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Effects of dietary glucose and dextrin on activity and gene expression of glucokinase and fructose-1,6-bisphosphatase in liver of turbot Scophthalmus maximus

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Abstract

Glucokinase (GK) and fructose-1,6-bisphosphatase (FBPase) play crucial role in glucose metabolism. In the present study, the cDNA encoding GK and FBPase was cloned from the liver of turbot Scophthalmus maximus by rapid amplification of cDNA end technique. Effects of dietary glucose and dextrin on the activities and gene expressions of these two enzymes were also studied. Results showed that the full length of GK cDNA was 2226 bp, consisting of an open reading frame (ORF) of 1434 bp. The full-length cDNA coding FBPase was 1314 bp with a 1014 bp ORF encoding 337 amino acids. Analyses of gene expression of GK and FBPase were conducted in gill, liver, the whole intestine, the whole kidney, heart, the dorsal white muscle and brain. The highest expression of GK was found in liver, followed by muscle. The expression of FBPase was found higher in liver than heart and gill. Both hepatic GK activity and mRNA expression were highly induced in turbot after being fed with dietary carbohydrates (p < 0.05). However, the GK activity and mRNA expression in the group with dietary glucose did not significantly differ from those in the group with dietary dextrin (p > 0.05). Compared with the control group, there were no significant differences in FBPase activity and mRNA expression in the glucose as well as dextrin group (p > 0.05). The increased hepatic GK activity and gene expression indicated that the first step of glycolysis was activated in turbot by dietary carbohydrates.

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References

  • Borrebaek B, Christophersen B (2000) Hepatic glucose phosphorylating activities in perch (Perca fluviatilis) after different dietary treatments. Comp Biochem Phys B 125:387–393

    Article  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Capilla E, Médale F, Navarro I, Panserat S, Vachot C, Kaushik S, Gutiérrez J (2003) Muscle insulin binding and plasma levels in relation to liver glucokinase activity, glucose metabolism and dietary carbohydrates in rainbow trout. Regul Pept 110:123–132

    Article  CAS  PubMed  Google Scholar 

  • Caseras A, Metón I, Fernández F, Baanante IV (2000) Glucokinase gene expression is nutritionally regulated in liver of gilthead sea bream (Sparus aurata). BBA Gene Struct Expr 1493:135–141

    Article  CAS  Google Scholar 

  • Caseras A, Metón I, Vives C, Egea M, Fernández F, Baanante IV (2002) Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata). Br J Nutr 88:607–614

    Article  CAS  PubMed  Google Scholar 

  • El-Maghrabi MR, Lange AJ, Kümmel L, Pilkis SJ (1991) The rat fructose-1,6-bisphosphatase gene. J Boil Chem 266:2115–2120

    CAS  Google Scholar 

  • El-Maghrabi MR, Gidh-Jain M, Austin LR, Pilkis SJ (1993) Isolation of a human liver fructose-1,6-bisphosphatase cDNA and expression of the protein in Escherichia coli. J Boil Chem 268:9466–9472

    CAS  Google Scholar 

  • Enes P, Panserat S, Kaushik S, Oliva-Teles A (2006a) Effect of normal and waxy maize starch on growth, food utilization and hepatic glucose metabolism in European sea bass (Dicentrarchus labrax) juveniles. Comp Biochem Phys A 143:89–96

    Article  CAS  Google Scholar 

  • Enes P, Panserat S, Kaushik S, Oliva-Teles A (2006b) Rapid metabolic adaptation in European sea bass (Dicentrarchus labrax) juveniles fed different carbohydrate sources after heat shock stress. Comp Biochem Phys A 145:73–81

    Article  CAS  Google Scholar 

  • Enes P, Panserat S, Kaushik S, Oliva-Teles A (2008) Growth performance and metabolic utilization of diets with native and waxy maize starch by gilthead sea bream (Sparus aurata) juveniles. Aquaculture 274:101–108

