QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Aschenbach, J. R. Articles by Gäbel, G. Search for Related Content PubMed PubMed Citation Articles by Aschenbach, J. R. Articles by Gäbel, G.

---

Nutrient Metabolism
Research Communication

Glucose Uptake via SGLT-1 Is Stimulated by ß₂-Adrenoceptors in the Ruminal Epithelium of Sheep^{1 ,2}

Department of Veterinary Physiology, Leipzig University, D-04103 Leipzig, Germany

³To whom correspondence should be addressed. E-mail: aschenb{at}rz.uni-leipzig.de.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Glucose absorption via the sodium glucose-linked transporter (SGLT)-1, decreases the glucose concentration in the ruminant forestomach and may ameliorate or prevent ruminal lactic acidosis. Because acidotic ruminants show increased sympathetic activity, the possibility of adrenergic modulation of SGLT-1 was investigated. Glucose uptake into ovine ruminal epithelia was measured in Ussing chambers after the addition of 200 µmol/L ¹⁴C-labeled glucose to the mucosal solution. Glucose uptake decreased (P < 0.05) by >50% in comparison with control after mucosal addition of the SGLT-1 inhibitor, phlorizin (100 µmol/L). Serosal preincubation with 100 µmol/L epinephrine increased (P < 0.05) the phlorizin-sensitive glucose uptake in the absence and presence of indomethacin (10 µmol/L). The effect of epinephrine was simulated by ß- (100 µmol/L isoproterenol) and ß₂-receptor agonists (10 µmol/L terbutaline), as well as by direct stimulation of adenylyl cyclase (10 µmol/L forskolin). The serosal addition of methoxamine, clonidine, dobutamine or BRL 37344 had no effect. Inhibition of protein kinase A with 2 µmol/L H 89 completely abolished the stimulation of glucose uptake by epinephrine. We conclude that ruminal SGLT-1 can be stimulated via ß₂-dependent generation of cyclic adenosine monophosphate.

KEY WORDS: • glucose absorption • cAMP • epinephrine • rumen • sheep

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Ruminants cover their energy demands predominantly by microbial fermentation of carbohydrates to short-chain fatty acids. Glucose is usually considered to be only a short-lived intermediate during ruminal fermentation (1 ). However, after consumption of large amounts of easily fermentable carbohydrates, large increases in the ruminal concentration of free glucose (>10 mmol/L) can occur and favor lactic acid production (2 ). The high glucose availability in the rumen finally leads to severe bacterial dysfermentation and ruminal lactic acidosis (2 ,3 ). Absorption of glucose from the rumen could be an important mechanism to decrease the incidence of lactic acidosis. In principle, pathways to recover glucose from ruminal contents are available, namely, the sodium glucose-linked transporter, SGLT-1⁴ (4 ,5 ). Studies in vivo demonstrated efficient glucose clearance from the washed and temporarily isolated reticulorumen of sheep via this transporter (6 ).

An activation of the sympathetic system is a second important feature of the lactic acidosis syndrome during carbohydrate overload (7 ). In turn, the sympathetic mediator, epinephrine, was shown to stimulate intestinal glucose absorption in rats via ß₂-receptors and subsequent activation of the adenylyl cyclase pathway (8 ). If up-regulation of glucose absorption by epinephrine were also present in the ruminal epithelium, this could stabilize ruminal fermentation and counteract acidosis. Therefore, the possibility of adrenergic modulation of ruminal SGLT-1 function was investigated in the present study.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Animals and preparation of epithelia.

Adult (2–4 y old) female sheep (Ovis aries) of the Merino breed were obtained from the University’s Teaching and Trial Manor (Oberholz, Germany). They had free access to meadow hay, ⁵ mineral blocks and water at least 2 wk before the experiments. Sheep were slaughtered according to the Good Manufacturing Practice standards of meat production at the faculty’s abattoir. Immediately after exsanguination, the gastrointestinal tract was removed from the abdominal cavity. Stripped ruminal epithelia were prepared from the ventral ruminal sac and mounted in Ussing chambers (9 ). Epithelial preparations were incubated with 15 mL buffer solution on their mucosal (i.e., lumen-oriented) and serosal (i.e., blood-oriented) sides under short-circuit conditions (5 ). Experiments were in accordance with the German Law on the Protection of Animals and were communicated to the Regierungspräsidium Leipzig (AZ 74–9162.11–01-T53/01).

