The effect of insulin on plasma glucose concentrations, expression of hepatic glucose transporters and key gluconeogenic enzymes during the perinatal period in broiler chickens

Franssens, L.; Lesuisse, J.; Wang, Yuan; Willems, E.; Willemsen, H.; Koppenol, A.; Guo, X.; Buyse, J.; Decuypere, E.; Everaert, Nadia

doi:10.1016/j.ygcen.2015.12.026

Article (Scientific journals)

The effect of insulin on plasma glucose concentrations, expression of hepatic glucose transporters and key gluconeogenic enzymes during the perinatal period in broiler chickens

Franssens, L.; Lesuisse, J.; Wang, Yuan et al.

2016 • In General and Comparative Endocrinology

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/195260

DOI
10.1016/j.ygcen.2015.12.026

PubMed
26723190

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Franssens et al 2016 Gen and Comp Endocrinol.pdf

Publisher postprint (758.98 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Embryonic development; Glucose transporter; Hypoglycemia; Insulin; Regulatory enzymes of gluconeogenesis

Abstract :

[en] Chickens have blood glucose concentrations that are twofold higher than those observed in mammals. Moreover, the insulin sensitivity seems to decrease with postnatal age in both broiler and layer chickens. However, little is known about the response of insulin on plasma glucose concentrations and mRNA abundance of hepatic glucose transporters 1, 2, 3, 8, 9 and 12 (GLUT1, 2, 3, 8, 9 and 12) and three regulatory enzymes of the gluconeogenesis, phosphoenolpyruvate carboxykinase 1 and 2 (PCK1 and 2) or fructose-1,6-biphosphatase 1 (FBP1) in chicks during the perinatal period. In the present study, broiler embryos on embryonic day (ED)16, ED18 or newly-hatched broiler chicks were injected intravenously with bovine insulin (1. μg/g body weight (BW)) to examine plasma glucose response and changes in hepatic mRNA abundance of the GLUTs, PCK1 and 2 and FBP1. Results were compared with a non-treated control group and a saline-injected sham group. Plasma glucose levels of insulin-treated ED18 embryos recovered faster from their minimum level than those of insulin-treated ED16 embryos or newly-hatched chicks. In addition, at the minimum plasma glucose level seven hours post-injection (PI), hepatic GLUT2, FBP1 and PCK2 mRNA abundance was decreased in insulin-injected embryos, compared to sham and control groups, being most pronounced when insulin injection occurred on ED16. © 2015 Elsevier Inc.

Disciplines :

Animal production & animal husbandry

Author, co-author :

Franssens, L.; KU Leuven, Department of Biosystems, Laboratory of Livestock Physiology, Kasteelpark Arenberg 30, Box 2456, 3001 Leuven, Belgium

Lesuisse, J.; KU Leuven, Department of Biosystems, Laboratory of Livestock Physiology, Kasteelpark Arenberg 30, Box 2456, 3001 Leuven, Belgium

Wang, Yuan ; Université de Liège > Dép. d'électric., électron. et informat. (Inst.Montefiore) > Systèmes microélectroniques intégrés

Willems, E.; KU Leuven, Department of Biosystems, Laboratory of Livestock Physiology, Kasteelpark Arenberg 30, Box 2456, 3001 Leuven, Belgium

Willemsen, H.; KU Leuven, Department of Biosystems, Laboratory of Livestock Physiology, Kasteelpark Arenberg 30, Box 2456, 3001 Leuven, Belgium

Koppenol, A.; KU Leuven, Department of Biosystems, Laboratory of Livestock Physiology, Kasteelpark Arenberg 30, Box 2456, 3001 Leuven, Belgium, ILVO Animal Sciences Unit, Scheldeweg 68, 9090 Melle, Belgium

Guo, X.; College of Animal Science and Technology, Jiangxi Agricultural University, 330045 Jiangxi, China

Buyse, J.; KU Leuven, Department of Biosystems, Laboratory of Livestock Physiology, Kasteelpark Arenberg 30, Box 2456, 3001 Leuven, Belgium

Decuypere, E.; KU Leuven, Department of Biosystems, Laboratory of Livestock Physiology, Kasteelpark Arenberg 30, Box 2456, 3001 Leuven, Belgium

Everaert, Nadia ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Zootechnie

Title :

The effect of insulin on plasma glucose concentrations, expression of hepatic glucose transporters and key gluconeogenic enzymes during the perinatal period in broiler chickens

Publication date :

2016

Journal title :

General and Comparative Endocrinology

ISSN :

0016-6480

eISSN :

1095-6840

Publisher :

Academic Press Inc.

