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Apical sodium–glucose co-transport can be regulated by blood-borne glucose in the ruminal epithelium of sheep (Ovis aries, Merino breed)

Published online by Cambridge University Press:  09 March 2007

Cengiz Atasoglu ,
Gotthold Gäbel  and
Jörg R. Aschenbach
Cengiz Atasoglu
Affiliation:
Institute of Veterinary Physiology, Leipzig University, An den Tierkliniken 7, D-04103, Leipzig, Germany Canakkale Onsekiz Mart University, Faculty of Agriculture, Department of Animal Science, 17100 Canakkale, Turkey
Gotthold Gäbel
Affiliation:
Institute of Veterinary Physiology, Leipzig University, An den Tierkliniken 7, D-04103, Leipzig, Germany
Jörg R. Aschenbach*
Affiliation:
Institute of Veterinary Physiology, Leipzig University, An den Tierkliniken 7, D-04103, Leipzig, Germany
*
*Corresponding author: Dr J. R. Aschenbach, fax +49 341 97 38097, email, aschenb@rz.uni-leipzig.de
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Abstract

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The intestinal Na-dependent D-glucose co-transporter (SGLT)-1 in sheep is under dietary regulation by luminal substrates. The aim of the present study was to find out whether the SGLT-1 in the forestomach of sheep is also regulated by sugars. Furthermore, the location of a possible glucosensor (luminal v. intracellular v. basolateral) was to be elucidated. Ruminal epithelia of sheep (Ovis aries, Merino breed) were pre-incubated in Ussing chambers with various substrates on the mucosal (i.e. luminal) or serosal (i.e. blood) side. This pre-incubation period was followed by a second pre-incubation period without the tested substrates (washout period). Thereafter, apical D-glucose uptake by ruminal epithelial cells was determined with 200 μmol D-[14C]glucose/l in the absence or co-presence of the SGLT-1 inhibitor, phlorizin. Pre-incubation with D-glucose on the mucosal side had no significant effect on apical D-glucose uptake (P>0.05). In contrast, pre-incubation with D-glucose, D-mannose, 3-O-methyl-D-glucose or sucrose on the serosal side significantly increased D-glucose uptake compared with mannitol-treated controls (P<0.05). Serosal pre-incubation with cellobiose or D-xylose had no effect. The stimulation of D-glucose uptake by serosal D-glucose pre-incubation was concentration dependent, with maximal stimulation at about 10 mmol/l. We conclude that the ruminal SGLT-1 can be up-regulated in a concentration-dependent manner by blood-borne D-glucose via an extracellular sugar-sensing mechanism.

Keywords

Sodium–glucose-linked transportGlucosensorRumenSheep
Type
Research Article
Information
British Journal of Nutrition , Volume 92 , Issue 5 , November 2004 , pp. 777 - 783
Copyright
Copyright © The Nutrition Society 2004

