Advertisement

Fish Physiology and Biochemistry

, Volume 44, Issue 3, pp 869–883 | Cite as

Molecular characterization and identification of facilitative glucose transporter 2 (GLUT2) and its expression and of the related glycometabolism enzymes in response to different starch levels in blunt snout bream (Megalobrama amblycephala)

  • Hualiang Liang
  • Ahmed Mokrani
  • Hopeson Chisomo-Kasiya
  • Ogwok-Manas Wilson-Arop
  • Haifeng Mi
  • Ke Ji
  • Xianping Ge
  • Mingchun Ren
Article

Abstract

Facilitative glucose transporters (GLUT) are transmembrane transporters involved in glucose transport across the plasma membrane. In this study, blunt snout bream GLUT2 gene was cloned, and its expression in various tissues and in liver in response to diets with different carbohydrate levels (17.1; 21.8; 26.4; 32.0; 36.3; and 41.9% of dry matter). Blunt snout bream GLUT2 was also characterized. A full-length cDNA fragment of 2577 bp was cloned, which contains a 5′-untranslated region (UTR) of 73 bp, a 3′-UTR of 992 bp, and an open reading frame of 1512 bp that encodes a polypeptide of 503 amino acids with predicted molecular mass of 55.046 kDa and theoretical isoelectric point was 7.52. The predicted GLUT2 protein has 12 transmembrane domains between amino acid residues at 7–29; 71–93; 106–123; 133–155; 168–190; 195–217; 282–301; 316–338; 345–367; 377–399; 412–434; and 438–460. Besides, the conservative structure domains located at 12–477 amino acids belong to the sugar porter family which is the major facilitator superfamily (MFS) of transporters. Blunt snout bream GLUT2 had the high degree of sequence identity to four GLUT2s from zebrafish, chicken, human, and mouse, with 91, 63, 57, and 54% identity, respectively. Quantitative real-time (qRT) PCR assays revealed that GLUT2 expression was high in the liver, intestine, and kidney; highest in the liver and was regulated by carbohydrate intake. Compared with the control group (17.1%), fed by 3 h with higher starch levels (32.0; 36.3; and 41.9%), increased plasma glucose levels and glycemic level went back to basal by 24 h after treatment. Furthermore, higher dietary starch levels significantly increase GLUT2, glucokinase (GK), and pyruvate kinase (PK) expression and concurrently decrease phosphoenolpyruvate carboxykinase (PEPCK) and glucose-6-phosphatase (G6P) mRNA levels (P < 0.05), and these changes were also back to basal levels after 24 h of any dietary treatment. These results indicate that the blunt snout bream is able to regulate their ability to metabolize glucose by improving GLUT2, GK, and PK expression levels and decreasing PEPCK and G6P expression levels.

Keywords

Blunt snout bream Glucose transporter 2 Glycometabolism Starch 

Notes

Acknowledgements

We thank Ahmed Mokrani and Hopeson Chisomo-Kasiya for checking and revising our manuscript.

Funding information

This study was financially supported by the National Natural Science Foundation of Jiangsu Province (BK20161143), the Natural Science Foundation of China, NSFC (31772820), and the Modern Agriculture Industrial Technology System special project—the National Technology System for Conventional Freshwater Fish Industries (CARS-45).

Compliance with ethical standards

The handling of the experimental animal (pre-adult blunt snout bream) is based on the Ministry of Agriculture, China, and international animal welfare laws, guidelines, and policies (FAO 2004).

