Effects of insulin infusion on glucose homeostasis and glucose metabolism in rainbow trout fed a high-carbohydrate diet

Polakof, Sergio; Moon, Thomas W.; Aguirre, Pierre; Skiba‐Cassy, Sandrine; Panserat, Stéphane

doi:10.1242/jeb.050807

Cited by 43 publications

(31 citation statements)

References 45 publications

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“…Current information shows that insulin plays a major role in blocking R a glucose in animals undergoing acute elevation in glycemia. In mammals as well as trout, hepatic production is decreased when high insulin levels inhibit glucose release in the circulation by terminating the transcription of glucose 6-phosphatase (G6Pase) (Polakof et al, 2010a;Rojas and Schwartz, 2014 mammals (Shrayyef and Gerich, 2010). Similarly, gluconeogenesis is inhibited by high levels of insulin, which inhibits transcription of mammalian phosphoenolpyruvate carboxykinase (PEPCK) (Rojas and Schwartz, 2014).…”

Section: Suppression Of Hepatic Glucose Productionmentioning

confidence: 99%

Pushing the limits of glucose kinetics: how rainbow trout cope with a carbohydrate overload

Choi

Weber

2015

Journal of Experimental Biology

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Rainbow trout are generally considered to be poor glucoregulators. To evaluate this, exogenous glucose was administered to chronically hyperglycemic fish at twice the endogenous rate of hepatic production, and their ability to modulate glucose fluxes was tested. Our goals were to determine: (1) whether hyperglycemic fish maintain higher glucose fluxes than normal; (2) whether they can lower hepatic production (R a glucose) or stimulate disposal (R d glucose) to cope with a carbohydrate overload; and (3) an estimate of the relative importance of glucose as an oxidative fuel. Results show that hyperglycemic trout sustain elevated baseline R a and R d glucose of 10.6±0.1 µmol kg −1 min −1 (or 30% above normal). If 50% of R d glucose was oxidized as in mammals, glucose could account for 36 to 100% of metabolic rate when exogenous glucose is supplied. In response to exogenous glucose, rainbow trout can completely suppress hepatic glucose production and increase disposal 2.6-fold, even with chronically elevated baseline fluxes. Such large changes in fluxes limit the increase in blood glucose to 2.5-fold and are probably mediated by the effects of insulin on glucose transporters 2 and 4 and on key enzymes of carbohydrate metabolism. Without this strong and rapid modulation of glucose kinetics, glycemia would rise four times faster to reach dangerous levels, exceeding 100 mmol l −1. Such responses are typical of mammals, but rather unexpected for an ectotherm. The impressive plasticity of glucose kinetics demonstrated here suggests that trout have a much better glucoregulatory capacity than is usually portrayed in the literature.

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Section: Suppression Of Hepatic Glucose Productionmentioning

confidence: 99%

Pushing the limits of glucose kinetics: how rainbow trout cope with a carbohydrate overload

Choi

Weber

2015

Journal of Experimental Biology

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“…Insulin receptors are present in the major insulin-responsive tissues, including white muscle, liver, and adipose tissues (4,11,27), and upregulation of insulin-binding and tyrosine kinase activities is observed after insulin treatment and carbohydrate-rich diets, respectively (2,11,27). Moreover, we have recently demonstrated that both fasted and high-carbohydrate-fed rainbow trout respond to increased circulating exogenous insulin levels and that insulin improved glucose distribution and uptake by peripheral tissues, enhancing the capacity of the animal to deal with a glucose load (31,32).…”

