Effect of tannic acid on brush border disaccharidases in mammalian intestine

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1 Indian Journal of Experimental Biology Vol. 45, April 2007, pp Effect of tannic acid on brush border disaccharidases in mammalian intestine Ayesha Chauhan, Shiffalli Gupta & Akhtar Mahmood* Department of Biochemistry, Panjab University, Chandigarh , India Received 20 June 2006; revised 21 December 2006 Tannic acid is a glucoside (penta-m-digallolyl-glucose), which exhibits a wide variety of physiological functions. Around neutral ph, 0.4 mm tannic acid produced 84% inhibition of rat brush border sucrase activity, but 35-40% enzyme inhibition was observed in the rabbit intestine at 0.08 mm concentration. In the mice, 74-77% enzyme inhibition was observed at 0.05 mm concentration of tannic acid. The observed inhibition was reversible in rat intestine. Tannic acid (0.2 mm) also inhibited lactase (18% in adult and 71% in suckling animals), maltase (76%) and trehalase (88%) activities in rat intestine. ph versus activity curves showed that 0.2 mm tannic acid inhibited enzyme activity in rat by 91% at ph 5.5 which was reduced to 14% at ph 8.5 compared to the respective controls. In the rabbit 18-60% enzyme inhibition was noticed below ph 7.0, however at ph 8.5, it was of the order of 38%. Kinetic analysis revealed that tannic acid is a competitive inhibitor of rat brush border sucrase at ph 6.8. Effect of tannic acid together with various SH group reacting reagents revealed that the enzyme inhibition is additive in nature, suggesting the distinct nature of binding sites on the enzyme for these compounds. The results suggest that tannic acid is a potent inhibitor of intestinal brush border disaccharidases, and could modulate the intestinal functions. Keywords: Competitive inhibition, Intestinal disaccharidases, Mice, ph effects, Rat, Rabbit brush border sucrase, Tannic acid Tannins are a group of compounds belonging to the phenolics class of secondary metabolites in plants. These compounds, in particular tannic acid, exhibit a wide variety of activities and physiological functions 1. Chemically, it is a penta m digalloyl glucose in which each of the five-hydroxyl groups of the sugar residue is esterified with a molecule of digallic acid 2. Tebib et al 3 reported that porcine jejunal brush border enzymes are inhibited by hydrolysable tannins. Tannic acid also inhibits amino acid and sugar absorption in mouse intestine 4. Studies on the effect of tannic acid on the functional state of rat intestinal epithelium show an inhibition of oxygen consumption and succinic dehydrogenase activity in the homogenate and an increased excretion of sialic acid and glucosamine 5. Among the constituents of intestinal brush border membrane of the small intestine, the dimeric enzyme complex, sucrase isomaltase is the most abundant protein, accounting for all the sucrase activity, approximately 90% of isomaltase and 70-80% of maltase activities of the small intestine 6. Correspondent author Telephone: Fax: akhtarmah@yahoo.com Welsch et al. 7 reported that tannic acid inhibits nearly 80% of sucrase activity but oxidized tannic acid has no effect on enzyme activity. However, the underlying mechanism of sucrase inhibition by tannic acid is not known. Tannic acid has structural similarity to tris, a well-known inhibitor of brush border sucrase due to polyhydroxyl constellation of the molecule 8. Thus to elucidate the mechanism of interaction of tannic acid with intestinal brush border sucrase, detailed studies on the effect of tannic acid on brush border sucrase in rat intestine have been undertaken. The effect of tannic acid on brush border sucrase in rabbit and mice was also studied. These findings suggest that tannic acid is a potent competitive inhibitor of the rat brush border sucrase. The enzyme inhibition is modulated by ph and is reversible in nature. Tannic acid also impairs the activities of other disaccharidases in rat intestine. Materials and Methods All the chemicals used were of analytical grade, obtained either from E. Merck (India) or Glindia Ltd. Tannic acid, bovine serum albumin, 4- aminoantipyrine, glucose oxidase (Type V), glucose peroxidase, D-glucose and Tris were purchased from Sigma Chemical Company, Saint Louis (U.S.A).

