Abstract
In waterfowls, overfeeding leads to a hepatic steatosis, also called “foie gras.” We decided to investigate the role of glucose metabolism in steatosis emergence. For this, we measured the expression of genes during the 12 h following the last meal of the overfeeding period. As expected, it showed that the expression of glucose transporter is more precocious in jejunal mucosa, especially for SGLT1, known to be the major transporter at the apical surface. In the liver, GLUT2 and HK1 are upregulated at the same time and seem to work together to import glucose. In peripherals tissues, such as muscle and subcutaneous adipose tissue (SAT), expression of genes of interest occurs later than the one in jejunum and liver. These results are in accordance with the evolution of glycemia. This study allows us to better understand the kinetic treatment of glucose after a meal in overfed ducks. It also will allow researchers to better target their sampling time knowing the optimal point of expression of each gene.
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References
André JM, Guy G, Gontier-Latonnelle K, Bernadet MD, Davail B, Hoo-Paris R, Davail S (2007) Influence of lipoprotein-lipase activity on plasma triacylglycerol concentration and lipid storage in three genotypes of ducks. Comp Biochem Physiol A Mol Integr Physiol 148:899–902. doi:10.1016/j.cbpa.2007.09.006
Awad WA, Aschenbach JR, Ghareeb K, Khayal B, Hess C, Hess M (2014) Campylobacter jejuni influences the expression of nutrient transporter genes in the intestine of chickens. Vet Microbiol 172:195–201. doi:10.1016/j.vetmic.2014.04.001
Belo P, Romsos D, Leveille G (1976) Blood metabolites and glucose metabolism in the fed and fasted chicken. J Nutr 106:1135–1143
Carayannopoulos MO, Chi MM, Cui Y, Pingsterhaus JM, McKnight RA, Mueckler M, Devaskar SU, Moley KH (2000) GLUT8 is a glucose transporter responsible for insulin-stimulated glucose uptake in the blastocyst. Proc Natl Acad Sci USA 97:7313–7318. doi:10.1073/pnas.97.13.7313
Chartrin P, Bernadet M-D, Guy G, Mourot J, Hocquette J-F, Rideau N, Duclos MJ, Baéza E (2006) Does overfeeding enhance genotype effects on energy metabolism and lipid deposition in breast muscle of ducks? Comp Biochem Physiol A Mol Integr Physiol 145:413–418. doi:10.1016/j.cbpa.2006.07.024
Coudert E, Pascal G, Dupont J, Simon J, Cailleau-Audouin E, Crochet S, Duclos MJ, Tesseraud S, Métayer-Coustard S (2015) Phylogenesis and biological characterization of a new glucose transporter in the chicken (Gallus gallus), GLUT12. PLoS ONE 10:1–18. doi:10.1371/journal.pone.0139517
Davail S, Rideau N, Guy G, André J-M, Hermier D, Hoo-Paris R (2003) Hormonal and metabolic responses to overfeeding in three genotypes of ducks. Comp Biochem Physiol Part A Mol Integr Physiol 134:707–715. doi:10.1016/S1095-6433(02)00365-3
Doege H, Schürmann A, Bahrenberg G, Brauers A, Joost HG (2000) GLUT8, a novel member of the sugar transport facilitator family with glucose transport activity. J Biol Chem 275:16275–16280. doi:10.1074/jbc.275.21.16275
Dong XY, Wang YM, Yuan C, Zou XT (2012) The ontogeny of nutrient transporter and digestive enzyme gene expression in domestic pigeon (Columba livia) intestine and yolk sac membrane during pre- and posthatch development. Poult Sci 91:1974–1982. doi:10.3382/ps.2012-02164
Farhat A, Chavez ER (2000) Comparative performance, blood chemistry, and carcass composition of two lines of pekin ducks reared mixed or separated by sex. Poult Sci 79:460–465
Fernandez X, Bouillier-Oudot M, Molette C, Bernadet MD, Manse H (2011) Duration of transport and holding in lairage at constant postprandial delay to slaughter–effects on fatty liver and breast muscle quality in mule ducks. Poult Sci 90:2360–2369. doi:10.3382/ps.2011-01483
Ferrer R, Gil M, Moret M, Oliveras M, Planas JM (1994) Hexose transport across the apical and basolateral membrane of enterocytes from different regions of the chicken intestine ". Pflügers Archiv 426:83–88.
