scholarly journals New insights into the nutritional regulation of gluconeogenesis in carnivorous rainbow trout (Oncorhynchus mykiss): a gene duplication trail

2015 ◽  
Vol 47 (7) ◽  
pp. 253-263 ◽  
Author(s):  
Lucie Marandel ◽  
Iban Seiliez ◽  
Vincent Véron ◽  
Sandrine Skiba-Cassy ◽  
Stéphane Panserat

The rainbow trout ( Oncorhynchus mykiss) is considered to be a strictly carnivorous fish species that is metabolically adapted for high catabolism of proteins and low utilization of dietary carbohydrates. This species consequently has a “glucose-intolerant” phenotype manifested by persistent hyperglycemia when fed a high-carbohydrate diet. Gluconeogenesis in adult fish is also poorly, if ever, regulated by carbohydrates, suggesting that this metabolic pathway is involved in this specific phenotype. In this study, we hypothesized that the fate of duplicated genes after the salmonid-specific 4th whole genome duplication (Ss4R) may have led to adaptive innovation and that their study might provide new elements to enhance our understanding of gluconeogenesis and poor dietary carbohydrate use in this species. Our evolutionary analysis of gluconeogenic genes revealed that pck1, pck2, fbp1a, and g6pca were retained as singletons after Ss4r, while g6pcb1, g6pcb2, and fbp1b ohnolog pairs were maintained. For all genes, duplication may have led to sub- or neofunctionalization. Expression profiles suggest that the gluconeogenesis pathway remained active in trout fed a no-carbohydrate diet. When trout were fed a high-carbohydrate diet (30%), most of the gluconeogenic genes were non- or downregulated, except for g6pbc2 ohnologs, whose RNA levels were surprisingly increased. This study demonstrates that Ss4R in trout involved adaptive innovation via gene duplication and via the outcome of the resulting ohnologs. Indeed, maintenance of ohnologous g6pcb2 pair may contribute in a significant way to the glucose-intolerant phenotype of trout and may partially explain its poor use of dietary carbohydrates.

2001 ◽  
Vol 204 (2) ◽  
pp. 359-365 ◽  
Author(s):  
S. Panserat ◽  
E. Plagnes-Juan ◽  
J. Breque ◽  
S. Kaushik

Phosphoenolpyruvate carboxykinase (PEPCK) is a rate-limiting enzyme in hepatic gluconeogenesis and therefore plays a central role in glucose homeostasis. The aim of this study was to analyse the nutritional regulation of PEPCK gene expression in rainbow trout (Oncorhynchus mykiss), which are known to use dietary carbohydrates poorly. A full-length hepatic PEPCK cDNA (2637 base pairs with one open reading frame putatively encoding a 635-residue protein) was cloned and found to be highly homologous to mammalian PEPCKs. The presence of a putative peptide signal specific to a mitochondrial-type PEPCK in the deduced amino acid sequence suggests that this PEPCK gene codes for a mitochondrial form. In gluconeogenic tissues such as liver, kidney and intestine, this PEPCK gene was expressed at high levels and, in the liver we found no regulation of PEPCK gene expression by dietary carbohydrates. These results suggest that the first step of the hepatic gluconeogenic pathway in rainbow trout is functional and highly active irrespective of the dietary carbohydrate supply.


2001 ◽  
Vol 204 (13) ◽  
pp. 2351-2360 ◽  
Author(s):  
S. Panserat ◽  
E. Plagnes-Juan ◽  
S. Kaushik

SUMMARY Rainbow trout (Oncorhynchus mykiss) are known to use dietary carbohydrates poorly. One of the hypotheses to explain the poor utilisation of dietary glucose by these fish is a dysfunction in nutritional regulation of hepatic glucose metabolism. In this study, we obtained partial clones of rainbow trout cDNAs coding for a glucose transporter (Glut2), and for the enzymes 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (6PF-2K/F-2,6BPase), fructose-1,6-bisphosphatase (FBPase) and pyruvate kinase (PK). Their deduced amino acid sequences were highly similar to those of mammals (up to 80% similarity). In a study of nutritional regulation, the Glut2 gene was highly expressed in the liver irrespective of the nutritional status of the trout, in agreement with the role of this transporter in the input (during refeeding) and output (during fasting) of glucose from the liver. Moreover, whereas PK and FBPase gene expression was high irrespective of the nutritional status, levels of hepatic 6PF-2K/F-2,6BPase mRNA were higher in fish fed with carbohydrates than in fish deprived of food. The high levels of hepatic PK, Glut2 and 6PF-2K/F-2,6BPase gene expression observed in this study suggest a high potential for tissue carbohydrate utilisation in rainbow trout. The persistence of a high level of FBPase gene expression suggests an absence of regulation of the gluconeogenic pathway by dietary carbohydrates.