Buffer solutions.

Buffer solutions used for washing, transport, and incubation of epithelia contained the following (mmol/L): 75 NaCl, 5 KCl, 1 CaCl₂, 1 MgCl₂, 1 NaH₂PO₄, 2 Na₂HPO₄, 1 L-glutamine, 10 sodium acetate, 10 sodium propionate, 10 butyric acid, 5 sodium-D/L-lactate, 10 N-(2-hydroxyethyl)piperazine-N'-(2-ethanesulfonic acid) (HEPES, free acid), 40 mannitol and 10 NaOH (283–293 mosmol/kg; pH 7.36–7.44). Solutions were gassed with 100% oxygen. Temperature was held at 37°C using either Dewar containers (washing and transport buffer) or thermostated water jackets (incubation buffer).

Glucose uptake technique.

A technique was developed to study short-term regulation of SGLT-1 in the ruminal epithelium. Using glucose-free buffer solution (see above), epithelia were incubated in Ussing chambers for at least 1 h. Thereafter, glucose (spiked with 50 kBq [¹⁴C]glucose) was added to a final concentration of 200 µmol/L to the bathing solution on the mucosal side. After 1 min of incubation with glucose, epithelia were washed three times with ice-cold buffer solution to stop protein-mediated transport processes. Ussing chambers were taken off their holders and epithelia were transferred to a precooled, self-made lysing device in <1 min. The lysing device consisted of a flat teflon plate on which to place the epithelia (mucosal side up) and anodized aluminum cylinders fixed over the epithelia. Epithelial cells previously exposed to the uptake buffer were lysed by applying 4 mL ice-cold NaOH (100 mmol/L) into the aluminum cylinders for 3 min. Cornified aggregates were removed from the lysate by centrifugation (3000 x g, 15 min). Glucose and protein contents were determined in the lysate in duplicate. Glucose was measured by scintillation counting (WALLAC 1409 LSC; Berthold, Bad Wilbach, Germany) after the addition of a liquid scintillation fluid (Aquasafe 300). Analysis of protein contents followed the method of Smith and co-workers (10 ).

Pharmacological modulation of glucose uptake.

The inhibitor of SGLT-1, phlorizin, was added to the mucosal side in a final concentration of 100 µmol/L. The influence of the sympathetic system on glucose uptake was tested by serosal addition of epinephrine (100 µmol/L, final concentration) or specific adrenoceptor agonists. Selective agonists for adrenoceptor characterization were methoxamine (₁), clonidine (₂), and isoproterenol (ß) in final concentrations of 100 µmol/L (11 ). For subclassification of ß-receptors, dobutamine (ß₁), terbutaline (ß₂) and BRL 37344 (ß₃) were used in final concentrations of 10 µmol/L (12 ). Phlorizin, epinephrine and selective adrenergic agonists were added 15 min before mucosal glucose addition. Prostanoid production in the epithelial preparations was suppressed by bilateral addition of indomethacin (10 µmol/L, final concentration) during preparation and incubation. A possible involvement of cAMP in the signaling pathway of epinephrine was investigated by blocking protein kinase A (PKA) with H 89 (2 µmol/L, final bilateral concentration) during the whole incubation period. Epithelial cAMP production was stimulated by bilateral application of forskolin (10 µmol/L, final concentration) 15 s before mucosal glucose addition.

Phlorizin was dissolved in ethanol; H 89 was dissolved in dimethyl sulfoxide. Other substances were diluted in bidistilled water. Control epithelia received the solvents only.

The allotment of epithelia to different pharmacologic treatments was based on their tissue conductance values 30 min after mounting. Epithelial tissues used for direct comparison of different treatments were not allowed to differ in their conductance values by >30%.