Fon Tacer K, Rozman D (2011) Nonalcoholic fatty liver disease: focus on lipoprotein and lipid deregulation. J Lipids 2011:783976. doi:10.1155/2011/783976
Gal-garber O, Mabjeesh SJ, Sklan D, Uni Z (2000) Nutrient-gene expression partial sequence and expression of the gene for and activity of the sodium glucose transporter in the small intestine of fed, starved and refed chickens. J Nutr 130:2174–2179
Garriga C, Moreto M, Planas JM (1997) Hexose transport across the basolateral membrane of the chicken jejunum. Am J Physiol 272:R1330–R1335
Garriga C, Moretó M, Planas JM (1999) Hexose transport in the apical and basolateral membranes of enterocytes in chickens adapted to high and low NaCl intakes. J Physiol 514:189–199. doi:10.1111/j.1469-7793.1999.189af.x
Gilbert ER, Li H, Emmerson DA, Webb KE, Wong EA (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poult Sci 86:1739–1753
Gontier K, André J-M, Bernadet M-D, Ricaud K, Davail S, (2013) Insulin effect on lipogenesis and fat distribution in three genotypes of ducks during overfeeding. Comp Biochem Physiol A Mol Integr Physiol 164:499–505. doi:10.1016/j.cbpa.2012.12.019
Guerre-Millo M (1995) Les transporteurs d’hexoses. Médecine Sci 11: 1111–1119.
Hazelwood RL, Lorenz W (1959) Effects of fasting and insulin on carbohydrate metabolism of the domestic fowl. Am J Physiol 197:47–51
Hermier D, Saadounb A, Salichonb M, Sellierc N, Rousselot D (1991) Plasma lipoproteins and liver lipids in two breeds of geese with different susceptibility to hepatic steatosis: changes induced by development and force-feeding. Lipids 26, 331–339.
Humphrey BD, Stephensen CB, Calvert CC, Klasing KC (2004) Glucose and cationic amino acid transporter expression in growing chickens (Gallus gallus domesticus). Comp Biochem Physiol A Mol Integr Physiol 138:515–525. doi:10.1016/j.cbpb.2004.06.016
Iizuka K, Bruick RK, Liang G, Horton JD, Uyeda K (2004) Deficiency of carbohydrate response element-binding protein (ChREBP) reduces lipogenesis as well as glycolysis. Proc Natl Acad Sci U S A 101:7281–7286. doi:10.1073/pnas.0401516101
Katz EB, Stenbit, a E., Hatton K, DePinho R, Charron MJ (1995) Cardiac and adipose tissue abnormalities but not diabetes in mice deficient in GLUT4. Nature. doi:10.1038/377151a0
Kono T, Nishida M, Nishiki Y, Seki Y, Sato K, Akiba Y (2005) Characterisation of glucose transporter (GLUT) gene expression in broiler chickens. Br Poult Sci 46:510–515. doi:10.1080/00071660500181289
Kwon O, Eck P, Chen S, Corpe CP, Lee J-H, Kruhlak M, Levine M (2007) Inhibition of the intestinal glucose transporter GLUT2 by flavonoids. FASEB J 21:366–377. doi:10.1096/fj.06-6620com
Li Y, Cai HY, Liu GH, Dong XL, Chang WH, Zhang S, Zheng, A J, Chen GL (2009) Effects of stress simulated by dexamethasone on jejunal glucose transport in broilers. Poult Sci 88:330–337. doi:10.3382/ps.2008-00257
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Lu L, Chen Y, Wang Z, Li X, Chen W, Tao Z, Shen J, Tian Y, Wang D, Li G, Chen L, Chen F, Fang D, Yu L, Sun Y, Ma Y, Li J, Wang J (2015) The goose genome sequence leads to insights into the evolution of waterfowl and susceptibility to fatty liver. Genome Biol 16:1–11. doi:10.1186/s13059-015-0652-y
Mueckler M (1994) Facilitative glucose transporters. Eur J Biochem 219:713–725. doi:10.1111/j.1432-1033.1994.tb18550.x
Mueckler M, Thorens B (2013) The SLC2 (GLUT) family of membrane transporters. Mol Aspects Med 34:121–138. doi:10.1016/j.mam.2012.07.001