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 05 April 2016

Statistics

Number of views

54 (6 by ULiège)

Number of downloads

2 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Aschenbach, J.R., Steglich, K., Gäbel, G., Honscha, K.U., Expression of mRNA for glucose transport proteins in jejenum, liver, kidney and skeletal muscle of pigs. J. Physiol. Biochem. 65 (2009), 251–266.
Bigot, K., Taouis, M., Tesseraud, S., Refeeding and insulin regulate S6K1 activity in chicken skeletal muscles. J. Nutr. 133 (2003), 369–373.
Brichard, S.M., Desbuquois, B., Girard, J., Vandate treatment of diabetic rats reverses the impaired expression of genes involved in hepatic glucose metabolism: effects on glycolytic and gluconeogenic enzymes, and on glucose transporter GLUT2. Mol. Cell. Endocrinol. 91 (1993), 91–97.
Burcelin, R., Eddouks, M., Kande, J., Assan, R., Girard, J., Evidence that GLUT-2 mRNA and protein concentrations are decreased by hyperinsulinemia and increased by hyperglycaemia in liver of diabetic rats. Biochem. J. 288 (1992), 675–679.
Caprio, S., Gelfand, R.A., Tamborlane, W.V., Sherwin, R.S., Oxidative fuel metabolism during mild hypoglycemia: critical role of free fatty acids. Am. J. Physiol. 256 (1989), E413–419.
Carayannopoulos, M.O., Chi, M.M.-Y., Cui, Y., Pingsterhaus, J.M., McKnight, R.A., Mueckler, M., Devaskar, S.U., Moley, K.H., GLUT8 is a glucose transporter responsible for insulin-stimulated glucose uptake in the blastocyst. Proc. Natl. Acad. Sci. USA 97 (2000), 7313–7318.
Carver, F.M., Shibley, I.A. Jr., Pennington, J.S., Pennington, S.N., Differential expression of glucose transporters during chick embryogenesis. Cell. Mol. Life Sci. 58 (2001), 645–652.
Chida, Y., Ohtsu, H., Takahashi, K., Sato, K., Toyomizu, M., Akiba, Y., Carbohydrate metabolism in temporal and persistent hypoglycemic chickens induced by insulin infusion. Comp. Biochem. Physiol. C 126 (2000), 187–193.
Cho, H.-S., Ahn, J.-M., Han, H.-J., Cho, J.-Y., Glypican 3 binds to GLUT1 and decreases glucose transport activity in hepatocellular carcinoma cells. J. Cell. Biochem. 111 (2010), 1252–1259.
Copland, J.A., Pardini, A.W., Wood, T.G., Yin, D., Green, A., Bodenburg, Y.H., Urban, R.J., Stuart, C.A., IGF-1 controls GLUT3 expression in muscle via the transcriptional factor Sp1. Biochim. Biophys. Acta 1769 (2007), 631–640.
Coudert, E., Pascal, G., Dupont, J., Simon, J., Cailleau-Audouin, E., Crochet, S., Duclos, M.J., Tesseraud, S., Métayer-Coustard, S., Phylogenesis and biological characterization of a new glucose transporter in the chicken (Gallus gallus), GLUT12. PLoS One, 10(10), 2015, e0139517, 10.1371/journal.pone.0139517.
Danby, R.W., Martin, I.K., Gibson, W.R., Effects of pancreatectomy, tolbutamide and insulin on glucose fluxes in chickens. J. Endocrinol. 94 (1982), 429–441.
Datar, S.P., Suryavanshi, D.S., Bhonde, R.R., Chick pancreatic B islets as an alternative in vitro model for screening insulin secretagogues. Poult. Sci. 85 (2006), 2260–2264.
Davis, S.N., Dobbins, R., Tarumi, C., Colburn, C., Neal, D., Cherrington, A.D., Effects of differing insulin levels on response to equivalent hypoglycemia in conscious dogs. Am. J. Physiol. Endocrinol. Metab. 263 (1992), E688–E695.
Dupont, J., Derouet, M., Simon, J., Taouis, M., Nutritional state regulates insulin receptor and IRS-1 phosphorylation and expression in chicken. Am. J. Physiol. Endocrinol. Metab. 274 (1998), E309–E316.
Dupont, J., Derouet, M., Simon, J., Taouis, M., Effect of nutritional state on the formation of a complex involving insulin receptor IRS-1, the 52 kDa Src homology/collagen protein (Shc) isoform and phosphatidylinositol 3′-kinase activity. Biochem. J. 335 (1998), 293–300.
Dupont, J., Dagou, C., Derouet, M., Simon, J., Taouis, M., Early steps of insulin receptor signaling in chicken and rat: apparent refractoriness in chicken muscle. Domest. Anim. Endocrinol. 26 (2004), 127–142.