2012 ◽  
Vol 109 (8) ◽  
pp. 1359-1372 ◽  
Author(s):  
Sandrine Skiba-Cassy ◽  
Stéphane Panserat ◽  
Mélanie Larquier ◽  
Karine Dias ◽  
Anne Surget ◽  
...  

The rainbow trout (Oncorhynchus mykiss) exhibits high dietary amino acid requirements and an apparent inefficiency to use dietary carbohydrates. Using this species, we investigated the metabolic consequences of long-term high carbohydrates/low protein feeding. Fish were fed two experimental diets containing either 20 % carbohydrates/50 % proteins (C20P50), or high levels of carbohydrates at the expense of proteins (35 % carbohydrates/35 % proteins – C35P35). The expression of genes related to hepatic and muscle glycolysis (glucokinase (GK), pyruvate kinase and hexokinase) illustrates the poor utilisation of carbohydrates irrespective of their dietary levels. The increased postprandial GK activity and the absence of inhibition of the gluconeogenic enzyme glucose-6-phosphatase activity support the hypothesis of the existence of a futile cycle around glucose phosphorylation extending postprandial hyperglycaemia. After 9 weeks of feeding, the C35P35-fed trout displayed lower body weight and feed efficiency and reduced protein and fat gains than those fed C20P50. The reduced activation of eukaryotic translation initiation factor 4-E binding protein 1 (4E-BP1) in the muscle in this C35P35 group suggests a reduction in protein synthesis, possibly contributing to the reduction in N gain. An increase in the dietary carbohydrate:protein ratio decreased the expression of genes involved in amino acid catabolism (serine dehydratase and branched-chain α-keto acid dehydrogenase E1α and E1β), and increased that of carnitine palmitoyltransferase 1, suggesting a higher reliance on lipids as energy source in fish fed high-carbohydrate and low-protein diets. This probably also contributes to the lower fat gain. Together, these results show that different metabolic pathways are affected by a high-carbohydrate/low-protein diet in rainbow trout.


2021 ◽  
Vol 21 (07) ◽  
pp. 309-322
Author(s):  
Mitra Ravardshiri ◽  
Somayeh Bahram ◽  
Seyed Rohollah Javadian ◽  
Masoumeh Bahrekazemi

This study was conducted to investigate the effect of cinnamon in high- and low carbohydrate diets on the physiology of rainbow trout (Oncorhynchus mykiss (16.12±1.33 g). Six experimental diets including control/LCarb (200 g/kg carbohydrate), LCarb-3C (200 g/kg carbohydrate, 30 g/kg cinnamon), LCarb-5C (200g/kg carbohydrate, 50 g/kg cinnamon), HCarb (300 g/kg carbohydrate), HCarb-3C (300 g/kg carbohydrate, 30 g/kg cinnamon), and HCarb-5C (300 g/kg carbohydrate, 50 g/kg cinnamon) were formulated to feed fish for eight weeks. The results showed that fish fed dietary LCarb-3C (72.64 g) and LCarb-5C (73.17 g) had higher weight gain as compared with treatments without cinnamon (P<0.05). Blood performance in LCarb3C (67.10) was significantly higher than the HCarb-3C group (P<0.05). Fish fed dietary LCarb-3C had the best performance so that cinnamon in this group lowered glucose, total cholesterol, and low-density lipoprotein, improved total protein, and highdensity lipoprotein contents. Supplementation of this herb also improved protease and lipase in LCarb-3C and LCarb-5C groups as compared with control. Individuals fed supplemented diets but not HCarb had a higher superoxide dismutase activity when compared with the control group (P<0.05). Generally, cinnamon improved parameters in this study in fish fed a low-carbohydrate diet rather than a high-carbohydrate diet.


2020 ◽  
Vol 11 ◽  
Author(s):  
Thérèse Callet ◽  
Huihua Hu ◽  
Laurence Larroquet ◽  
Anne Surget ◽  
Jingwei Liu ◽  
...  

2002 ◽  
Vol 26 (4) ◽  
pp. 309-314 ◽  
Author(s):  
Melissa M. Ehrman ◽  
Gregory T. Melroe ◽  
Craig A. Moore ◽  
Jeffrey D. Kittilson ◽  
Mark A. Sheridan

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