References

  1. Barron CC, Bilan PJ, Tsakiridis T, Tsiani E (2016) Facilitative glucose transporters: implications for cancer detection, prognosis and treatment. Metabolism 65(2):124–139.  https://doi.org/10.1016/j.metabol.2015.10.007 CrossRefPubMedGoogle Scholar
  2. Bergot F (1979a) Effects of dietary carbohydrate and of their mode of distribution on glycaemia in rainbow trout (Salmo gairdneri, Richardson). Comp Biochem Physiol A 64(4):543–547.  https://doi.org/10.1016/0300-9629(79)90581-4 CrossRefGoogle Scholar
  3. Bergot F. (1979b) Carbohydrate in rainbow trout diets: effects of the level and source of carbohydrate and the number of meals on growth and body composition. Aquaculture 18(2):157-167.CrossRefGoogle Scholar
  4. Brauge C, Corraze G, Me’dale F (1995) Effect of dietary levels of lipid and carbohydrate on growth performance, body composition, nitrogen excretion and plasma glucose levels in rainbow trout reared at 8 or 18°C. Reprod Nutr Dev 35(3):277–290.  https://doi.org/10.1051/rnd:19950304 CrossRefPubMedGoogle Scholar
  5. 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(06):607–614.  https://doi.org/10.1079/BJN2002701 CrossRefPubMedGoogle Scholar
  6. Castillo J, Crespo D, Capilla E, Diaz M, Chauvigne F, Cerda J, Planas JV (2009) Evolutionary structural and functional conservation of an ortholog of the GLUT2 glucose transporter gene (SLC2A2) in zebrafish. Am J Physiol Regul Integr Comp Physiol 297:R1570–R1581CrossRefPubMedGoogle Scholar
  7. Cournarie F, Azzout-Marniche D, Foretz M, Guichard C, Ferre P, Foufelle F (1999) The inhibitory effect of glucose on phosphoenolpyruvate carboxykinase gene expression in cultured hepatocytes is transcriptional and requires glucose metabolism. FEBS Lett 460(3):527–532.  https://doi.org/10.1016/S0014-5793(99)01407-6 CrossRefPubMedGoogle Scholar
  8. Deng DF, Refstie S, Hung SSO (2001) Glycemic and glycosuric responses in white sturgeon (Acipenser transmontanus) after oral administration of simple and complex carbohydrate. Aquaculture 199:107–117CrossRefGoogle Scholar
  9. Dias J, Rueda-Jasso R, Panserat S, da Conceição LEC, Gomes EF, Dinis MT (2004) Effect of dietary carbohydrate-to-lipid ratios on growth, lipid deposition and metabolic hepatic enzymes in juvenile Senegalese sole (Solea senegalensis, Kaup). Aquac Res 35(12):1122–1130.  https://doi.org/10.1111/j.1365-2109.2004.01135.x CrossRefGoogle Scholar
  10. Enes P, Panserat S, Kaushik S, Oliva-Teles A (2006) Effect of normal and waxy maize starch on growth, food utilization and hepatic glucose metabolism in European sea bass (Dicentrarchus labrax) juveniles. Comp Biochem Physiol A 143(1):89–96.  https://doi.org/10.1016/j.cbpa.2005.10.027 CrossRefGoogle Scholar
  11. FAO 2004 In: Spreij M (ed) National Aquaculture Legislation Overview—China. National Aquaculture Legislation Overview (NALO) Fact Sheets. FAO Fisheries and Aquaculture Department, Rome, Italy (http://www.fao.org/fishery/legalframework/nalo_china/en#tcNB0041)
  12. Feksa LR, Cornelio AR, Vargas CR (2003) Alanine prevents the inhibition of pyruvate kinase activity caused by tryptophan in cerebral cortex of rats. Metab Brain Dis 18(2):129–137.  https://doi.org/10.1023/A:1023811019023 CrossRefPubMedGoogle Scholar
