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Molecular cloning of glucose transporter 1 in grouper Epinephelus coioides and effects of an acute hyperglycemia stress on its expression and glucose tolerance

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Abstract

The glucose transporter family proteins play pivotal roles in glucose metabolism. In this study, we successfully cloned the orange spotted grouper (Epinephelus coioides) glucose transporter 1 (EcGlut1) gene (GenBank accession: JQ623903). The full-length EcGlut1 cDNA was 2126 bp with a 1476 bp ORF, a 437bp5′-UTR and 223bp3′-UTR. EcGlut1 is predicted to encode a 491 amino acid protein with a MW of 53.9 kDa, a pI of 8.66 and a Pfam domain. Bioinformatics analysis revealed that EcGlut1 was evolutionally conserved between fishes with 80–89 % amino acid identities. EcGlut1 was expressed predominantly in heart and liver and at lower levels in muscle, intestine, stomach and brain. We also investigated the effect of acute hyperglycemia stress on EcGlut1 expression. In glucose tolerance test, changes in EcGlut1 mRNA expression in response to glucose injection and glucose metabolism-related indictors were assessed at the same time. Glucose injection significantly suppressed EcGlut1 mRNA expression in liver at 12 h and in brain at 24 h postinjection (P < 0.05). EcGlut1 mRNA levels in heart were increased at 6 h (P < 0.05). Plasma glucose level increased significantly and reached its maximum at 3 h postinjection (P < 0.05). The spatiotemporal expression of EcGlut1 and glucose metabolism suggested that orange spotted grouper might rely on fat anabolism to reduce acute hyperglycemia stress and the delayed transcription of EcGlut1 gene might be one reason for glucose intolerance in E. coioides.

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References

  • Abdul-Ghani MA, DeFronzo RA (2014) Lowering plasma glucose concentration by inhibiting renal sodium–glucose cotransport. J Intern Med 276:352–363

    Article  CAS  PubMed  Google Scholar 

  • Balmaceda-Aguilera C, Martos-Sitcha JA, Mancera JM, Martínez-Rodríguez G (2012) Cloning and expression pattern of facilitative glucose transporter 1 (GLUT1) in gilthead sea bream Sparus aurata in response to salinity acclimation. Comp Biochem Physiol A Mol Integr Physiol 163:38–46

    Article  CAS  PubMed  Google Scholar 

  • Boonyaratpalin M (1997) Nutrient requirements of marine food fish cultured in Southeast Asia. Aquaculture 151:283–313

    Article  CAS  Google Scholar 

  • Deng DF, Refstie S, Hung SS (2001) Glycemic and glycosuric responses in white sturgeon (Acipenser transmontanus) after oral administration of simple and complex carbohydrates. Aquaculture 199:107–117

    Article  CAS  Google Scholar 

  • Deng D, Xu C, Sun P, Wu J, Yan C, Hu M, Yan N (2014) Crystal structure of the human glucose transporter GLUT1. Nature 510(7503):121–125

    Article  CAS  PubMed  Google Scholar 

  • Díaz M, Vraskou Y, Gutiérrez J, Planas JV (2009) Expression of rainbow trout glucose transporters GLUT1 and GLUT4 during in vitro muscle cell differentiation and regulation by insulin and IGF-I. Am J Physiol Regul Integr Comp Physiol 296:R794–R800

    Article  PubMed  Google Scholar 

  • Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42

    Article  Google Scholar 

  • Eusebio PS, Coloso RM, Mamauag RE (2004) Apparent digestibility of selected ingredients in diets for juvenile grouper, Epinephelus coioides (Hamilton). Aquac Res 35:1261–1269

    Article  CAS  Google Scholar 

  • Geurden I, Mennigen J, Plagnes-Juan E, Veron V, Cerezo T, Mazurais D, Zambonino-Infante J, Gatesoupe J, Skiba-Cassy S, Panserat S (2014) High or low dietary carbohydrate: protein ratios during first-feeding affect glucose metabolism and intestinal microbiota in juvenile rainbow trout. J Exp Biol 217:3396–3406

    Article  CAS  PubMed  Google Scholar 

  • Hall JR, MacCormack TJ, Barry CA, Driedzic WR (2004) Sequence and expression of a constitutive, facilitated glucose transporter (GLUT1) in Atlantic cod Gadus morhua. J Exp Biol 207:4697–4706

    Article  CAS  PubMed  Google Scholar 

  • Hall JR, Clow KA, Short CE, Driedzic WR (2014) Transcript levels of class I GLUTs within individual tissues and the direct relationship between GLUT1 expression and glucose metabolism in Atlantic cod (Gadus morhua). J Comp Physiol B 184:483–496

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hrytsenko O, Pohajdak B, Xu BY, Morrison C, Wright JR (2010) Cloning and molecular characterization of the glucose transporter 1 in tilapia (Oreochromis niloticus). Gen Comp Endocrinol 165:293–303

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Legate N, Bonen A, Moon T (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 122:48–59