Statistics.

Arithmetic means are presented together with their SEM. Differences between two means were established by Student’s paired t test. Factorial designs were analyzed by three-way ANOVA (Fig. 1) or repeated-measures two-way ANOVA (Fig. 2) . After ANOVA, groups that differed were isolated by Student-Newman-Keul’s test. Paired or repeated-measures tests were used whenever possible to account for the variability of control uptake in different animals. All hypothesis were tested with = 0.05, using the statistical software Jandel SigmaStat 2.0 (SPSS, Chicago, IL).

View larger version (22K): [in this window] [in a new window]   FIGURE 1 Influence of epinephrine (Epi), cyclooxigenase inhibition and protein kinase A (PKA) inhibition on apical glucose uptake by ruminal epithelia in the absence or presence of phlorizin. Epinephrine (100 µmol/L, serosally) and phlorizin (100 µmol/L, mucosally) were added to Ussing-chambered ruminal epithelia 15 min before a 1-min glucose uptake period. At the beginning of the experiment, some epithelia also received indomethacin (10 µmol/L, bilaterally; B, C) ± the inhibitor of PKA, H 89 (2 µmol/L, bilaterally; C). Data represent means + SEM, n = 8 epithelia of four sheep (A) or n = 6 epithelia of six sheep (B, C). Epinephrine increased glucose uptake independently of the presence of indomethacin but only in the absence of both phlorizin and H 89 (P < 0.05, see Results).

View larger version (20K): [in this window] [in a new window]   FIGURE 2 Influence of forskolin on apical glucose uptake by ruminal epithelia. The stimulator of adenylyl cyclase, forskolin (10 µmol/L), was applied 15 s before a 1-min glucose uptake period to both sides of ovine ruminal epithelia in the mucosal absence or presence of phlorizin (100 µmol/L). Indomethacin (10 µmol/L) was present bilaterally. Values represent means + SEM, n = 10 epithelia of five sheep. Forskolin stimulated glucose uptake but only in the absence of phlorizin (P < 0.05, see Results).

Oxygen was supplied by Messer Griesheim (Krefeld, Germany). D-[U-¹⁴C]glucose and Aquasafe 300 Plus were purchased from Amersham Pharmacia Biotech (Freiburg, Germany) and Zinsser Analytic (Maidenhead, UK), respectively. Clonidine and forskolin were obtained from Calbiochem (San Diego, CA) and epinephrine from Fluka (Buchs, Switzerland). All other chemicals were supplied by either Merck (Darmstadt, Germany) or Sigma-Aldrich (Deisenhofen, Germany).

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Glucose uptake under control conditions.

Without pharmacologic modulation, apical glucose uptake was 52.0 ± 8.3 pmol/(mg protein · min) (n = 8; Fig. 1A ). The contribution of SGLT-1 to total glucose uptake was estimated by inhibiting SGLT-1 with phlorizin (100 µmol/L). Phlorizin-sensitive uptake was 31.3 ± 6.5 pmol/(mg protein · min) (Fig. 1 A). Despite controlled prefeeding, large variations of total and phlorizin-sensitive glucose uptake existed among sheep.

Effect of epinephrine and role of prostanoids.

The effect of epinephrine (100 µmol/L) was tested in a 3 x 3 factorial design (Fig. 1 A and B). We applied 100 µmol/L phlorizin to evaluate whether a suspected adrenergic effect was SGLT-1 specific, and cyclooxygenase was inhibited by 10 µmol/L indomethacin (13 ) to exclude or verify indirect effects of epinephrine via cyclooxygenase metabolites (14 ,15 ). Glucose uptake was inhibited by phlorizin (P < 0.01) and stimulated by epinephrine (P < 0.05). The interaction between phlorizin and epinephrine (P < 0.01) showed that stimulation by epinephrine depended on the absence of phlorizin (P < 0.05, Fig. 1 A and B). Indomethacin had no effect on glucose uptake and did not influence the effect of epinephrine.

Involvement of cAMP in adrenergic stimulation.