  13. Ferre T, Riu E, Bosch F, Valera A (1996) Evidence from transgenic mice that glucokinase is rate limiting for glucose utilization in the liver. FASEB J 10(10):1213–1218.  https://doi.org/10.1096/fasebj.10.10.8751724 CrossRefPubMedGoogle Scholar
  14. Furuichi M, Yone Y (1981) Change of blood sugar and plasma insulin levels of fishes in glucose tolerance test. Bull Jpn Sot Sci Fish 47(6):761–764.  https://doi.org/10.2331/suisan.47.761 CrossRefGoogle Scholar
  15. Gao Z, Luo W, Liu H, Zeng C, Liu X, Yi S, Wang W (2012) Transcriptome analysis and SSR/SNP markers information of the blunt snout bream (Megalobrama amblycephala). PLoS One 7(8):e42637.  https://doi.org/10.1371/journal.pone.0042637 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Habte-Tsion HM, Ge XP, Liu B, Xie J, Ren MC, Zhou QL, Miao LH, Pan LK, Chen RL (2015) A deficiency or an excess of dietary threonine level affects weight gain, enzyme activity, immune response and immune-related gene expression in juvenile blunt snout bream (Megalobrama amblycephala). Fish Shellfish Immunol 42(2):439–446.  https://doi.org/10.1016/j.fsi.2014.11.021 CrossRefPubMedGoogle Scholar
  17. Hall JR, MacCormack TJ, Barry CA, Driezic WR (2004) Sequence and expression of a constitutive, facilitated glucose transporter (GLUT1) in Atlantic cod Gadus morhua. J Exp Biol 207(26):4697–4706.  https://doi.org/10.1242/jeb.01346 CrossRefPubMedGoogle Scholar
  18. Hall JR, Richards RC, MacCormack TJ, Ewart KV, Driezic WR (2005) Cloning of GLUT3 cDNA from Atlantic cod Gadus morhua and expression of GLUT1 and GLUT3 in response to hypoxia. Biochim Biophys Acta 1730(3):245–252.  https://doi.org/10.1016/j.bbaexp.2005.07.001 CrossRefPubMedGoogle Scholar
  19. Hall JR, Short CE, Driedzic WR (2006) Sequence of Atlantic cod (Gadus morhua) GLUT4, GLUT2 and GPDH: developmental stage expression, tissue expression and relationship to starvation-induced changes in blood glucose. J Exp Biol 209(22):4490–4502.  https://doi.org/10.1242/jeb.02532 CrossRefPubMedGoogle Scholar
  20. Hanson RW, Reshef L (1997) Regulation of phosphoenolpyruvate carboxykinase (GTP) gene expression. Annu Rev Biochem 66(1):581–611.  https://doi.org/10.1146/annurev.biochem.66.1.581 CrossRefPubMedGoogle Scholar
  21. James DE, Brown R, Navarro J, Pilch PF (1988) Insulin-regulatable tissues express a unique insulin sensitive glucose transport protein. Nature 333(6169):183–185.  https://doi.org/10.1038/333183a0 CrossRefPubMedGoogle Scholar
  22. Joost HG, Thorens B (2001) The extended GLUT-family of sugar/polyol transport facilitators: nomenclature, sequence characteristics, and potential function of its novel members. Mol Membr Biol 18(4):247–256.  https://doi.org/10.1080/09687680110090456 CrossRefPubMedGoogle Scholar
  23. Joost HG, Bell GI, Best JD, Birnbaum MJ, Charron MJ, Chen YT, Doege H, James DE, Lodish H, Moley KH, Moley JF, Mueckler M, Rogers S, Schurmann A, Seino S, Thorens B (2002) Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. Am J Physiol Endocrinol Metab 282(4):E974–E976.  https://doi.org/10.1152/ajpendo.00407.2001 CrossRefPubMedGoogle Scholar
  24. Kahn CR, Lauris V, Koch S, Crettaz M, Granner DK (1989) Acute and chronic regulation of phosphoenolpyruvate carboxykinase mRNA by insulin and glucose. Mol Endocrinol 3:840–845CrossRefPubMedGoogle Scholar