    Article  CAS  PubMed  Google Scholar 

  • 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 23:127–132

    Article  CAS  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(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Mazur CN, Higgs D, Plisetskaya E, March B (1992) Utilization of dietary starch and glucose tolerance in juvenile Chinook salmon (Oncorhynchus tshawytscha) of different strains in seawater. Fish Physiol Biochem 10:303–313

    Article  CAS  PubMed  Google Scholar 

  • Min SY, Hwang SY, Jung YO, Jeong J, Park SH, Cho CS, Kim HY, Kim WU (2004) Increase of cyclooxygenase-2 expression by interleukin 15 in rheumatoid synoviocytes. J Rheumatol 31:875–883

    CAS  PubMed  Google Scholar 

  • Moon TW (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Physiol B Biochem Mol Biol 129:243–249

    Article  CAS  PubMed  Google Scholar 

  • Peres H, Goncalves P, Oliva-Teles A (1999) Glucose tolerance in gilthead seabream (Sparus aurata) and European seabass (Dicentrarchus labrax). Aquaculture 179:415–423

    Article  CAS  Google Scholar 

  • Polakof S, Mommsen TP, Soengas JL (2011) Glucosensing and glucose homeostasis: from fish to mammals. Comp Biochem Physiol B Biochem Mol Biol 160:123–149

    Article  CAS  PubMed  Google Scholar 

  • Polakof S, Panserat S, Soengas JL, Moon TW (2012) Glucose metabolism in fish: a review. J Comp Physiol B 182:1015–1045

    Article  CAS  PubMed  Google Scholar 

  • Tacon AG, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285:146–158

    Article  CAS  Google Scholar 

  • Tan Q, Xie S, Zhu X, Lei W, Yang Y (2006) Effect of dietary carbohydrate sources on growth performance and utilization for gibel carp (Carassius auratus gibelio) and Chinese longsnout catfish (Leiocassis longirostris Günther). Aquac Nutr 12:61–70

    Article  CAS  Google Scholar 

  • Teerijoki H, Krasnov A, Pitkänen TI, Mölsä H (2000) Cloning and characterization of glucose transporter in teleost fish rainbow trout (Oncorhynchus mykiss). Biochim Biophys Acta (BBA) Gene Struct Exp 1494:290–294

    Article  CAS  Google Scholar 

  • Teerijoki H, Krasnov A, Gorodilov Y, Krishna S, Mölsä H (2001a) Rainbow trout glucose transporter (OnmyGLUT1): functional assessment in Xenopus laevis oocytes and expression in fish embryos. J Exp Biol 204:2667–2673

    CAS  PubMed  Google Scholar 

  • Teerijoki H, Krasnov A, Pitkänen TI, Mölsä H (2001b) Monosaccharide uptake in common carp (Cyprinus carpio) EPC cells is mediated by a facilitative glucose carrier. Comp Biochem Physiol B Biochem Mol Biol 128:483–491

    Article  CAS  PubMed  Google Scholar 

  • Tian LX, Liu YJ, Yang HJ, Liang GY, Niu J (2012) Effects of different dietary wheat starch levels on growth, feed efficiency and digestibility in grass carp (Ctenopharyngodon idella). Aquac Int 20:283–293

    Article  CAS  Google Scholar 

  • Tseng YC, Lee JR, Lee SJ, Hwang PP (2011) Functional analysis of the glucose transporters-1α,-6, and-13.1 expressed by zebrafish epithelial cells. Ame J Physiol Regul Integr Comp Physiol 300:R321–R329

    Article  CAS  Google Scholar 

  • Viegas I, Rito J, González JD, Jarak I, Carvalho RA, Metón I, Pardal MA, Baanante IV, Jones JG (2013) Effects of food-deprivation and refeeding on the regulation and sources of blood glucose appearance in European seabass (Dicentrarchus labrax L.). Comp Biochem Physiol A Mol Integr Physiol 166:399–405

    Article  CAS  PubMed  Google Scholar 

  • Wood IS, Trayhurn P (2003) Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br J Nutr 89:3–9

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31272673), the National Basic Research Program of China (2014CB138600), Guangdong Natural Science Foundation (S2013010016511), Foundation of Guangdong Provincial Key Laboratory of Marine Biotechnology (No. GPKLMB201401), Colleges Pearl River Scholar (GDUPS) (2011) and Project of Enhancing School With Innovation of Guangdong Ocean University (2015KTSCX055). We thank Prof. Ya-Xiong Tao at Auburn University (Auburn, Alabama, USA) for his expert help in editing the English language of an earlier version of this manuscript.

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Correspondence to Beiping Tan.

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Liu, H., Dong, X., Chi, S. et al. Molecular cloning of glucose transporter 1 in grouper Epinephelus coioides and effects of an acute hyperglycemia stress on its expression and glucose tolerance. Fish Physiol Biochem 43, 103–114 (2017). https://doi.org/10.1007/s10695-016-0271-x

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  • DOI: https://doi.org/10.1007/s10695-016-0271-x

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