In the intestinal epithelium of rats, the stimulatory effect of epinephrine on glucose absorption is signaled intracellularly via adenylyl cyclase activation and subsequent generation of cAMP (8 ). To elucidate a possible involvement of cAMP in the ruminal effect of epinephrine, the enzyme distal to adenylyl cyclase (i.e., PKA) was inhibited specifically with H 89 (16 ,17 ). This was done in a 3 x 3 factorial design by applying 100 µmol/L epinephrine, 2 µmol/L H 89 and 100 µmol/L phlorizin (in the presence of indomethacin, Fig. 1 B and C). Probability levels (P) for the overall effects of epinephrine, H 89, and phlorizin were 0.061, 0.057, and < 0.01, respectively. Given the interaction among epinephrine, H 89 and phlorizin (P < 0.05), epinephrine stimulated glucose uptake only in the absence of both H 89 and phlorizin (P < 0.05, Fig. 1 B and C).

The results presented in Figure 1 indicate that stimulation by epinephrine affects SGLT-1 specifically and requires activation of PKA by cAMP. Stimulation of SGLT-1 by cAMP was further investigated in a 2 x 2 factorial design using 10 µmol/L forskolin [direct activator of adenylyl cyclase; (18 )] and 100 µmol/L phlorizin (Fig. 2 ). Forskolin (P < 0.05) and phlorizin (P < 0.01) interacted to affect glucose uptake (P < 0.05). Forskolin simulated the effect of epinephrine by increasing glucose uptake only in the absence of phlorizin (P < 0.05, Fig. 2 ).

Characterization of adrenoceptor subtype.

Specific adrenoceptor agonists were used to elucidate type and subtype of the receptor involved. Glucose uptake increased (P < 0.05) after serosal preincubation of epithelia with 100 µmol/L of the ß-agonist, isoproterenol (Fig. 3 ). Methoxamine and clonidine (100 µmol/L, ₁- and ₂-agonists, respectively) did not affect apical glucose uptake (data not shown). Of the ß-receptor subtype agonists, only the ß₂-agonist, terbutaline (10 µmol/L; Fig. 3 ), stimulated apical glucose uptake (P < 0.05). Dobutamine and BRL 37344 (10 µmol/L, ß₁- and ß₃-agonists, respectively) had no effects (data not shown).

View larger version (34K): [in this window] [in a new window]   FIGURE 3 Effects of ß-adrenoceptor agonists on apical glucose uptake by ruminal epithelia. The ß-agonist, isoproterenol (100 µmol/L), or the ß2-agonist, terbutaline (10 µmol/L), were applied 15 min before a 1-min glucose uptake period to the serosal sides of ovine ruminal epithelia in the presence of indomethacin (10 µmol/L, bilaterally). Values represent mean uptakes + SEM, n = 12 (left panel) or n = 7 epithelia (right panel) of four sheep. *Differences are indicated, P < 0.05.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

In the epithelial preparations used, >50% of the 1-min glucose uptake under control conditions represented SGLT-1–dependent glucose transport as demonstrated by its sensitivity to phlorizin (Figs. 1 and 2) . The phlorizin-sensitive part of glucose uptake was selectively increased by serosal application of epinephrine (Fig. 1) . Consequently, epinephrine was verified for the first time to be a modulator of epithelial transport in the rumen, specifically with regard to SGLT-1 function.