  25. Katsumata M, Burton KA, Li J, Dauncey MJ (1999) Suboptimal energy balance selectively up-regulates muscle GLUT gene expression but reduces insulin dependent glucose uptake during postnatal development. FASEB J 13(11):1405–1413.  https://doi.org/10.1096/fasebj.13.11.1405 CrossRefPubMedGoogle Scholar
  26. Kayano T, Fukumoto H, Eddy RL, Fan YS, Byers MG, Shows TB, Bell GI (1988) Evidence for a family of human glucose transporter-like proteins. Sequence and gene localization of a protein expressed in fetal skeletal muscle and other tissues. J Biol Chem 263(30):15245–15248PubMedGoogle Scholar
  27. Kellett GL (2001) The facilitated component of intestinal glucose absorption. J Physiol 531(3):585–595.  https://doi.org/10.1111/j.1469-7793.2001.0585h.x CrossRefPubMedPubMedCentralGoogle Scholar
  28. Krasnov A, Teerijoki H, Mölsä H (2001) Rainbow trout (Oncorhynchus mykiss) hepatic glucose transporter. Biochim Biophys Acta 1520(2):174–178.  https://doi.org/10.1016/S0167-4781(01)00258-5 CrossRefPubMedGoogle Scholar
  29. Legate NJ, Bonen A, Moon TW (2001) Glucose tolerance and peripheral glucose utilization in rainbow trout (Oncorhynchus mykiss), American eel (Anguilla rostrata), and black bullhead catfish (Ameiurus melas). Gen Comp Endocrinol 122:48–59CrossRefPubMedGoogle Scholar
  30. Leibiger B, Leibiger IB (1995) Functional analysis of DNA-elements involved in transcriptional control of the human glucose transporter 2 (GLUT 2) gene in the insulin-producing cell line βTC-3. Diabetologia 38(1):112–115.  https://doi.org/10.1007/BF02369360 CrossRefPubMedGoogle Scholar
  31. Li XF, Liu WB, Jiang YY, Zhu H, Ge XP (2010) Effects of dietary protein and lipid levels in practical diets on growth performance and body composition of blunt snout bream (Megalobrama amblycephala) fingerlings. Aquaculture 303(1):65–70.  https://doi.org/10.1016/j.aquaculture.2010.03.014 CrossRefGoogle Scholar
  32. Liang HL, Ren MC, Habte-Tsion HM, Ge XP, Xie J, Mi HF, Xi BW, Miao LH, Liu B, Zhou QL, Fang W (2016) Dietary arginine affects growth performance, plasma amino acid contents and gene expressions of the TOR signaling pathway in juvenile blunt snout bream, Megalobrama amblycephala. Aquaculture 461:1–8.  https://doi.org/10.1016/j.aquaculture.2016.04.009 CrossRefGoogle Scholar
  33. Likimani TA, Wilson RP (1982) Effects of diet on lipogenic enzyme activities in channel catfish hepatic and adipose tissue. J Nutr 112(1):112–117.  https://doi.org/10.1093/jn/112.1.112 CrossRefPubMedGoogle Scholar
  34. Lin SC, Liou CH, Shiau SY (2000) Renal threshold for urinary glucose excretion by tilapia in response to orally administered carbohydrates and injected glucose. Fish Physiol Biochem 3:127–132CrossRefGoogle Scholar
  35. Liu HL, Wang JT, Wan WJ, Fu PS, Sun MM, Wang HW (2014) Expression of glucose transporter 4 and glucose transporter 2 in different tissues of tilapia and its response to glucose injection. Chin J Anim Nutr 26(11):3500–3509Google Scholar
  36. Macheda ML, Rogers S, Best JD (2005) Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 202(3):654–662.  https://doi.org/10.1002/jcp.20166 CrossRefPubMedGoogle Scholar
  37. Massa ML, Gagliardino JJ, Francini F (2011) Liver glucokinase: an overview on the regulatory mechanisms of its activity. IUBMB Life 63(1):1–6.  https://doi.org/10.1002/iub.411 CrossRefPubMedGoogle Scholar