mentioning

confidence: 96%

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

Polakof

Moon

Aguirre

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Polakof S, Moon TW, Aguirre P, Skiba-Cassy S, Panserat S. Glucose homeostasis in rainbow trout fed a high-carbohydrate diet: metformin and insulin interact in a tissue-dependent manner. Am J Physiol Regul Integr Comp Physiol 300: R166 -R174, 2011. First published November 10, 2010; doi:10.1152/ajpregu.00619.2010.-Carnivorous fish species such as the rainbow trout (Oncorhynchus mykiss) are considered to be "glucose intolerant" because of the prolonged hyperglycemia experienced after intake of a carbohydrateenriched meal. In the present study, we use this species to study glucose homeostasis in fish chronically infused with the hypoglycemic agents, insulin, and metformin, and fed with a high proportion of carbohydrates (30%). We analyzed liver, skeletal muscle, and white adipose tissue (WAT), which are insulin-and metformin-specific targets at both the biochemical and molecular levels. Trout infused with the combination of insulin and metformin can effectively utilize dietary glucose at the liver, resulting in lowered glycemia, increased insulin sensitivity, and glucose storage capacity, combined with reduced glucose output. However, in both WAT and skeletal muscle, we observed decreased insulin sensitivity with the combined insulin ϩ metformin treatment, resulting in the absence of changes at the metabolic level in the skeletal muscle and an increased potential for glucose uptake and storage in the WAT. Thus, the poor utilization by rainbow trout of a diet with a high proportion of carbohydrate can at least be partially improved by a combined treatment with insulin and metformin, and the glucose intolerance observed in this species could be, in part, due to some of the downstream components of the insulin and metformin signaling pathways. However, the predominant effects of metformin treatment on the action of insulin in these three tissues thought to be involved in glucose homeostasis remain exclusive in this species.fish; glucose homeostasis; muscle; liver; white adipose tissue; insulin; metformin COMMERCIAL AQUACULTURE OF most carnivorous fish species requires feeding these species a high-protein diet that currently is met with fish meal-based diets. The sustainability of this practice, which requires high quantities of wild fish is accepted today but not for the long term. Thus, it is recognized that the replacement of fish meal with plant raw materials represents a sustainable alternative for the stability and further expansion of aquaculture. However, such substitution remains problematic since feedstuffs of plant origin are naturally rich in carbohydrates, and species like the rainbow trout Oncorhynchus mykiss are considered to be "glucose intolerant" (21, 42) due mainly to the prolonged hyperglycemia experienced after a glucose load or intake of a carbohydrate-enriched meal (3, 24). This intolerance is not thought to be related to the absence of insulin, but, nonetheless, the mechanism(s) by which insulin regulates plasma glucose levels in fish remain speculative, and the relative contribution of the main...

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“…In primary cell culture of rainbow trout hepatocytes, insulin is able to stimulate GK gene expression, but the presence of amino acids seems to be necessary; otherwise, GK gene expression is repressed by insulin Lansard et al, 2010b). The inhibitory effect of insulin on GK gene expression was further confirmed in vivo following acute intraperitoneal administration of insulin or chronic infusion of insulin (4 days) in both fasted and high-carbohydrate fed fish (Polakof et al, 2010b(Polakof et al, , 2010d. The in vivo repression of GK gene by insulin in trout liver represents a paradoxical regulation in a fish species in which the natural carbohydrate intake is very low and the insulin secretion is well stimulated in fish fed high carbohydrate diets (Capilla et al, 2003).…”

Section: Glycolysismentioning

confidence: 87%

“…In rainbow trout, acute administration of insulin failed to stimulate PK gene expression in liver Polakof et al, 2010d), whereas it faintly decreased PK mRNA level in skeletal muscle. When insulin is chronically administered to fasted and high-carbohydrate rainbow trout using osmotic pumps, PK gene expression becomes slightly reduced in liver but no more different from saline-treated fish in muscle (Polakof et al, 2010b(Polakof et al, , 2010d. All these data indicate that in vivo, exogenous insulin poorly affect PK gene expression.…”

Section: Glycolysismentioning

confidence: 92%

“…For instance, studies conducted to investigate the phosphorylation status of the protein indicate that in liver the dephosphorylated form is the more active (Su and Storey, 1994), while in muscle phosphorylation by cAMP-dependent protein kinase increases 6PF1K activity (Mediavilla et al, 2007). Conversely, expression of 6PF1K was significantly enhanced by intraperitoneal administration of glucose to rainbow trout (Polakof et al, 2009b), whereas acute or chronic administration of insulin failed to regulate expression of 6PF1K both in liver and muscle of fasted and high-carbohydrate fed fish (Polakof et al, 2010b(Polakof et al, , 2010d. The regulation of 6PF1K gene expression was also investigated in vitro using primary cell culture of hepatocytes; in this cellular model, expression of 6PF1K is positively regulated by the combination of insulin and amino acids (Lansard et al, 2010b).…”

Section: Glycolysismentioning

confidence: 99%

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Functional Genomic Analysis of the Nutritional and Hormonal Regulation of Fish Glucose and Lipid Metabolism

Skiba‐Cassy¹,

Polakof²,

Seilez³

et al. 2012

Functional Genomics in Aquaculture

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Effects of insulin infusion on glucose homeostasis and glucose metabolism in rainbow trout fed a high-carbohydrate diet

Cited by 43 publications

References 45 publications

Pushing the limits of glucose kinetics: how rainbow trout cope with a carbohydrate overload

Pushing the limits of glucose kinetics: how rainbow trout cope with a carbohydrate overload

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

Functional Genomic Analysis of the Nutritional and Hormonal Regulation of Fish Glucose and Lipid Metabolism

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