References

Aschenbach, JR, Bhatia, SK, Pfannkuche, H & Gäbel, G (2000 a) Glucose is absorbed in a sodium-dependent manner from forestomach contents of sheep. J Nutr 13, 2797–2801.CrossRefGoogle Scholar
Aschenbach, JR, Wehning, H, Kurze, M, Schaberg, E, Nieper, H, Burckhardt, G, Gäbel, G (2000 b) Functional and molecular biological evidence of SGLT-1 in the ruminal epithelium of sheep. Am J Physiol 279, G20–G27.Google ScholarPubMed
Aschenbach, JR, Borau, T, Gäbel, G (2002 a) Glucose uptake via SGLT-1 is stimulated by β2 -adrenoceptors in the ruminal epithelium of sheep. J Nutr 13, 1254–1257.CrossRefGoogle Scholar
Aschenbach, JR, Borau, T, Gäbel, G (2002 b) Sodium glucose-linked transport in the ruminal epithelium of fallow deer – comparison to sheep. J Comp Physiol B 17, 561–567.Google Scholar
Baldwin, RL & McLeod, KR (2000) Effects of diet forage:concentrate ratio and metabolizable energy intake on isolated rumen epithelial cell metabolism in vitro. J Anim Sci 78, 771–783.CrossRefGoogle ScholarPubMed
Bauer, ML, Harmon, DL, McLeod, KR & Huntington, GB (1995) Adaptation to small intestinal starch assimilation and glucose transport in ruminants. J Anim Sci 73, 1828–1838.CrossRefGoogle ScholarPubMed
Britton, R & Krehbiel, C (1993) Nutrient metabolism by gut tissues. J Dairy Sci 76, 2125–2131.CrossRefGoogle ScholarPubMed
Debnam, ES (1994) Rapid adaptation of intestinal sugar transport. News Physiol Sci 9, 84–88.Google Scholar
Dougherty, RW, Klavano, CS, Dickson, WM & Klavano, PA (1956) Blood sugar level in cattle and sheep fed various amounts of glucose. Cornell Vet 46, 397–409.Google ScholarPubMed
Dyer, J, Barker, PJ, Shirazi-Beechey, SP (1997) Nutrient regulation of the intestinal Na + /glucose co-transporter (SGLT1) gene expression. Biochem Biophys Res Commun 23, 624–629.CrossRefGoogle Scholar
Dyer, J, Vayro, S, King, TP, Shirazi-Beechey, SP (2003) Glucose sensing in the intestinal epithelium. Eur J Biochem 27, 3377–3388.CrossRefGoogle Scholar
Dyer, J, Wood, IS, Palejwala, A, Shirazi-Beechey, SP (2002) Expression of monosaccharide transporters in intestine of diabetic humans. Am J Physiol 28, G241–G248.Google Scholar
El-Sherif, MMA & Assad, F (2001) Changes in some blood constituents of Barki ewes during pregnancy and lactation under semi arid conditions. Small Rumin Res 40, 269–277.CrossRefGoogle ScholarPubMed
Francis, SM, Veenvliet, BA, Littlejohn, RP & Suttie, JM (1999) Plasma glucose and insulin levels in genetically lean and fat sheep. Gen Comp Endocrinol 11, 104–113.CrossRefGoogle Scholar
Gäbel, G & Aschenbach, JR (2002) Influence of food deprivation on the transport of 3- O -methyl- d -glucose across the isolated ruminal epithelium of sheep. J Anim Sci 80, 2740–2746.Google ScholarPubMed
Gäbel, G, Aschenbach, JR, Müller, F (2002) Transfer of energy substrates across the ruminal epithelium: implications and limitations. Anim Health Res Rev 3, 15–30.CrossRefGoogle ScholarPubMed
Giduck, SA, Fontenot, JP & Rahnema, S (1988) Effect of ruminal infusion of glucose, volatile fatty acids and hydrochloric acid on mineral metabolism in sheep. J Anim Sci 66, 532–542.CrossRefGoogle ScholarPubMed
Gow, IF, Mitchell, E & Wait, M (2003) Intravenous magnesium reduces the rate of glucose disposal in lactating sheep. Exp Physiol 88, 533–540.CrossRefGoogle ScholarPubMed
Han, XT, Noziere, P, Remond, D, Chabrot, J & Doreau, M (2002) Effects of nutrient supply and dietary bulk on O 2 uptake and nutrient net fluxes across rumen, mesenteric- and portal-drained viscera in ewes. J Anim Sci 80, 1362–1374.CrossRefGoogle Scholar
Ishikawa, Y, Eguchi, T & Ishida, H (1997) Mechanism of β-adrenergic agonist-induced transmural transport of glucose in rat small intestine. Regulation of phosphorylation of SGLT1 controls the function. Biochim Biophys Acta 135, 306–318.CrossRefGoogle Scholar
