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Fish Physiology and Biochemistry

, Volume 45, Issue 1, pp 401–415 | Cite as

Glucose-6-phosphate dehydrogenase in blunt snout bream Megalobrama amblycephala: molecular characterization, tissue distribution, and the responsiveness to dietary carbohydrate levels

  • Guang-Zhen Jiang
  • Hua-Juan Shi
  • Chao Xu
  • Ding-Dong Zhang
  • Wen-Bin Liu
  • Xiang-Fei LiEmail author
Article

Abstract

This study aimed to characterize the full-length cDNA of glucose-6-phosphate dehydrogenase (G6PD) from Megalobrama amblycephala with its responses to dietary carbohydrate levels characterized. The cDNA obtained covered 2768 bp with an open reading frame of 1572 bp. Sequence alignment and phylogenetic analysis revealed a high degree of conservation (77–97%) among most fish and other higher vertebrates. The highest transcription of G6PD was observed in kidney followed by liver, whereas relatively low abundance was detected in eye. Then, the transcriptions and activities of G6PD as well as lipid contents were determined in the liver, muscle, and the adipose tissue of fish fed two dietary carbohydrate levels (30 and 42%) for 12 weeks. Hepatic transcriptions of fatty acid synthetase (FAS), acetyl-CoA carboxylase α (ACCα), sterol regulatory element-binding protein-1 (SREBP1), and peroxisome proliferator-activated receptor γ (PPARγ) were also measured to corroborate the lipogenesis derived from carbohydrates. The G6PD expressions and activities in both liver and the adipose tissue as well as the lipid contents in whole-body, liver, and the adipose tissue all increased significantly after high-carbohydrate feeding. Hepatic transcriptions of FAS, ACCα, SREBP1, and PPARγ were also up-regulated remarkably by the intake of a high-carbohydrate diet. These results indicated that the G6PD of M. amblycephala shared a high similarity with that of other vertebrates. Its expressions and activities in tissues were both highly inducible by high-carbohydrate feeding, as also held true for the transcriptions of other enzymes and/or transcription factors involved in lipogenesis, evidencing an enhanced lipogenesis by high dietary carbohydrate levels.

Keywords

Glucose-6-phosphate dehydrogenase Gene cloning Transcriptional analysis Carbohydrate levels Megalobrama amblycephala 

