other fish species (14-25 mmol l -1 ) orally or intraperitoneally injected with the same glucose dose (Palmer and Ryman 1972;Hemre et al 1995;Garcia-Riera and Hemre 1996;Peres et al 1999;Stone et al 2003;Booth et al 2006;Polakof et al 2010;Enes et al 2011). Time to reach the glucose peak in white sea bream was similar to that observed in European sea bass Dicentrarchus labrax (2 h) (Enes et al 2011) and lower than in turbot Scophthalmus maximus, and snapper Pagrus auratus, which required 3 h to reach the glucose peak (Garcia-Riera and Hemre 1996; Booth et al 2006).…”

Glucose homeostasis in rainbow trout fed a high-carbohydrate diet: metformin and insulin interact in a tissue-dependent manner

“…This glycemic effect of metformin was previously observed in fish, although the administration method was different: transdermally for zebrafish embryos (8), in the food for trout (26), or intaperitoneally (acute) for carp (13). The fact that the lowering effects on glycemia were observed in trout fed with carbohydrates as opposed to a previous study using fasted trout injected acutely (intraperitoneally) with glucose (33), confirmed that the nutritional status of the animal is key for the metformin action and supports a possible indirect involvement of the gastrointestinal tract on glucose homeostasis (29).…”

ACTH-stimulated cortisol release from head kidney of rainbow trout is modulated by glucose concentration

“…In contrast to the GK-mediated sensor, there is no clear evidence in fish regarding the presence of any of these sensors yet, with only preliminary evidence describing SGLT-1 in rainbow trout intestine (Polakof et al, 2010). We have evaluated the response of several parameters related to these putative glucosensor systems in head kidneys of rainbow trout maintained under different glucose concentrations.…”

“…The primary antibodies used in this study were polyclonal rabbit anti-GK (Santa Cruz Biotechnology, Santa Cruz, CA, USA), polyclonal rabbit anti-SGLT-1 (Millipore, Billerica, MA, USA) and monoclonal mouse anti-TH (tyrosine hydroxylase, Millipore). The specificity of GK and SGLT-1 antibodies was previously tested by western blotting (Polakof et al, 2010).…”