    Article  CAS  Google Scholar 

  • Fernández F, Miquel AG, Córdoba M, Varas M, Metón I, Caseras A, Baanante IV (2007) Effects of diets with distinct protein-to-carbohydrate ratios on nutrient digestibility, growth performance, body composition and liver inter-mediary enzyme activities in gilthead sea bream (Sparus aurata, L.) fingerlings. J Exp Mar Biol Ecol 343:1–10

    Article  Google Scholar 

  • Garcia-Riera MP, Hemre GI (1996) Glucose tolerance in turbot, Scophthalmus maximus (L.). Aquac Nutr 2:117–120

    Article  CAS  Google Scholar 

  • Gong G, Xue M, Wang J, Su X O, Wu X F, Zheng Y H, Han F (2013) Cloning and sequence analysis of full length cDNA of key enzymes of gluconeogenesis in Siberian Sturgeon (Acipenser baerii). Chin J Anim Nutr 25(7):1504–1518 (in Chinese with English abstract)

  • Gouillou-Coustans MF, Fournier V, Métailler R, Vachot C, Desbruyères E, Huelvan C, Moriceau J, Delliou HL, Kaushik SJ (2002) Dietary arginine degradation is a major pathway in ureagenesis in juvenile turbot (Psetta maxima). Comp Biochem Phys A 132:305–319

    Article  CAS  Google Scholar 

  • Hemre GI, Mommsen TP, Krogdahl Å (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194

  • Iynedjian PB (2009) Molecular physiology of mammalian glucokinase. Cell Mol Life Sci 66:27–42

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jafri AK (1995) Protein-sparing effect of dietary carbohydrate in diets for fingerling Labeo rohita. Aquaculture 136(3):331–339

    Google Scholar 

  • Kirchner S, Kaushik S, Panserat S (2003) Low protein intake is associated with reduced hepatic gluconeogenic enzyme expression in rainbow trout (Oncorhynchus mykiss). J Nutr 133:2561–2564

    CAS  PubMed  Google Scholar 

  • Kirchner S, Panserat S, Lim PL, Kaushik S, Ferraris RP (2008) The role of hepatic, renal and intestinal gluconeogenic enzymes in glucose homeostasis of juvenile rainbow trout. J Comp Physiol B 178:429–438

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Mahalingam B, Cuesta-Munoz A, Davis EA, Matschinsky FM, Harrison RW, Weber IT (1999) Structural model of human glucokinase in complex with glucose and ATP. Diabetes 48:1698–1705

    Article  CAS  PubMed  Google Scholar 

  • Metón I, Caseras A, Fernández F, Baanante IV (2004) Molecular cloning of hepatic glucose-6-phosphatase catalytic subunit from gilthead sea bream (Sparus aurata): response of its mRNA levels and glucokinase expression to refeeding and diet composition. Comp Biochem Phys B 138:145–153

    Article  Google Scholar 

  • Miao SY, Nie Q, Miao HJ, Zhang WB, Mai KS (2013) Effects of different carbohydrate sources and levels on growth performance and metabolic response of juvenile turbot Scophthalmus maximus. J Fish China 37(6):910–919 (in Chinese with English abstract)

    Article  Google Scholar 

  • Moreira IS, Peres H, Couto A, Enes P, Oliva-Teles A (2008) Temperature and dietary carbohydrate level effects on performance and metabolic utilisation of diets in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 274:153–160

    Article  CAS  Google Scholar 

  • Nie Q, Miao HJ, Miao SY, Chen CY, Li J, Zhang WB, Mai KS (2013) Effects of dietary carbohydrate sources and levels on the activities of carbohydrate metabolic enzymes in turbot Scophthalmus maximus L. Acta Hydrobiol Sin 37(3):425–433 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Okar DA, Lange AJ (1999) Fructose-2, 6-bisphosphate and control of carbohydrate metabolism in eukaryotes. Biofactors 10(1):1–14