Dupont, J., Tesseraud, S., Derouet, M., Collin, A., Rideau, N., Crochet, S., Godet, E., Cailleau-Audouin, E., Métayer-Coustard, S., Duclos, M.J., Gespach, C., Porter, T.E., Cogburn, L.A., Simon, J., Insulin immuno-neutralization in chicken: effects on insulin signaling and gene expression in liver and muscle. J. Endocrinol. 197 (2008), 531–542.
Dupont, J., Tesseraud, S., Simon, J., Insulin signaling in chicken liver and muscle. Gen. Comp. Endocrinol. 163 (2009), 52–57.
Dupont, J., Métayer-Coustard, S., Ji, B., Ramé, C., Gespach, C., Voy, B., Simon, J., Characterization of major elements of insulin signaling cascade in chicken adipose tissue: apparent insulin refractoriness. Gen. Comp. Endocrinol. 176 (2012), 86–93.
Gezginci-Oktayoglu, S., Sacan, O., Bolkent, S., Ipci, Y., Kabasakal, L., Sener, G., Yanardag, R., Chard (Beta vulgaris L. var. cicla) extract ameliorates hyperglycemia by increasing GLUT2 through Akt2 and antioxidant defense in the liver of rats. Acta Histochem. 116 (2013), 32–39.
Gorovits, N., Cui, L., Busik, J.V., Ranalletta, M., Hauguel de-Mouzon, S., Charron, M.J., Regulation of hepatic GLUT8 expression in normal and diabetic models. Endocrinology 144 (2003), 1703–1711.
Gould, G.W., Brant, A.M., Kahn, B.B., Shepherd, P.R., McCoid, S.C., Gibbs, E.M., Expression of the brain-type glucose transporter is restricted to brain and neuronal cells in mice. Diabetologia 35 (1992), 304–309.
Gunton, J.E., Delhanty, P.J.D., Takahashi, S.-I., Baxter, R.C., Metformin rapidly increases insulin receptor activation in human liver and signals preferentially through insulin-receptor substrate-2. J. Clin. Endocrinol. Metab. 88 (2003), 1323–1332.
Hamada, T., Matsumoto, M., Effects of nutrition and ontogeny of liver cytosolic and mitochondrial phosphoenolpyruvate carboxykinase activity of the rat, hamster, guinea-pig, pig, kid, calf and chick. Comp. Biochem. Physiol. B 77 (1984), 547–550.
Joseph, J., Dandekar, D.S., Ramachandran, A.V., Dexamethasone-induced alterations in glucose tolerance and insulin, glucagon and adrenaline responses during the first month in White Leghorn chicks. Br. Poult. Sci. 37 (1996), 665–676.
Keembiyehetty, C., Augustin, R., Carayannopoulos, M.O., Steer, S., Manolescu, A., Cheeseman, C.I., Moley, K.H., Mouse glucose transporter 9 splice variants are expressed in adult liver and kidney and are up-regulated in diabetes. Mol. Endocrinol. 20 (2006), 686–697.
Kono, T., Nishida, M., Nishiki, Y., Seki, Y., Sato, K., Akiba, Dr., Characterization of glucose transporter (GLUT) gene expression in broiler chickens. Br. Poult. Sci. 46 (2005), 510–515.
Lane, R.H., Crawford, S.E., Flozak, A.S., Simmons, R.A., Localization and quantification of glucose transporters in liver of growth-retarded fetal and neonatal rats. Am. J. Physiol. Endocrinol. Metab. 276 (1999), E135–E142.
Lisinski, I., Schürmann, A., Joost, H.-G., Cushman, S.W., Al-Hasani, H., Targeting of GLUT6 (formerly GLUT9) and GLUT8 in rat adipose cells. Biochem. J. 358 (2001), 517–522.
Lisinski, I., Schürmann, A., Joost, H.G., Cushman, S.W., Al-Hasani, H., Targeting GLUT6 (formerly GLUT9) and GLUT8 in rat adipose cells. Biochem. J. 358 (2001), 517–522.
Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25 (2001), 402–408.
Lu, J.W., McMurtry, J.P., Coon, C.N., Developmental changes of plasma insulin, glucagon, insulin-like growth factors, thyroid hormones, and glucose concentrations in chick embryos and hatched chicks. Poult. Sci. 86 (2007), 673–683.
McClain, D.A., Abuelgasim, K.A., Nouraie, M., Salomon-Andonie, J., Niu, X., Maisnikova, G., Polykova, L.A., Sergueeva, A., Okhotin, D.J., Cherqaoui, R., Okhotin, D., Cox, J.E., Swierczek, S., Song, J., Simon, M.C., Huang, J., Simcox, J.A., Yoon, D., Prchal, J.T., Gordeuk, V.R., Decreased serum glucose and glycosylated hemoglobin levels in patients with Chuvash polycythemia: a role for HIF in glucose metabolism. J. Mol. Med. 91 (2013), 59–67.