2 354 INDIAN J EXP BIOL, APRIL 2007 Rat (Wistar strain), Rabbit (White New Zealand strain) and Mice (Balb c) were used. Animals were kept on standard pellet diet and had free access to water. Brush border membranes (BBM) were isolated and purified following the method of Kessler et al. 9. Starting from the ligament of trietz, cm intestine was removed from each animal species. In rat and mice, tissues from 2-3 animals were pooled. The final membrane preparation exhibited fold enrichment of brush border sucrase compared to the crude homogenate. The membrane preparation was stored at 20 C and used for various biochemical studies. At least 4 membrane preparations were used for various biochemical studies. Protein was estimated by the method of Lowry et al. 10, using bovine serum albumin as the standard. The activities of various brush border enzymes were determined in absence and presence of different concentrations ( mm) of tannic acid. Sucrase, maltase, trehalase and lactase activities were assayed by measuring D-glucose liberated from the respective disaccharides, using a glucose-oxidase-peroxidase system. The method used was a modification of the procedure described by Dahlqvist 11. Kinetic parameters of brush border sucrase were determined by assaying the enzyme activity at different sucrose concentrations (2-20 mm) in absence and presence of 0.2 mm tannic acid. K m and V max were calculated from straight lines obtained by plotting of 1/V vs 1/S, as described earlier 12. The effect of ph on tannic acid (0.2mM) interactions with brush border sucrase was studied by assaying the enzyme activity at ph 4.8, 5.5, 6.0, 6.5, 7.0, 7.2, 7.7 and 8.5. To examine whether the effect of tannic acid on brush border sucrase was reversible or irreversible, the enzyme preparation with or without tannic acid was dialyzed exhaustively overnight against 20 mm sodium maleate buffer ph 6.8, with constant stirring at 4 C. The buffer was changed every 4-6 hr. The concentration of tannic acid used was 0.4mM, while the protein concentration in enzyme preparation was 2.16 mg/ml. The effect of various reagents viz. 0.1 mm trihydroxyaminomethane (tris), 2mM sodium arsenite, 2mM dithionitrobenzoic acid and 4mM harmaline, on brush border sucrase in presence and absence of 0.2 mm tannic acid, was studied in vitro in rat intestine. All experiments were performed at least 4 times and enzyme assays were done in duplicates or triplicates. The enzyme activities were calculated and expressed as enzyme units/mg protein. One enzyme unit is defined as the amount of enzyme required to hydrolyze 1 μmole of the substrate to the product per minute under standard assay conditions. Statistical analysis of the data was done using the Students' t test. Differences between means with values P < 0.05 were considered significant. Results Addition of tannic acid ( mm) to the enzyme assay system (ph 6.8) showed a progressive decline in rat sucrase activity, from 21 to 84% inhibition at mm tannic acid concentration (Fig. 1a). Essentially a similar degree of enzyme inhibition was obtained (74 to 77%) at lower concentrations (0.05 mm) in the mice intestine (Fig. 1b). Fig. 1 Effect of tannic acid on brush border sucrase activity in (a) rat, (b) mice and (c) rabbit intestine. Values, expressed as units/mg protein are mean ± S.D. from 4 observations.

3 CHAUHAN et al.: DISACCHARIDASE INHIBITION BY TANNIC ACID 355 The effect of tannic acid on rabbit sucrase activity revealed that on increasing tannic acid concentration from 0.01 to 0.40 mm, inhibition of enzyme activity increased from 12 to 35% (Fig. 1c). Nearly 32% of the enzyme activity was inhibited at 0.08 mm tannic acid concentration and a further increase in tannic acid concentration by five-fold produced 35% enzyme inhibition. These observations indicate that compared to rat and murine sucrases, the rabbit enzyme is relatively resistant to inhibitory effects of tannic acid under in vitro conditions at ph 6.8. The results indicate that tannic acid inhibits the activity of brush border sucrase in the different animal species analysed, although the sensitivity of the enzyme to tannic acid varied, mice and rat being the most sensitive to inhibition, followed by rabbit sucrase. The effect of tannic acid on other disaccharidases viz: lactase, maltase and trehalase in rat intestine also was analyzed (Fig. 2). The results indicated that lactase activity in the adult animals was least sensitive to tannic acid, which showed 18% enzyme inhibition at 0.2 mm tannic acid concentration. However, in the suckling