  • Panserat S, Médale F, Blin C, Brèque J, Vachot C, Plagnes-Juan E, Gomes E, Krishnamoorthy R, Kaushik S (2000) Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilthead seabream, and common carp. Am J Physiol Regul Integr Comp Physiol 278:R1164–R1170

    CAS  PubMed  Google Scholar 

  • Panserat S, Capilla E, Gutierrez J, Frappart PO, Vachot C, Plagnes Juan E, Aguirre P, Breque J, Kaushik S (2001) Glucokinase is highly induced and glucose-6-phosphatase poorly repressed in liver of rainbow trout (Oncorhynchus mykiss) by a single meal with glucose. Comp Biochem Physiol B 128:275–283

    Article  CAS  PubMed  Google Scholar 

  • Panserat S, Plagnes-Juan E, Kaushik S (2002) Gluconeogenic enzyme gene expression is decreased by dietary carbohydrates in common carp (Cyprinus carpio) and gilthead seabream (Sparus aurata). BBA Gene Struct Expr 1579:35–42

    Article  CAS  Google Scholar 

  • Panserat S, Rideau N, Polakof S (2014) Nutritional regulation of glucokinase: a cross-species story. Nutr Res Rev 27:21–47

    Article  CAS  PubMed  Google Scholar 

  • Polakof S, Míguez JM, Soengas J (2008) Dietary carbohydrates induce changes in glucosensing capacity and food intake of rainbow trout. Am J Physiol Reg I 295:478–489

    Google Scholar 

  • Regost C, Arzel J, Cardinal M, Robin J, Laroche M, Kaushik SJ (2001) Dietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture 193:291–309

    Article  CAS  Google Scholar 

  • Stein S, Liehr T, Eschrich K (2001) Characterization of the mouse liver fructose-1,6-bisphosphatase gene. Gene 264:215–224

    Article  CAS  PubMed  Google Scholar 

  • Tanizawa Y, Koranyi LI, Welling CM, Permutt MA (1991) Human liver glucokinase gene: cloning and sequence determination of two alternatively spliced cDNAs. Proc Natl Acad Sci USA 88(16):7294–7297

  • Tillmann H, Bernhard D, Eschrich K (2002) Fructose-1,6-bisphosphatase genes in animals. Gene 291:57–66

    Article  CAS  PubMed  Google Scholar 

  • Tranulis MA, Dregni O, Christophersen B, Krogdahl A, Borrebaek B (1996) A glucokinase-like-enzyme in the liver of Atlantic salmon (Salmo salar). Comp Biochem Physiol B 114:35–39

    Article  CAS  PubMed  Google Scholar 

  • Van Ham EH, Berntssen MHG, Imsland AK, Parpoura AC, Wendelaar Bonga SE, Stefansson SO (2003) The influence of temperature and ration on growth, feed conversion, body composition and nutrient retention of juvenile turbot (Scophthalmus maximus). Aquaculture 217:547–558

    Article  Google Scholar 

  • Veiga-da-Cunha M, Courtois S, Michel A, Gosselain E, Schaftingen EV (1996) Amino acid conservation in animal glucokinases. J Biol Chem 27:6292–6297

    Google Scholar 

  • Zhang Y, Liang JY, Huang S, Ke H, Lipscomb WN (1993) Crystallographic studies of the catalytic mechanism of the neutral form of fructose-1, 6-bisphosphatase. Biochemistry 32:1844–1857

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was financially supported by the National Basic Research Program (973 Program, No. 2014CB138600) and the National Natural Science Foundation of China (No. 31072219).

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Correspondence to Wenbing Zhang.

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Nie, Q., Miao, H., Miao, S. et al. Effects of dietary glucose and dextrin on activity and gene expression of glucokinase and fructose-1,6-bisphosphatase in liver of turbot Scophthalmus maximus . Fish Physiol Biochem 41, 819–832 (2015). https://doi.org/10.1007/s10695-015-0049-6

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  • DOI: https://doi.org/10.1007/s10695-015-0049-6

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