Adrenergic receptors elicit their effects in certain tissues by modulation of PG synthesis via cyclooxygenase (14 ,15 ). PGE₂, in turn, is part of the signaling cascade in cholinergic muscarinic stimulation of the rat intestinal SGLT-1 (24 ). Therefore, we had to evaluate the possibility that the observed effect of epinephrine was secondarily mediated via prostanoids especially, in view of the proven presence of PGE₂ receptors in the ruminal epithelium (25 ). The stimulatory effect of epinephrine on glucose uptake persisted after pretreatment with the cyclooxygenase inhibitor, indomethacin (Fig. 1 B). Consequently, PG do not seem to play a role in adrenergic stimulation of the ruminal SGLT-1. On the other hand, the intracellular cAMP pathway is central to the epinephrine effect in the ruminal epithelium. The general ability of cAMP to stimulate apical glucose uptake rapidly (i.e., within seconds) could be demonstrated by adenylyl cylase activation with forskolin (Fig. 2) . This first evidence on cAMP-dependent stimulation of the ovine SGLT-1 is consistent with results of numerous studies in heterologous SGLT-1 proteins (8 ,20 ,21 ,24 ,26 ). We further investigated the specific implementation of cAMP in the signaling pathway of epinephrine by pharmacologic inhibition of cAMP-activated PKA. At the low concentration chosen, H 89 is a specific PKA inhibitor (16 ,17 ). The abolition of adrenergic stimulation of the phlorizin-sensitive glucose uptake by H 89 (Fig. 1 C), therefore, points to the necessity of cAMP signaling distal to the adrenergic receptor.

The receptor subtype responsible for adrenergic activation of SGLT-1 was identified as ß₂ (Fig. 3) . Consequently, epinephrine effects in the forestomach of ruminants bear similarities to the effect in the intestine of rats (8 ). SGLT-1 is activated via ß₂ receptors and the cAMP/PKA pathway in both tissues. However, the physiologic importance is likely different in these tissues. Adrenergic stimulation of intestinal glucose absorption could increase blood glucose levels under conditions of stress or exercise, whereas very little glucose is freely available in the rumen under most circumstances [<0.7 mmol/L, (27 )]. An epinephrine-induced increase in the ruminal capacity for glucose absorption would thus contribute very little to plasma glucose availability during stress and exercise. By contrast, intraruminal glucose levels can rise suddenly to >10 mmol/L in acidotic and preacidotic feeding conditions (2 ,3 ). Under these circumstances, adrenergic enhancement of ruminal glucose extraction would counteract bacterial dysfermentation and acidosis. However, a final assessment of the latter conclusion has yet to consider several other facts such as the adrenergic influence on splanchnic blood flow (28 ) and the epithelial damage occurring early in acidosis (29 ). In addition, prolonged effects of cAMP on the ruminal epithelium include impairment of Na⁺ driving forces (25 ), which may counteract direct stimulation of SGLT-1 in later stages. Further studies are required to address these questions.

	FOOTNOTES

 
¹ Presented in part in abstract form [Aschenbach, J. R., Borau, T. & Gäbel, G. (2001) Adrenergic modulation of glucose absorption in the ruminal epithelium of sheep. IUPS Abstract CD-ROM, 486.]

² Supported by the H. Wilhelm Schaumann Foundation.

⁴ Abbreviations used: PG, prostaglandin; PKA, protein kinase A; SGLT, sodium glucose-linked transport.

⁵ The hay contained 93.3% dry matter with the following approximate composition (in % of dry matter): 92.9% organic matter, 10.7% crude protein, 31.2% crude fiber, 3.0% ether extract, 48.0% nitrogen-free extractives; energy content: 8.53 MJ/kg dry matter.

Manuscript received 11 December 2001. Initial review completed 12 January 2002. Revision accepted 11 March 2002.

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

1. Bergman, E. N. (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev. 70:567-590.[Abstract/Free Full Text]

2. Ganter, M., Bickhardt, K., Winicker, M. & Schwert, B. (1993) Experimental studies of the pathogenesis of rumen acidosis in sheep. Zentbl. Vetmed. Riehe A 40:731-740.