  38. Metón I, Mediavilla D, Caseras A, Cantó E, Fernández F, Baanante IV (1999) Effect of diet composition and ration size on key enzyme activities of glycolysis–gluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata). Br J Nutr 82(3):223–232PubMedGoogle Scholar
  39. Metón I, Fernández F, Baanante IV (2003) Short- and long-term effects of refeeding on key enzyme activities in glycolysis-gluconeogenesis in the liver of gilthead seabream (Sparus aurata). Aquaculture 225:99–107CrossRefGoogle Scholar
  40. Meyer S, Höppner W, Seitz HJ (1991) Transcriptional and post-transcriptional effects of glucose on liver phosphoenolpyruvate-carboxykinase gene expression. Eur J Biochem 202:985–991CrossRefPubMedGoogle Scholar
  41. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA, Kahn CR (2000) Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell 6(1):87–97.  https://doi.org/10.1016/S1097-2765(05)00015-8 CrossRefPubMedGoogle Scholar
  42. Ministry of Agriculture of the People’s Republic of China (2016) Chinese fisheries yearbook. Chinese Agricultural Press, Beijing.  https://doi.org/10.3390/jof2040034 CrossRefGoogle Scholar
  43. Miyamoto K, Hase K, Taketani Y, Minami H, Oka T, Nakabou Y, Hagihira H (1991) Diabetes and glucose transporter gene expression in rat small intestine. Biochem Biophys Res Commun 181(3):1110-1117.CrossRefPubMedGoogle Scholar
  44. Miyamoto K, Hase K, Takagi T, Fujii T, Taketani Y, Minami H, Oka T, Nakabou Y (1993) Differential responses of intestinal glucose transporter mRNA transcripts to levels of dietary sugars. Biochem J 295(1):211–215.  https://doi.org/10.1042/bj2950211 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mueckler M, Thorens B (2013) The SLC2 (GLUT) family of membrane transporters. Mol Asp Med 34(2-3):121–138.  https://doi.org/10.1016/j.mam.2012.07.001 CrossRefGoogle Scholar
  46. Mueckler M, Caruso C, Baldwin SA, Panico M, Blench I, Morris HR, Allard WJ, Lienhard GE, Lodish HF (1985) Sequence and structure of a human glucose transporter. Science 229(4717):941–945.  https://doi.org/10.1126/science.3839598 CrossRefPubMedGoogle Scholar
  47. Palmer TN, Ryman BE (1972) Studies on oral glucose intolerance in fish. J Fish Biol 4(2):311–319.  https://doi.org/10.1111/j.1095-8649.1972.tb05680.x CrossRefGoogle Scholar
  48. Panserat S, Médale F, Brèque J, Plagnes-Juan E, Kaushik S (2000a) Lack of significant long-term effect of dietary carbohydrate on hepatic glucose-6-phosphatase expression in rainbow trout (Oncorhynchus mykiss). J Nutr Biochem 11(1):22–29.  https://doi.org/10.1016/S0955-2863(99)00067-4 CrossRefPubMedGoogle Scholar
  49. Panserat S, Médale F, Blin C, Brèque J, Vachot C, Plagnes-Juan E, Gomes E, Krishnamoorthy R, Kaushik S (2000b) Hepatic glucokinase is induced by dietary carbohydrate in rainbow trout, gilthead seabream, and common carp. Am J Physiol Regul Integr Comp Physiol 278(5):R1164–R1170.  https://doi.org/10.1152/ajpregu.2000.278.5.R1164 CrossRefPubMedGoogle Scholar
  50. Panserat S, Plagnes-Juan E, Kaushik S (2001a) Nutritional regulation and tissue specificity of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204(Pt 13):2351–2360PubMedGoogle Scholar