Notes

Funding information

This research was funded by the Earmarked Fund for China Agriculture Research System (CARS-45-14) and the Fundamental Research Funds for the Central Universities in China (KJQN201708).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. AOAC (1995) Agricultural chemicals, contaminants, drugs. In: Official methods of analysis of AOAC International. AOAC International, Arlington, p 1298Google Scholar
  2. Bautista JM, Garrido-Pertierra A, Soler G (1988) Glucose-6-phosphate dehydrogenase from Dicentrarchus labrax liver: kinetic mechanism and kinetics of NADPH inhibition. Biochim Biophys Acta 967(3):354–363.  https://doi.org/10.1016/0304-4165(88)90098-0 Google Scholar
  3. Beydemir Ş, Gülçin İ, Hisar O, Küfrevioğlu Öİ, Yanik T (2005) Effect of melatonin on glucose-6-phosphate dehydrogenase from rainbow trout (Oncorhynchus mykiss) erythrocytes in vitro and in vivo. J Appl Anim Res 28(1):65–68.  https://doi.org/10.1080/09712119.2005.9706791 Google Scholar
  4. Blasco J, Fernández-Borrás J, Marimón I, Requena A (1996) Plasma glucose kinetics and tissue uptake in brown trout in vivo: effect of an intravascular glucose load. J Comp Physiol B 165(7):534–541.  https://doi.org/10.1007/BF00387514 Google Scholar
  5. Blasco J, Marimón I, Viaplana I, Fernández-Borrás J (2001) Fate of plasma glucose in tissues of brown trout in vivo: effects of fasting and glucose loading. Fish Physiol Biochem 24(3):247–258.  https://doi.org/10.1023/A:101408431 Google Scholar
  6. Bou M, Todorčević M, Fontanillas R, Capilla E, Gutiérrez J, Navarro I (2014) Adipose tissue and liver metabolic responses to different levels of dietary carbohydrates in gilthead sea bream (Sparus aurata). Comp Biochem Physiol A Mol Integr Physiol 175(1):72–81.  https://doi.org/10.1016/j.cbpa.2014.05.014 Google Scholar
  7. Brown MS, Ye J, Rawson RB, Goldstein JL (2000) Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100(4):391–398.  https://doi.org/10.1016/S0092-8674(00)80675-3 Google Scholar
  8. Cappellini MD, Fiorelli G (2008) Glucose-6-phosphate dehydrogenase deficiency. Lancet 371(9606):64–74.  https://doi.org/10.1016/S0140-6736(08)60073-2 Google Scholar
  9. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325(5942):834–840.  https://doi.org/10.1126/science.1175371 Google Scholar
  10. Ciardiello MA, Camardella L, Carratore V, di Prisco G (1997) Enzymes in Antarctic fish: glucose-6-phosphate dehydrogenase and glutamate dehydrogenase. Comp Biochem Physiol A Physiol 118(4):1031–1036.  https://doi.org/10.1016/S0300-9629(97)86791-6 Google Scholar
  11. Ciesla J, Fraczyk T, Rode W (2011) Phosphorylation of basic amino acid residues in proteins: important but easily missed. Acta Biochim Pol 58(2):137–147Google Scholar
  12. Çiftçi M, Beydemir Ş, Yılmaz H, Altıkat S (2003) Purification of glucose 6-phosphate dehydrogenase from Buffalo (Bubalus bubalis) erythrocytes and investigation of some kinetic properties. Protein Expr Purif 29(2):304–310.  https://doi.org/10.1016/S1046-5928(03)00073-1 Google Scholar
  13. Ciftci M, Ciltas A, Erdogan O (2004) Purification and characterization of glucose 6-phosphate dehydrogenase from rainbow trout (Oncorhynchus mykiss) erythrocytes. Vet Med Czech 49(2):327–333.  https://doi.org/10.1016/S1046-5928(03)00073-1 Google Scholar
  14. Couto A, Enes P, Peres H, Oliva-Teles A (2008) Effect of water temperature and dietary starch on growth and metabolic utilization of diets in gilthead sea bream (Sparus aurata) juveniles. Comp Biochem Physiol A Mol Integr Physiol 151(1):45–50.  https://doi.org/10.1016/j.cbpa.2008.05.013 Google Scholar
  15. Craig PM, Moon TW (2013) Methionine restriction affects the phenotypic and transcriptional response of rainbow trout (Oncorhynchus mykiss) to carbohydrate-enriched diets. Brit J Nutr 109(3):402–412.  https://doi.org/10.1017/S0007114512001663 Google Scholar
  16. Deane EE, Woo NYS (2005) Expression studies on glucose-6-phosphate dehydrogenase in sea bream: effects of growth hormone, somatostatin, salinity and temperature. J Exp Zool A 303((8):676–688.  https://doi.org/10.1002/jez.a.201 Google Scholar