3. Owens, F. N., Secrist, D. S., Hill, W. J. & Gill, D. R. (1998) Acidosis in cattle: a review. J. Anim. Sci. 76:275-286.[Abstract/Free Full Text]

4. Zhao, F. Q., Okine, E. K., Cheeseman, C. I., Shirazi-Beechey, S. P. & Kennelly, J. J. (1998) Glucose transporter gene expression in lactating bovine gastrointestinal tract. J. Anim. Sci. 76:2921-2929.[Abstract/Free Full Text]

5. Aschenbach, J. R., Wehning, H., Kurze, M., Schaberg, E., Nieper, H., Burckhardt, G. & Gäbel, G. (2000) Functional and molecular biological evidence of SGLT-1 in the ruminal epithelium of sheep. Am. J. Physiol. 279:G20-G27.[Abstract/Free Full Text]

6. Aschenbach, J. R., Bhatia, S. K., Pfannkuche, H. & Gäbel, G. (2000) Glucose is absorbed in a sodium-dependent manner from forestomach contents of sheep. J. Nutr. 130:2797-2801.[Abstract/Free Full Text]

7. Svendsen, C. K. (1979) Effects of acute lactic acidosis on some hemodynamic and hematologic values in three cows. Nord. Vetmed. 31:497-507.

8. Ishikawa, Y., Eguchi, T. & Ishida, H. (1997) Mechanism of beta-adrenergic agonist-induced transmural transport of glucose in rat small intestine. Regulation of phosphorylation of SGLT1 controls the function. Biochim. Biophys. Acta 1357:306-318.[Medline]

9. Gaebel, G., Bell, M. & Martens, H. (1989) The effect of low mucosal pH on sodium and chloride movement across the isolated rumen mucosa of sheep. Q. J. Exp. Physiol. 74:35-44.[Abstract/Free Full Text]

10. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J. & Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:76-85.[Medline]

11. Lee, E. K., Chan, V. C., Chang, J. P., Yunker, W. K. & Wong, A. O. (2000) Norepinephrine regulation of growth hormone release from goldfish pituitary cells. I. Involvement of 2 adrenoreceptor and interactions with dopamine and salmon gonadotropin-releasing hormone. J. Neuroendocrinol. 12:311-322.[Medline]

12. Brechet, S., Plaisancie, P., Dumoulin, V., Chayvialle, J. A., Cuber, J. C. & Claustre, J. (2001) Involvement of beta1- and beta2- but not beta3-adrenoceptor activation in adrenergic PYY secretion from the isolated colon. J. Endocrinol. 168:177-183.[Abstract]

13. Sim, S. S., Choi, J. C., Min, D. S., Rhie, D. J., Yoon, S. H., Hahn, S. J., Kim, C. J., Kim, M. S. & Jo, Y. H. (2001) The involvement of phospholipase A₂ in ethanol-induced gastric muscle contraction. Eur. J. Pharmacol. 413:281-285.[Medline]

14. Borda, E. S., Peredo, H. & Gimeno, M. F. (1983) Alpha adrenergic stimulation modified prostaglandins release in vas deferens. Prostaglandins 26:701-710.[Medline]

15. Schultheiss, G. & Diener, M. (2000) Adrenoceptor-mediated secretion across the rat colonic epithelium. Eur. J. Pharmacol. 403:251-258.[Medline]

16. Geilen, C. C., Wieprecht, M., Wieder, T. & Reutter, W. (1992) A selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-bromocinnamyl(amino)ethyl]-5-soquinolinesulfonamide (H-89), inhibits phosphatidylcholine biosynthesis in HeLa cells. FEBS Lett. 309:381-384.[Medline]

17. de Rooij, J, Zwartkruis, F. J., Verheijen, M. H., Cool, R. H., Nijman, S. M., Wittinghofer, A. & Bos, J. L. (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature (Lond.) 396:474-477.[Medline]

18. Bajo, A., Carrero, I., Hristov, R. L., Valenzuela, P., Martinez, P., Cortes, J., Prieto, J. C. & Guijarro, L. G. (2000) Impairment of adenylate cyclase activity and G-proteins in human uterine leiomyoma. Tissue Cell 32:399-404.[Medline]

19. Collie, N. L., Zhu, Z., Jordan, S. & Reeve, J. R., Jr (1997) Oxyntomodulin stimulates intestinal glucose uptake in rats. Gastroenterology 112:1961-1970.[Medline]

20. Stümpel, F., Scholtka, B. & Jungermann, K. (1997) A new role for enteric glucagon-37: acute stimulation of glucose absorption in rat small intestine. FEBS Lett. 410:515-519.[Medline]