  51. Panserat S, Plagnesjuan E, Brèque J, Kaushik S (2001b) Hepatic phosphoenolpyruvate carboxykinase gene expression is not repressed by dietary carbohydrate in rainbow trout (Oncorhynchus mykiss). J Exp Biol 204:359PubMedGoogle Scholar
  52. Panserat S, Plagnes-Juan E, Kaushik S (2002) Gluconeogenic enzyme gene expression is decreased by dietary carbohydrate in common carp (Cyprinus carpio) and gilthead seabream (Sparus aurata). Biochim Biophys Acta 1579(1):35–42.  https://doi.org/10.1016/S0167-4781(02)00501-8 CrossRefPubMedGoogle Scholar
  53. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007CrossRefGoogle Scholar
  54. Planas JV, Capilla E, Gutierrez J (2000) Molecular identification of a glucose transporter from fish muscle. FEBS Lett 481(3):266–270.  https://doi.org/10.1016/S0014-5793(00)02020-2 CrossRefPubMedGoogle Scholar
  55. Ren MC, Ai QH, Mai KS, Ma HM, Wang XJ (2011) Effect of dietary carbohydrate level on growth performance, body composition, apparent digestibility coefficient and digestive enzyme activities of juvenile cobia, Rachycentron canadum L. Aquac Res 42(10):1467–1475.  https://doi.org/10.1111/j.1365-2109.2010.02739.x CrossRefGoogle Scholar
  56. Ren MC, Liao YJ, Xie J, Liu B, Zhou QL, Ge XP, Cui HH, Pan LK, Chen RL (2013) Dietary arginine requirement of juvenile blunt snout bream, Megalobrama amblycephala. Aquaculture 414-415:229–234.  https://doi.org/10.1016/j.aquaculture.2013.08.021 CrossRefGoogle Scholar
  57. Ren MC, Habte-Tsion HM, Liu B, Xie J, Ge XP, Zhou QL, Pan LK (2015a) Food deprivation of blunt snout bream, Megalobrama amblycephala fingerlings and the subsequent effect of feeding with different dietary starch levels on glucose metabolism. Isr J Aquacult Bamidgeh 67:9Google Scholar
  58. Ren MC, Habte-Tsion HM, Xie J, Liu B, Zhou QL, Ge XP, Pan LK, Chen RL (2015b) Effects of dietary carbohydrate source on growth performance, diet digestibility and liver glucose enzyme activity in blunt snout bream, Megalobrama amblycephala. Aquaculture 438:75–81.  https://doi.org/10.1016/j.aquaculture.2015.01.008 CrossRefGoogle Scholar
  59. Rencurel F, Girard J (1998) Regulation of liver gene expression by glucose. Proc Nutr Soc 57(02):265–275.  https://doi.org/10.1079/PNS19980041 CrossRefPubMedGoogle Scholar
  60. Santer R, Schneppenheim R, Dombrowski A, Götze H, Steinmann B, Schaub J (1997) Mutations in glut2, the gene for the liver-type glucose transporter, in patients with fanconi-bickel syndrome. Nat Genet 17(3):324–326.  https://doi.org/10.1038/ng1197-324 CrossRefPubMedGoogle Scholar
  61. Scott DK, O’Doherty RM, Stafford JM, Newgard CB, Granner DK (1998) The repression of hormone-activated PEPCK gene expression by glucose is insulin-independent but requires glucose metabolism. J Biol Chem 273(37):24145–24151.  https://doi.org/10.1074/jbc.273.37.24145 CrossRefPubMedGoogle Scholar
  62. Shi YS (1997) Utilization of carbohydrate in warmwater fish with particular reference to tilapia, Oreochromis niloticus x O. aureus. Aquaculture 151(1-4):79–96.  https://doi.org/10.1016/S0044-8486(96)01491-3 CrossRefGoogle Scholar
  63. Shikata T, Iwanaga S, Shimeno S (1994) Effects of dietary glucose, fructose and galactose on hepatopancreatic enzyme activities and body composition in carp. Fish Sci 60(5):613–617.  https://doi.org/10.2331/fishsci.60.613 CrossRefGoogle Scholar