Ruhnke I, Rӧhe I, Goodarzi Boroojeni F, Knorr F, Mader A, Hafeez A, Zentek J (2015) Feed supplemented with organic acids does not affect starch digestibility, nor intestinal absorptive or secretory function in broiler chickens. J Anim Physiol Anim Nutr (Berl) 99:29–35. doi:10.1111/jpn.12313
Saadoun A, Bernard L (1986) In vivo lipogenesis of genetically lean and fat chickens: effects of nutritional state and dietary fat. J Nutr 117:428–435
Saez G, Baéza E, Davail S, Durand D, Bauchart D, Gruffat D (2009) Hepatic metabolism of glucose and linoleic acid varies in relation to susceptibility to fatty liver in ad libitum-fed Muscovy and Pekin ducks. Br J Nutr 101:510–517. doi:10.1017/S0007114508019892
Schettler T (2003) Corn and corn-derived products: sources of endocrine disruptors. Environ Health Perspect 111:691
Seiliez I, Médale F, Aguirre P, Larquier M, Lanneretonne L, Alami-Durante H, Panserat S, Skiba-Cassy S (2013) Postprandial regulation of growth- and metabolism-related factors in zebrafish. Zebrafish 10:237–248. doi:10.1089/zeb.2012.0835
Seki Y, Sato K, Kono T, Abe H, Akiba Y (2003) Broiler chickens (Ross strain) lack insulin-responsive glucose transporter GLUT4 and have GLUT8 cDNA. Gen Comp Endocrinol 133:80–87. doi:10.1016/S0016-6480(03)00145-X
Shepherd EJ, Helliwell, P A, Mace OJ, Morgan EL, Patel N, Kellett GL (2004) Stress and glucocorticoid inhibit apical GLUT2-trafficking and intestinal glucose absorption in rat small intestine. J Physiol 560:281–290. doi:10.1113/jphysiol.2004.072447
Sun X, Zhang H, Sheikhahmadi A, Wang Y, Jiao H, Lin H, Song Z(2014) Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (Gallus gallus domesticus). Int J Biometeorol. 127–135. doi:10.1007/s00484-014-0829-1
Thorens B, Cheng Z-Q, Brown D, Lodish FH (1990) Liver glucose transporter: a basolateral protein in hepatocytes and intestine and kidney cells. Am J Physiol 259:C279–C285
Uldry M, Thorens B (2004) The SLC2 family of facilitated hexose and polyol transporters. Pflugers Arch. Eur. J Physiol 447:480–489. doi:10.1007/s00424-003-1085-0
Welch KC, Allalou A, Sehgal P, Cheng J, Ashok A (2013) Glucose transporter expression in an avian nectarivore: the ruby-throated hummingbird (Archilochus colubris). PLoS ONE 14:8. doi:10.1371/journal.pone.0077003
Wright EM, Turk E (2004) The sodium/glucose cotransport family SLC5. Pflugers Arch Eur J Physiol 447:510–518. doi:10.1007/s00424-003-1063-6
Acknowledgements
We thank the “Conseil Général des Landes” and the “Comité Interprofessionnel des Palmipèdes à Foie Gras” (CIFOG) for financing this work. We also thank the technical staff of INRA Artiguères for rearing ducks (Certificate of Authorization to Experiment on Living animals, No. B40-037-1, Ministry of Agriculture and Fish Products, ethic committee Aquitaine birds and fish No.C2EA-73). We are grateful to Frédéric Martins and Jean-José Maoret for performing Fluidigm analysis (Génopole Toulouse/Midi-pyrénées, Plateau Transcriptomique Quantitative (TQ), Toulouse, France). We finally thank Patrick Daniel, Karine Bellet, and Martine Chague of the laboratory Pyrénées Landes (LPL, Mont de Marsan) to let us use their materials.
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Annabelle, T., Karine, R., Marie-Dominique, B. et al. Kinetics of expression of genes involved in glucose metabolism after the last meal in overfed mule ducks. Mol Cell Biochem 430, 127–137 (2017). https://doi.org/10.1007/s11010-017-2960-x
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DOI: https://doi.org/10.1007/s11010-017-2960-x