21. Stümpel, F., Scholtka, B., Hunger, A. & Jungermann, K. (1998) Enteric glucagon 37 rather than pancreatic glucagon 29 stimulates glucose absorption in rat intestine. Gastroenterology 115:1163-1171.[Medline]

22. Hyun, H. S., Onaga, T., Mineo, H. & Kato, S. (1997) Responses of glucose absorption and fructose absorption to prostaglandin E₂ in intestinal loops of sheep. Res. Vet. Sci. 62:153-157.[Medline]

23. Scholtka, B., Stümpel, F. & Jungermann, K. (1999) Acute increase, stimulated by prostaglandin E2, in glucose absorption via the sodium dependent glucose transporter-1 in rat intestine. Gut 44:490-496.[Abstract/Free Full Text]

24. Stümpel, F., Scholtka, B. & Jungermann, K. (2000) Stimulation by portal insulin of intestinal glucose absorption via hepatoenteral nerves and prostaglandin E₂ in the isolated, jointly perfused small intestine and liver of the rat. Ann. N.Y. Acad. Sci. 915:111-116.[Medline]

25. Gäbel, G., Butter, H. & Martens, H. (1999) Regulatory role of cAMP in transport of Na⁺, Cl^- and short-chain fatty acids across sheep ruminal epithelium. Exp. Physiol. 84:333-345.[Abstract]

26. Wright, E. M., Hirsch, J. R., Loo, D.D.F. & Zampighi, G. A. (1997) Regulation of Na⁺/glucose cotransporters. J. Exp. Biol. 200:287-293.[Abstract]

27. Kajikawa, H., Amari, M. & Masaki, S. (1997) Glucose transport by mixed ruminal bacteria from a cow. Appl. Environ. Microbiol. 63:1847-1851.[Abstract]

28. Loj, W. (1974) Pharmacological analysis of regulation of the intestinal blood flow in sheep. The effect of autacoids and catecholamines. Acta Physiol. Pol. 25:263-273.[Medline]

29. Aschenbach, J. R. & Gäbel, G. (2000) Effect and absorption of histamine in sheep rumen: significance of acidotic epithelial damage. J. Anim. Sci. 78:464-470.[Abstract/Free Full Text]

This article has been cited by other articles:

				G. B. Penner, J. R. Aschenbach, G. Gabel, R. Rackwitz, and M. Oba Epithelial Capacity for Apical Uptake of Short Chain Fatty Acids Is a Key Determinant for Intraruminal pH and the Susceptibility to Subacute Ruminal Acidosis in Sheep J. Nutr., September 1, 2009; 139(9): 1714 - 1720. [Abstract] [Full Text] [PDF]

				J. R. Aschenbach, S. Bilk, G. Tadesse, F. Stumpff, and G. Gabel Bicarbonate-dependent and bicarbonate-independent mechanisms contribute to nondiffusive uptake of acetate in the ruminal epithelium of sheep Am J Physiol Gastrointest Liver Physiol, May 1, 2009; 296(5): G1098 - G1107. [Abstract] [Full Text] [PDF]

				W. A. Awad, J. R. Aschenbach, F. M. C. S. Setyabudi, E. Razzazi-Fazeli, J. Bohm, and J. Zentek In Vitro Effects of Deoxynivalenol on Small Intestinal D-Glucose Uptake and Absorption of Deoxynivalenol Across the Isolated Jejunal Epithelium of Laying Hens Poult. Sci., January 1, 2007; 86(1): 15 - 20. [Abstract] [Full Text] [PDF]

				R. R. Pencek, Y. Koyama, D. B. Lacy, F. D. James, P. T. Fueger, K. Jabbour, P. E. Williams, and D. H. Wasserman Prior exercise enhances passive absorption of intraduodenal glucose J Appl Physiol, September 1, 2003; 95(3): 1132 - 1138. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Aschenbach, J. R. Articles by Gäbel, G. Search for Related Content PubMed PubMed Citation Articles by Aschenbach, J. R. Articles by Gäbel, G.