  64. Shimeno S, Takeda M, Takayama S, Fukui A, Sasaki H, Kajiyama H (1981) Adapatation of hepatopancreatic enzymes to dietary carbohydrate in carp (Cyprinus carpio). Nippon Suisan Gakkaishi 47(1):71–77.  https://doi.org/10.2331/suisan.47.71 CrossRefGoogle Scholar
  65. Stone DAJ, Allan GL, Anderson AJ (2003) Carbohydrate utilization by juvenile silver perch, Bidyanus bidyanus (Mitchell). III. The protein-sparing effect of wheat starch-based carbohydrate. Aquac Res 34(2):123–134.  https://doi.org/10.1046/j.1365-2109.2003.00774.x CrossRefGoogle Scholar
  66. Suárez MD, Sanz A, Bazoco J, García-Gallego M (2002) Metabolic effects of changes in the dietary protein: carbohydrate ratio in eel (Anguilla anguilla) and trout (Oncorhynchus mykiss). Aquaculture 10:143–156.  https://doi.org/10.1023/A:1021371104839 CrossRefGoogle Scholar
  67. Sun SM, Gu ZM, Fu HT, Zhu J, Ge XP, Xuan FJ (2016) Molecular cloning, characterization, and expression analysis of p53 from the oriental river prawn, Macrobrachium nipponense, in response to hypoxia. Fish Shellfish Immunol 54:68–76.  https://doi.org/10.1016/j.fsi.2016.03.167 CrossRefPubMedGoogle Scholar
  68. Teerijoki H, Krasnov A, Pitkanen TI, Molsa H (2000) Cloning and characterization of glucose transporter in teleost fish rainbow trout (Oncorhynchus mykiss). Biochim Biophys Acta 1494(3):290–294.  https://doi.org/10.1016/S0167-4781(00)00216-5 CrossRefPubMedGoogle Scholar
  69. Teerijoki H, Krasnov A, Pitkanen TI, Molsa H (2001) Monosaccharide uptake in common carp (Cyprinus carpio) EPC cells is mediated by a facilitative glucose carrier. Comp Biochem Physiol B 128(3):483–491.  https://doi.org/10.1016/S1096-4959(00)00346-8 CrossRefPubMedGoogle Scholar
  70. Terova G, Rimoldi S, Brambilla F, Gornati R, Bernardini G, Saroglia M (2009) In vivo regulation of GLUT2 mRNA in sea bass (Dicentrarchus labrax) in response to acute and chronic hypoxia. Comp Biochem Physiol B 152(4):306–316.  https://doi.org/10.1016/j.cbpb.2008.12.011 CrossRefPubMedGoogle Scholar
  71. Thompson KS, Towle HC (1991) Localization of the carbohydrate response element of the rat L-type pyruvate kinase gene. J Biol Chem 266(14):8679–8682PubMedGoogle Scholar
  72. Thorens B (1996) Glucose transporters in the regulation of intestinal, renal, and liver glucose fluxes. Am J Physiol Gastrointest Liver Physiol 270(4):G541–G553.  https://doi.org/10.1152/ajpgi.1996.270.4.G541 CrossRefGoogle Scholar
  73. Thorens B, Charron MJ, Lodish HF (1990) Molecular physiology of glucose transporters. Diabetes Care 13(3):209–218.  https://doi.org/10.2337/diacare.13.3.209 CrossRefPubMedGoogle Scholar
  74. 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 CrossRefGoogle Scholar
  75. Wilson RP, Poe WE (1987) Apparent inability of channel catfish to utilize dietary mono-and disaccharides as energy sources. J Nutr 117(2):280–285.  https://doi.org/10.1093/jn/117.2.280 CrossRefPubMedGoogle Scholar
  76. Wood IS, Trayhurn P (2003) Glucose transporters (GLUT and SGLUT): expanded families of sugar transport proteins. Br J Nutr 89(01):3–9.  https://doi.org/10.1079/BJN2002763 CrossRefPubMedGoogle Scholar
  77. Wood IS, Wang B, Lorente-Cebrián S, Trayhurn P (2007) Hypoxia increases expression of selective facilitative glucose transporters (GLUT) and 2-deoxy-D-glucose uptake in human adipocytes. Biochem Biophys Res Commun 361(2):468–473.  https://doi.org/10.1016/j.bbrc.2007.07.032 CrossRefPubMedGoogle Scholar