Kajikawa, H, Amari, M & Masaki, S (1997) Glucose transport by mixed ruminal bacteria from a cow. Appl Environ Microbiol 63, 1847–1851.CrossRefGoogle ScholarPubMed
Lozano, O, Theurer, CB, Alio, A, Huber, JT, Delgado-Elorduy, A, Cuneo, P, DeYoung, D, Sadik, M & Swingle, RS (2000) Net absorption and hepatic metabolism of glucose, l -lactate, and volatile fatty acids by steers fed diets containing sorghum grain processed as dry-rolled or steam-flaked at different densities. J Anim Sci 78, 1364–1371.CrossRefGoogle ScholarPubMed
Maas, JA, Wilson, GF, McCutcheon, SN, Lynch, GA, Burnham, DL & France, J (2001) The effect of season and monensin sodium on the digestive characteristics of autumn and spring pasture fed to sheep. J Anim Sci 79, 1052–1058.CrossRefGoogle ScholarPubMed
Merchen, NR (1988) Digestion, absorption and excretion in ruminants. In The Ruminant Animal. Digestive Physiology and Nutrition, pp. 172–201 [Church, DC, editors] Englewood Cliffs, NJ: Prentice Hall.Google Scholar
Remond, D, Chaise, JP, Delval, E & Poncet, C (1993) Net flux of metabolites across the ruminal wall of sheep fed twice a day with orchard grass hay. J Anim Sci 71, 2529–2538.CrossRefGoogle Scholar
Russell, RW & Gahr, SA (2000) Glucose availability and associated metabolism. In Farm Animal Metabolism and Nutrition, pp. 121–147 [D'Mello, JPF, editor]. Wallingford, Oxon: CAB International.CrossRefGoogle Scholar
Sharp, PA, Boyer, S, Srai, SK, Baldwin, SA & Debnam, ES (1997) Early diabetes-induced changes in rat jejunal glucose transport and the response to insulin. J Endocrinol 15, 19–25.CrossRefGoogle Scholar
Sharp, PA & Debnam, ES (1994) The effect of rapid changes in plasma sugar concentration on the brush-border potential difference in rat jejunum. Exp Physiol 79, 415–421.CrossRefGoogle ScholarPubMed
Shirazi-Beechey, SP (1996) Intestinal sodium-dependent d -glucose co-transporter: dietary regulation. Proc Nutr Soc 55, 167–178.CrossRefGoogle ScholarPubMed
Shirazi-Beechey, SP, Gribble, SM, Wood, IS, Tarpey, PS, Beechey, RB, Dyer, J, Scott, D & Barker, PJ (1994) Dietary regulation of the intestinal sodium-dependent glucose cotransporter (SGLT1). Biochem Soc Trans 22, 655–658.CrossRefGoogle ScholarPubMed
Shirazi-Beechey, SP, Hirayama, BA, Wang, Y, Scott, D, Smith, MW & Wright, EM (1991) Ontogenic development of lamb intestinal sodium-glucose co-transporter is regulated by diet. J Physiol 43, 699–708.CrossRefGoogle Scholar
Shirazi-Beechey, SP, Wood, IS, Dyer, J, Scott, D & King, TP (1995) Intestinal sugar transport in ruminants. Ruminant Physiology: Digestion, Metabolism, Growth and Reproduction, pp. 117–133 [Engelhardt, WV, Leonhard-Marek, S, Breves, G and Giesecke, D, editors]. Stuttgart: Enke Verlag.Google Scholar
Smith, PK, Krohn, RI, Hermanson, GT, Mallia, AK, Gartner, FH, Provenzano, MD & Fujimoto, EK (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 15, 76–85.CrossRefGoogle Scholar
Swanson, KC, Matthews, JC, Matthews, AD, Howell, JA, Richards, CJ & Harmon, DL (2000) Dietary carbohydrate source and energy intake influence the expression of pancreatic alpha-amylase in lambs. J Nutr 13, 2157–2165.CrossRefGoogle Scholar
Webster, JR, Corson, ID, Littlejohn, RP, Stuart, SK & Suttie, JM (1996) Effects of photoperiod on the cessation of growth during autumn in male red deer and growth hormone and insulin-like growth factor-I secretion. Gen Comp Endocrinol 11, 464–477.Google Scholar
Wood, IS, Dyer, J, Hofmann, RR, Shirazi-Beechey, SP (2000) Expression of the Na + /glucose co-transporter (SGLT1) in the intestine of domestic and wild ruminants. Pflugers Arch 44, 155–162.CrossRefGoogle Scholar
Wood, IS & Trayhurn, P (2003) Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br J Nutr 89, 3–9.CrossRefGoogle ScholarPubMed
Wright, EM (1993) The intestinal Na + /glucose cotransporter. Annu Rev Physiol 55, 575–589.CrossRefGoogle ScholarPubMed