animals, lactase activity was inhibited to the tune of 71% under these conditions. Similarly, maltase and trehalase activities were reduced by 76-88% in presence of 0.2 mm tannic acid under the in vitro assay conditions. To analyze the kinetic basis of sucrase inhibition by tannic acid, the effect of varying substrate concentrations on rat sucrase activity was studied in presence and absence of 0.2 mm tannic acid. Double reciprocal plot of the data is shown in Fig. 3. This concentration of tannic acid was selected, since earlier experiments indicated that over 67% of the sucrase activity was inhibited by 0.2 mm tannic acid. There was no change in the V max of the enzyme (1.0 unit/mg protein) but the apparent K m was increased from 20 mm in the absence, to 50 mm in the presence of 0.2 mm tannic acid. These observations indicated that tannic acid is a competitive inhibitor of rat sucrase. The value of Ki calculated was mm. To further examine the interactions between brush border sucrase and tannic acid, the effect of ph on enzyme activity in rat intestine was studied in presence (0.2 mm) and absence of tannic acid (Fig. 4a). Between ph 4.8 to 8.5, a broad ph vs activity curve was obtained. Below ph 7.0, sucrase activity was markedly inhibited (by 78-91%) but at ph 8.5 the enzyme inhibition was 14% compared to controls. Thus, sucrase inhibition by tannic acid is ph-dependent; it is quite high in the acidic ph range but is reduced significantly at ph 8.5. Similar studies carried out with rabbit sucrase (Fig. 4b) indicated that compared to the control values, enzyme inhibition by tannic acid was relatively small (18-59%) below ph 6.0. However, between ph 6.5 to 7.7, enzyme inhibition was 65%. But at ph 8.5, sucrase inhibition by 0.08 mm tannic acid was 38%. These findings further corroborate the earlier contention that sucrase inhibition by tannic acid is ph-dependent. However, in rabbit, the inhibitory pattern was reverse compared to that observed in rat intestine. Thus, there is a species difference with regard to the sensitivity of sucrase inhibition by tannic acid as a function of ph. Fig. 2 Effect of tannic acid on brush border disaccharidases in adult rat intestine. However, lactase activity was assayed both in suckling and adult rat intestine. Values, expressed as units/mg protein are mean ± S.D. from 4 observations. Fig. 3 Double reciprocal plot for brush border sucrase in the absence ( ) and presence ( ) (0.2 mm) of tannic acid in rat intestine. V= enzyme units/mg protein. Each point is a mean of 2 preparations and enzyme assays are done in duplicates.

4 356 INDIAN J EXP BIOL, APRIL 2007 To examine whether the observed inhibition of sucrase activity by tannic acid is reversible or irreversible, the effect of tannic acid (0.2mM) removal by exhaustive dialysis of enzyme preparation was studied. Addition of tannic acid reduced the enzyme activity by 63%. But upon dialysis of the enzyme preparation containing tannic acid, the enzyme activity was restored to nearly 87% of the control value (Table 1). The mode of action of tannic acid on brush border sucrase was also studied by assaying the enzyme activity in the presence of certain known modulators of the enzyme activity, such as sodium-arsenite, dithionitrobenzoic acid (DTNB) and harmaline (Fig. 5). Addition of both tannic acid (0.1 mm) and tris (0.1 mm) produced enzyme inhibition of the order of 82%, in contrast to 65% inhibition observed in presence of tannic acid (0.1 mm) alone. Thus, sucrase inhibition in presence of tris and tannic acid is additive in nature, suggesting that both the molecules may be acting at different sites on the enzyme molecule. Similar results were obtained when the effect of tannic acid was studied in the presence of 2 mm sodium-arsenite or 4 mm harmaline and 2 mm DTNB, which also suggested that enzyme inhibition was additive in nature, under these conditions. Table 1 Effect of dialysis on tannic acid inhibition of brush border sucrase in rat intestine Assay System Activity (%) Control (Tannic acid=0mm) mM Tannic acid (Undialysed) mM Tannic acid (Dialysed) 87 Control (Tannic acid=0mm) mM Tannic acid (Undialysed) mM Tannic acid (Dialysed) 68 Fig. 4 Effect of tannic acid on brush border sucrase as a function of ph in (a) rat and (b) rabbit intestine. Values, expressed as units/mg protein are mean ± S.D. from 4 observations. Fig. 5 Effect of tannic acid, in presence and absence of certain reagents, on brush border sucrase in rat intestine. Values, expressed as units/mg protein are mean ± S.D. from 4 observations.