  78. Wright JR, O'Hali W, Yang H, Bonen A (1998) GLUT-4 deficiency and absolute peripheral resistance to insulin in the teleost fish tilapia. Gen Comp Endocrinol 111(1):20–27.  https://doi.org/10.1006/gcen.1998.7081 CrossRefPubMedGoogle Scholar
  79. Wu X, Freeze HH (2002) GLUT14, a duplicon of GLUT3, is specifically expressed in testis as alternative splice forms. Genomics 80(6):553–557.  https://doi.org/10.1006/geno.2002.7010 CrossRefPubMedGoogle Scholar
  80. Yamamoto T, Fukumoto H, Koh G, Yano H, Yasuda K, Masuda K, Ikeda H, Imura H, Seino Y (1991) Liver and muscle-fat type glucose transporter gene expression in obese and diabetic rats. Biochem Biophys Res Commun 175(3):995-1002.CrossRefPubMedGoogle Scholar
  81. Yang Y (2011) Effect of dietary carbohydrate level on growth performance and mRNA expression of several carbohydrate metabolism genes in juvenile Darkbarbel catfish, Pelteobagrus vachelli. East China Normal University, ShanghaiGoogle Scholar
  82. Yoo HW, Shin YL, Seo EJ, Kim GH (2002) Identification of a novel mutation in the glut2 gene in a patient with fanconi-bickel syndrome presenting with neonatal diabetes mellitus and galactosaemia. Eur J Pediatr 161(6):351–353.  https://doi.org/10.1007/s00431-002-0931-y CrossRefPubMedGoogle Scholar
  83. Yuan X, Zhou Y, Liang XF, Li J, Liu L, Li B, He Y, Guo X, Fang L (2013) Molecular cloning, expression and activity of pyruvate kinase in grass carp Ctenopharyngodon idella: effects of dietary carbohydrate level. Aquaculture 410-411(2):32–40CrossRefGoogle Scholar
  84. Zhang Z, Wu RS, Mok HO, Wang Y, Poon WL, Cheng SH, Kong RY (2003) Isolation, characterization and expression analysis of a hypoxia-responsive glucose transporter gene from the grass carp, Ctenopharyngodon idellus. Eur J Biochem 270(14):3010–3017.  https://doi.org/10.1046/j.1432-1033.2003.03678.x CrossRefPubMedGoogle Scholar
  85. Zhao FQ, Keating AF (2007) Functional properties and genomics of glucose transporters. Curr Genomics 8(2):113–128.  https://doi.org/10.2174/138920207780368187 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Zhou Z, Ren Z, Zeng H, Yao B (2008) Apparent digestibility of various feedstuffs for blunt snout bream, Megalobrama amblycephala. Aquac Nutr 4:153–165CrossRefGoogle Scholar
  87. Zhou CP, Ge XP, Liu B, Xie J, Chen RL, Ren MC (2015) Effect of high dietary carbohydrate on the growth performance, blood chemistry, hepatic enzyme activities and growth hormone gene expression of wuchang bream (megalobrama amblycephala) at two temperatures. Asian-Australas J Anim Sci 28(2):207–214.  https://doi.org/10.5713/ajas.13.0705 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Hualiang Liang
    • 1
  • Ahmed Mokrani
    • 1
  • Hopeson Chisomo-Kasiya
    • 1
  • Ogwok-Manas Wilson-Arop
    • 1
  • Haifeng Mi
    • 2
  • Ke Ji
    • 1
  • Xianping Ge
    • 1
    • 2
  • Mingchun Ren
    • 1
    • 2
  1. 1.Wuxi Fisheries CollegeNanjing Agricultural UniversityWuxiChina
  2. 2.Key Laboratory for Genetic Breeding of Aquatic Animals and Aquaculture Biology, Freshwater Fisheries Research Center (FFRC)Chinese Academy of Fishery Sciences (CAFS)WuxiChina

Personalised recommendations