McCormick, K.L., Widness, J.A., Susa, J.B., Schwartz, R., Effects of chronic hyperinsulinaemia on hepatic enzymes involved in lipogenesis and carbohydrate metabolism in the young rat. Biochem. J. 172 (1978), 327–331.
Miller, P.J., Finucane, K.A., Hughes, M., Zhao, F.-Q., Cloning and expression of bovine glucose transporter GLUT12. Mamm. Genome 16 (2005), 873–883.
Phay, J.E., Hussain, H.B., Moley, J.F., Cloning and expression analysis of a novel member of the facilitative glucose transporter family, SLCA9 (GLUT9). Genomics 66 (2000), 217–220.
Polakof, S., Mommsen, T.P., Soengas, J.L., Glucosensing and glucose homeostasis: from fish to mammals. Comp. Biochem. Physiol. B 160 (2011), 123–149.
Postic, C., Burcelin, R., Rencurel, F., Pegorier, J.-P., Loizeau, M., Girard, J., Leturque, A., Evidence for a transient inhibitory effect of insulin on GLUT2 expression in the liver: studies in vivo and in vitro. Biochem. J. 293 (1993), 119–124.
Postic, C., Leturque, A., Printz, R.L., Maulard, P., Loizeau, M., Granner, D.K., Girard, J., Development and regulation of glucose transporter and hexokinase expression in rat. Am. J. Physiol. Endocrinol. Metab. 266 (1994), E548–E559.
Rasmussen, R., Quantification of the LightCycler. Meuer, S., Wittwer, C., Nakagawara, K., (eds.) Rapid Cycle Real-Time PCR, Methods and Applications, 2001, Springer Press, Heidelberg, 21–34.
Seki, Y., Sato, K., Kono, T., Abe, H., Akiba, Y., Broiler chickens (Ross strain) lack insulin-responsive glucose transporter GLUT4 and have GLUT8 cDNA. Gen. Comp. Endocrinol. 133 (2003), 80–87.
Shin, B.C., McKnight, R.A., Devaskar, S.U., Glucose transporter GLUT8 translocation in neurons is not insulin responsive. J. Neurosci. Res. 75 (2004), 835–844.
Simon, J., Chicken as a useful species for the comprehension of insulin action. Crit. Rev. Poult. Biol. 2 (1989), 121–148.
Simon, J., Leclercq, B., Fat and lean chickens: prefattening period and in vivo sensitivity to insulin, atropine, and propranolol. Am. J. Physiol. 249 (1985), R393–R401.
Simon, J., Rideau, N., Taouis, M., Dupont, J., Plasma insulin levels are rather similar in chicken and rat. Gen. Comp. Endocrinol. 171 (2011), 267–268.
Takanaga, H., Chaudhuri, B., Frommer, W.B., GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochim. Biophys. Acta 1778 (2008), 1091–1099.
Thorn, S.R., Sekar, S.M., Lavezzi, J.R., O'Meara, M.C., Brown, L.D., Hay, W.W. Jr., Rozance, P.J., A physiological increase in insulin suppresses gluconeogenic gene activation in fetal sheep with sustained hypoglycemia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303 (2012), R861–R869.
Tinker, D.A., Brosnan, J.T., Herzberg, G.R., Interorgan metabolism of amino acids, glucose, lactate, glycerol and uric acid in the domestic fowl (Gallus domesticus). Biochem. J. 240 (1986), 829–836.
Tokushima, Y., Sulistiyanto, B., Takahashi, K., Akiba, Y., Insulin–glucose interactions characterized in newly hatched broiler chicks. Br. Poult. Sci. 44 (2003), 746–751.
Tokushima, Y., Takahashi, K., Sato, K., Akiba, Y., Glucose uptake in vivo in skeletal muscles of insulin-injected chicks. Comp. Biochem. Physiol. B 141 (2005), 43–48.
Zhang, W., Sumners, L.H., Siegel, P.B., Cline, M.A., Gilbert, E.R., Quantity of glucose transporter and appetite-associated factor mRNA in various tissues after insulin injection in chickens selected for low or high body weight. Physiol. Genomics 45 (2013), 1084–1094.
Zhao, J.P., Bao, J., Wang, X.J., Jiao, H.C., Song, Z.G., Lin, H., Altered gene and protein expression of glucose transporter1 underlies dexamethasone inhibition of insulin-stimulated glucose uptake in chicken muscles. J. Anim. Sci. 90 (2012), 4337–4345.
Zheng, Q., Levitsky, L.L., Mink, K., Rhoads, D.B., Glucose regulation of glucose transporters in cultured adult and fetal hepatocytes. Metabolism 44 (1995), 1553–1558.