  17. Ekmann KS, Dalsgaard J, Holm J, Campbell PJ, Skov PV (2013) Glycogenesis and de novo lipid synthesis from dietary starch in juvenile gilthead sea bream (Sparus aurata) quantified with stable isotopes. Brit J Nutr 109(12):2135–2146.  https://doi.org/10.1017/S000711451200445X Google Scholar
  18. 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(1):101–108.  https://doi.org/10.1016/j.aquaculture.2007.11.009 Google Scholar
  19. Enes P, Sanchez-Gurmaches J, Navarro I, Gutiérrez J, Oliva-Teles A (2010) Role of insulin and IGF-I on the regulation of glucose metabolism in European sea bass (Dicentrarchus labrax) fed with different dietary carbohydrate levels. Comp Biochem Physiol A Mol Integr Physiol 157(4):346–353.  https://doi.org/10.1016/j.cbpa.2010.08.006 Google Scholar
  20. Erdoğan O, Hisar O, Köroğlu G, Çiltaş A (2005) Sublethal ammonia and urea concentrations inhibit rainbow trout (Oncorhynchus mykiss) erythrocyte glucose-6-phosphate dehydrogenase. Comp Biochem Physiol C 141(2):145–150.  https://doi.org/10.1016/j.cca.2005.05.013 Google Scholar
  21. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of the total lipid from animal tissue. J Biol Chem 226(1):497–509Google Scholar
  22. Garrett RH, Grisham CM (1996) Biochemistry. Harcourt, Brace & Company, San Diego, p 762Google Scholar
  23. Hemre GI, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8(3):175–194.  https://doi.org/10.1046/j.1365-2095.2002.00200.x Google Scholar
  24. Hu W, Zhi L, Zhuo MQ, Zhu QL, Zheng JL, Chen QL, Gong Y, Liu CX (2013) Purification and characterization of glucose 6-phosphate dehydrogenase (G6PD) from grass carp (Ctenopharyngodon idella) and inhibition effects of several metal ions on G6PD activity in vitro. Fish Physiol Biochem 39(3):637–647.  https://doi.org/10.1007/s10695-012-9726-x Google Scholar
  25. Jiang YY, Li XF, Liu WB, Li HY, He JX (2016) Growth performance, body composition and plasma biochemical parameters of blunt snout bream (Megalobrama amblycephala) yearlings fed practical diets differing in carbohydrate levels. J Nanjing Agric Univ 39(2):281–288 (In Chinese with English Abstract).  https://doi.org/10.7685/jnau.201506002 Google Scholar
  26. Jin J, Médale F, Kamalam BS, Aguirre P, Véron V, Panserat S (2014) Comparison of glucose and lipid metabolic gene expressions between fat and lean lines of rainbow trout after a glucose load. PLoS One 9(8):e105548.  https://doi.org/10.1371/journal.pone.0105548 Google Scholar
  27. Kamalam BS, Medale F, Kaushik S, Polakof S, Skiba-Cassy S, Panserat S (2012) Regulation of metabolism by dietary carbohydrates in two lines of rainbow trout divergently selected for muscle fat content. J Exp Biol 215(15):2567–2578.  https://doi.org/10.1242/jeb.070581 Google Scholar
  28. Katsurada A, Iritani N, Fukuda H, Matsumura Y, Noguchi T, Tanaka T (1989) Effects of nutrients and insulin on transcriptional and post-transcriptional regulation of glucose-6-phosphate dehydrogenase synthesis in rat liver. Biochim Biophys Acta 1006(1):104–110.  https://doi.org/10.1016/0005-2760(89)90329-9 Google Scholar
  29. Kirchner S, Seixas P, Kaushik S, Panserat S (2005) Effects of low protein intake on extra-hepatic gluconeogenic enzyme expression and peripheral glucose phosphorylation in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B Biochem Mol Biol 140(2):333–340.  https://doi.org/10.1016/j.cbpc.2004.10.019 Google Scholar
  30. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9(4):299–306.  https://doi.org/10.1093/bib/bbn017 Google Scholar
  31. Kuzu M, Aslan A, Ahmed I, Comakli V, Demirdag R, Uzun N (2016) Purification of glucose-6-phosphate dehydrogenase and glutathione reductase enzymes from the gill tissue of Lake Van fish and analyzing the effects of some chalcone derivatives on enzyme activities. Fish Physiol Biochem 42:483–491.  https://doi.org/10.1007/s10695-015-0153-7 Google Scholar
