Contribution of dietary starch to hepatic and systemic carbohydrate fluxes in European seabass (Dicentrarchus labraxL.)

Abstract

In the present study, the effects of partial substitution of dietary protein by digestible starch on endogenous glucose production were evaluated in European seabass (Dicentrarchus labrax). The fractional contribution of dietary carbohydrates v. gluconeogenesis to blood glucose appearance and hepatic glycogen synthesis was quantified in two groups of seabass fed with a diet containing 30 % digestible starch (DS) or without a carbohydrate supplement as the control (CTRL). Measurements were performed by transferring the fish to a tank containing water enriched with 5 % 2 H 2 O over the last six feeding days, and quantifying the incorporation of 2 H into blood glucose and hepatic glycogen by 2 H NMR. For CTRL fish, gluconeogenesis accounted for the majority of circulating glucose while for the DS fish, this contribution was significantly lower (CTRL 85 (SEM 4) % v. DS 54 (SEM 2) %; P,0·001). Hepatic glycogen synthesis via gluconeogenesis (indirect pathway) was also significantly reduced in the DS fish, in both relative (CTRL 100 (SEM 1) % v. DS 72 (SEM 1) %; P, 0·001) and absolute terms (CTRL 28 (SEM 1) v. DS 17 (SEM 1) mmol/kg per h; P,0·001). A major fraction of the dietary carbohydrates that contributed to blood glucose appearance (33 (SEM 1) % of the total 47 (SEM 2) %) had undergone exchange with hepatic glucose 6-phosphate. This indicated the simultaneous activity of hepatic glucokinase and glucose 6-phosphatase. In conclusion, supplementation of digestible starch resulted in a significant reduction of gluconeogenic contributions to systemic glucose appearance and hepatic glycogen synthesis. Key words:2 H 2 O: Gluconeogenesis: Endogenous glucose production: Glucokinase: Starch utilisationIn aquaculture, substituting costly fishmeal with less expensive plant-derived carbohydrate (CHO) reduces feed input costs. The provision of dietary CHO to carnivorous fish such as the European seabass (Dicentrarchus labrax L.) may also have environmental benefits since CHO utilisation can potentially spare the catabolism of dietary amino acids to glucose and nitrogenous waste (1) . Dietary CHO influences growth, feed utilisation and deposition of nutrients according to species, quantity, origin and pre-treatment for improving digestibility (2 -4) . The effects of partial substitution of dietary protein by plant-derived CHO on food conversion efficiency and nutrient digestibility sources have been tested in seabass (5 -7) . In addition, its effects on energy retention and maintenance requirements (8) as well as the activity of key CHO-metabolising enzymes (6,9) have been studied. These studies have suggested that, on the one hand, carnivorous fish are able to up-regulate their capacity for hepatic glucose utilisation through the increased expression of gateway enzymes such as glucokinase when fed with a high-CHO diet. However, on the other hand, supplementation of fish feed with up to 30 % starch has not been shown to alter the overall protein efficiency ratio or nitrogen retention in seabass (7) . This is despite...

Hepatic fatty acid biosynthesis is more responsive to protein than carbohydrate in rainbow trout during acute stimulations

“…Given that AAs, especially gluconeogenic AAs, can promote glucose production through hepatic gluconeogenic pathway (5, 15), we presume that both the elevated FAA levels and the reduced glycemia by rapamycin may be related to the suppressed hepatic gluconeogenesis, as previously demonstrated (16), implicating the importance of hepatic gluconeogenesis in modulating glucose homeostasis. Notably, consistent with this deduction, recent work using stable tracer method by Viegas et al (89) revealed that supplementation of digestible starch resulted in a significant reduction of gluconeogenic contributions to systemic glucose appearance in sea bass.…”

Impact of dietary starch on extrahepatic tissue lipid metabolism in farmed European (Dicentrarchus labrax) and Asian seabass (Lates calcarifer)

“…In vitro studies, namely the infusion of adipocytes with 14 C-glucose (Bou et al, 2016) have also contributed to a better understanding this subject. Instead of following the metabolic fate of a single labeled substrate, the stable isotope deuterium ( 2 H), presented as deuterated water ( 2 H2O) in fish tanks, rapidly equilibrates with fish body water (Viegas et al, 2011) and gets widely incorporated in newly synthesized metabolites such as alanine (Marques et al, 2016), glucose or glycogen (Viegas et al, 2015). Similarly, 2 H gets incorporated into different sites of the triacylglycerol (TAG) molecule following well-defined metabolic steps from which estimations for de novo lipogenesis (DNL) and glycerol turnover can be derived (Viegas et al, 2016).…”

Role of upstream stimulatory factor 2 in glutamate dehydrogenase gene transcription

“…We cannot discard that in addition to speciesspecificity, differences in the effect of starvation on the expression of Gdh among experiments may result also from diet composition, ration size and feeding regime. In this regard, it is well known that dietary protein greatly influences the hepatic activity of Gdh in fish (Liu et al 2012, Borges et al 2013, Caballero-Solares et al 2015, Viegas et al 2015, Coutinho et al 2016. Indeed, it was reported that starvation decreased or unaffected Gdh activity in the liver of starved Dicentrarchus labrax depending on dietary protein levels (Pérez-Jiménez et al 2007).…”

“…Dietary protein increases plasma free amino acids, which in turn enhances Gdh-dependent deamination and leads to higher rates of ammonia excretion. Dietary supplementation of glutamate downregulates Gdh mRNA levels and decreases reductive Gdh activity in the liver of Sparus aurata (Gómez-Requeni et al 2003, Caballero-Solares et al 2015 and reduces Gdh activity in Pagellus bogaraveo (Figueiredo-Silva et al 2010), while it increases in Oncorhynchus mykiss (Moyano et al 1991).…”

“…The fact that Gdh plays a major role in amino acid oxidation in the liver, led to consider Gdh a marker for protein utilisation and ammonia excretion in fish (Liu et al 2012). Gdh is mainly expressed in the piscine liver, and high-protein diets usually stimulate growth and hepatic Gdh activity in fish (Bibiano Melo et al 2006, Borges et al 2013, Viegas et al 2015, Coutinho et al 2016. Dietary protein increases plasma free amino acids, which in turn enhances Gdh-dependent deamination and leads to higher rates of ammonia excretion.…”