  32. Lesk AM (1995) NAD-binding domains of dehydrogenases. Curr Opin Struct Biol 5(6):775–783.  https://doi.org/10.1016/0959-440X(95)80010-7 Google Scholar
  33. Li XF, Liu WB, Lu KL, Xu WN, Wang Y (2012) Dietary carbohydrate/lipid ratios affect stress, oxidative status and non-specific immune responses of fingerling blunt snout bream, Megalobrama amblycephala. Fish Shellfish Immun 33(2):316–323.  https://doi.org/10.1016/j.fsi.2012.05.007 Google Scholar
  34. Li XF, Wang Y, Liu WB, Jiang GZ, Zhu J (2013) Effects of dietary carbohydrate/lipid ratios on growth performance, body composition and glucose metabolism of fingerling blunt snout bream Megalobrama amblycephala. Aquac Nutr 19(5):701–708.  https://doi.org/10.1111/anu.12017 Google Scholar
  35. Li XF, Lu KL, Liu WB, Jiang GZ, Xu WN (2014) Effects of dietary lipid and carbohydrate and their interaction on growth performance and body composition of juvenile blunt snout bream, Megalobrama amblycephala. Isr J Aquacult Bamidgeh 66(1):931 http://hdl.handle.net/10524/49111 Google Scholar
  36. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408.  https://doi.org/10.1006/meth.2001.1262 Google Scholar
  37. Mason PJ, Stevens DJ, Luzzatto L, Brenner S, Aparicio S (1995) Genomic structure and sequence of the Fugu rubripes glucose-6-phosphate dehydrogenase gene (G6PD). Genomics 26(3):587–591.  https://doi.org/10.1016/0888-7543(95)80179-P Google Scholar
  38. Moon TW (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B Biochem Mol Biol 129:243–249.  https://doi.org/10.1016/S1096-4959(01)00316-5 Google Scholar
  39. Panserat S, Kaushik SJ (2010) Regulation of gene expression by nutritional factors in fish. Aquac Res 41(5):751–762.  https://doi.org/10.1111/j.1365-2109.2009.02173.x Google Scholar
  40. Panserat S, Plagnes-Juan E, Kaushik S (2001) Nutritional regulation and tissue specificity of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204(13):2351–2360Google Scholar
  41. Panserat S, Skiba-Cassy S, Seiliez I, Lansard M, Plagnes-Juan E, Vachot C, Aguirre P, Larroquet L, Chavernac G, Medale F, Corraze G, Kaushik S, Moon TW (2009) Metformin improves postprandial glucose homeostasis in rainbow trout fed dietary carbohydrates: a link with the induction of hepatic lipogenic capacities? Am J Phys Regul Integr Comp Phys 297(2):707–715.  https://doi.org/10.1152/ajpregu.00120.2009 Google Scholar
  42. Polakof S, Alvarez R, Soengas JL (2010a) Gut glucose metabolism in rainbow trout: implications in glucose homeostasis and glucosensing capacity. Am J Phys Regul Integr Comp Phys 299(1):19–32.  https://doi.org/10.1152/ajpregu.00005.2010 Google Scholar
  43. Polakof S, Moon TW, Aguirre P, Skiba-Cassy S, Panserat S (2010b) Effects of insulin infusion on glucose homeostasis and glucose metabolism in rainbow trout fed a high-carbohydrate diet. J Exp Biol 213(24):4151–4157.  https://doi.org/10.1242/jeb.050807 Google Scholar
  44. Polakof S, Panserat S, Soengas JL, Moon TW (2012) Glucose metabolism in fish: a review. J Comp Physiol B 182(8):1015–1045.  https://doi.org/10.1007/s00360-012-0658-7 Google Scholar
  45. Polevoda B, Sherman F (2003) N-Terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J Mol Biol 325(24):595–622.  https://doi.org/10.1016/S0022-2836(02)01269-X Google Scholar
  46. Prathomya P, Prisingkorn W, Jakovlić I, Deng FY, Zhao YH, Wang WM (2017) 1H NMR-based metabolomics approach reveals metabolic alterations in response to dietary imbalances in Megalobrama amblycephala. Metabolomics 13:17.  https://doi.org/10.1007/s11306-016-1158-7 Google Scholar
  47. Qian Y, Li XF, Zhang DD, Cai DS, Tian HY, Liu WB (2015) Effects of dietary pantothenic acid on growth, intestinal function, anti-oxidative status and fatty acids synthesis of juvenile blunt snout bream Megalobrama amblycephala. PLoS One 10(3):e0119518.  https://doi.org/10.1371/journal.pone.0119518 Google Scholar
  48. Qiang J, Yang H, He J, Wang H, Zhu ZX, Xu P (2014) Comparative study of the effects of two high-carbohydrate diets on growth and hepatic carbohydrate metabolic enzyme responses in juvenile gift tilapia (Oreochromis niloticus). Turk J Fish Aquat Sci 14(2):515–525.  https://doi.org/10.4194/1303-2712-v14_2_23 Google Scholar
  49. Rosemeyer MA (1987) The biochemistry of glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase and glutathione reductase. Cell Biochem Funct 5(2):79–95.  https://doi.org/10.1002/cbf.290050202 Google Scholar
  50. Sanden M, Frøyland L, Hemre GI (2003) Modulation of glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase and malic enzyme activity by glucose and alanine in Atlantic salmon, Salmo salar L. hepatocytes. Aquaculture 221(1–4):469–480.  https://doi.org/10.1016/S0044-8486(03)00077-2 Google Scholar
  51. Şentürk M, Ceyhun SB, Erdoğan O, Küfrevioğlu Öİ (2009) In vitro and in vivo effects of some pesticides on glucose-6-phosphate dehydrogenase enzyme activity from rainbow trout (Oncorhynchus mykiss) erythrocytes. Pestic Biochem Phys 95(2):95–99.  https://doi.org/10.1016/j.pestbp.2009.07.005
  52. Sheridan MA, Mommsen TP (1991) Effects of nutritional state on in vivo lipid and carbohydrate metabolism of coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 81(3):473–483.  https://doi.org/10.1016/0016-6480(91)90175-6
  53. Slenzka K, Appel R, Rahmann H (1995) Development and altered gravity dependent changes in glucose-6-phosphate dehydrogenase activity in the brain of the cichlid fish Oreochromis mossambicus. Neurochem Int 26(6):579–585.  https://doi.org/10.1016/0197-0186(94)00176-U Google Scholar
  54. Topal A, Atamanalp M, Oruç E, Kırıcı M, Kocaman EM (2014) Apoptotic effects and glucose-6-phosphate dehydrogenase responses in liver and gill tissues of rainbow trout treated with chlorpyrifos. Tissue Cell 46(6):490–496.  https://doi.org/10.1016/j.tice.2014.09.001 Google Scholar
  55. Walczak R, Tontonoz P (2002) PPARadigms and PPARadoxes: expanding roles for PPARγ in the control of lipid metabolism. J Lipid Res 43(2):177–186Google Scholar
  56. Wang XT, Chan TF, Lam VM, Engel PC (2008) What is the role of the second “structural” NADP+-binding site in human glucose 6-phosphate dehydrogenase? Protein Sci 17(8):1403–1411.  https://doi.org/10.1110/ps.035352.108 Google Scholar
  57. Wang BK, Liu WB, Xu C, Cao XF, Zhong XQ, Shi HJ, Li XF (2017) Dietary carbohydrate levels and lipid sources modulate the growth performance, fatty acid profiles and intermediary metabolism of blunt snout bream Megalobrama amblycephala in an interactive pattern. Aquaculture 481:140–153.  https://doi.org/10.1016/j.aquaculture.2017.08.034 Google Scholar
  58. Wilson RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124(1–4):67–80.  https://doi.org/10.1016/0044-8486(94)90363-8 Google Scholar
  59. Xu C, Liu WB, Dai YJ, Jiang GZ, Wang BK, Li XF (2017) Long-term administration of benfotiamine benefits the glucose homeostasis of juvenile blunt snout bream Megalobrama amblycephala fed a high-carbohydrate diet. Aquaculture 470:74–83.  https://doi.org/10.1016/j.aquaculture.2016.12.025 Google Scholar
  60. Xu C, Liu WB, Zhang DD, Cao XF, Shi HJ, Li XF (2018) Interactions between dietary carbohydrate and metformin: implications on energy sensing, insulin signaling pathway, glycolipid metabolism and glucose tolerance in blunt snout bream Megalobrama amblycephala. Aquaculture 483:183–195.  https://doi.org/10.1016/j.aquaculture.2017.10.022 Google Scholar
  61. Zar JH (1984) Biostatistical analysis. Prentice-Hall Inc., Englewood CliffsGoogle Scholar
  62. Zhang J, Wei XL, Chen LP, Chen N, Li YH, Wang WM, Wang HL (2013) Sequence analysis and expression differentiation of chemokine receptor CXCR4b among three populations of Megalobrama amblycephala. Dev Comp Immunol 40(2):195–201.  https://doi.org/10.1016/j.dci.2013.01.011 Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Key Laboratory of Aquaculture Nutrition and Feed Science of Jiangsu Province, College of Animal Science and TechnologyNanjing Agricultural UniversityNanjingPeople’s Republic of China

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