5 CHAUHAN et al.: DISACCHARIDASE INHIBITION BY TANNIC ACID 357 Discussion The results presented herein indicate that tannic acid is a potent inhibitor of brush border sucrase in rat, rabbit and mice intestine. These findings are in agreement with earlier studies by Welsch et al. 7, who showed that tannic acid and gallic acid inhibit rat sucrase activity by 40-80% in vitro. Feeding grape seed tannins at a dose of 2% is also reported to significantly impair the activities of various brush border enzymes in rat intestine 3. Toda et al. 13 also reported the inhibition of maltase-glucoamylase activity by ellagi- and gallotannins in rat intestine. Kinetic studies revealed that at ph 6.8, tannic acid is a fully competitive inhibitor of brush border sucrase in rat intestine. Since tannic acid is a polyhydroxyl compound and is structurally similar to substrate, thus likely to compete with sucrose. However, the possibility that tannic acid, being bulky in nature, may bind at a site, away from the active site of the enzyme, and overshadows the enzyme active center and thus behaves as a fully competitive inhibitor cannot be ruled out 14. Such a finding further corroborates that observed sucrase inhibition by tannic acid was essentially reversible. The comparison of I 50 (inhibitor concentration at which enzyme is 50% inhibited) of enzyme inhibition with well-known competitiveinhibitors of sucrase, such as tris, indicated that value was around 0.2 mm for tannic acid, compared to 2 mm of tris and 4 mm for harmaline 15. This indicates that tannic acid was times strong inhibitor of the enzyme compared to these compounds. Earlier studies have shown that sucrase undergoes ionization first in the acidic ph, around 5.2 and a second proton is dissociated as the ph is increased to 8.4 (ref. 16). It has been suggested that in the acidic ph, one key proton Hx behaves as a fully competitive inhibitor and another proton Hy, behaves as a mixed type partially non-competitive inhibitor. Loss of both Hx and Hy, and retention of Hz (proton that is the component of the basic ionization constant) are postulated to be required to yield the fully active monoprotonated enzyme form 8. The present findings indicate that enzyme inhibition was strong in the acidic ph range, but was considerably reduced (20-30% inhibition) ph 8.5. These findings are also in contrast to those observed with Tris, which is a potent inhibitor of sucrase at alkaline ph but exhibits no effect in the acidic ph 8. Thus ionization of the enzyme in the acidic ph makes it more susceptible to inhibition by tannic acid, whereas deprotonation around ph 8.5 interfere with enzyme inhibition process. However, these findings are in contrast to the results obtained with rabbit sucrase, where the enzyme was more sensitive to inhibition by tannic acid in the alkaline ph range. Because of the complex structure of tannic acid, it is difficult to speculate about the ionization of the groups in the molecule. Therefore, the observed inhibition is presumably related to the ionization of the enzyme protein. Studies using tris, sodium-arsenite, harmaline and dithionitrobenzoic acid suggested that the binding site of tannic acid is distinct from that of these compounds, since enzyme inhibition was additive in nature when tannic acid was added together with these compounds. In addition to sucrase, the tannic acid inhibited lactase, maltase and trehlase activities, although the degree of enzyme inhibition varied. Interestingly, lactase inhibition in adult rat intestine was only 18%, whereas in suckling rats, it was around 70%. This may be related to the fact that lactase activity in the adult animals is considerably low, whereas enzyme levels are quite high in suckling animals 17,18. This may indicate that lactase protein in adult animals is structurally distinct from that in the suckling animals. Buller et al. 19 showed that in the peri-natal period, lactase is sialylated, whereas in adult tissue, the enzyme is fucosylated. This difference in glycosylation pattern of the enzyme has been suggested to be responsible for low enzyme activity in the mature rat tissue 20. In conclusion, the present data indicate that tannic acid strongly inhibits brush border sucrase in various animal species. Kinetic studies indicate that tannic acid is a competitive inhibitor of the enzyme in acidic ph, which is in contrast to the action of tris, a wellknown competitive inhibitor of disaccharidases under alkaline conditions 8. Further, since enzyme inhibition is observed at low concentrations ( mm) of tannic acid, it makes the compound a strong inhibitor, which may be of significance and responsible for observed aberrations of intestinal functions upon the consumption of tannic acid containing diets. References 1 Carbonaro M, Grant G & Pustai A, Evaluation of polyphenol bioavailability in rat small intestine, Eur J Nutr, 40 (2001) Jain A, Martin M C Praveen N, Khan N U, Parish J N & Hadi S M, Reactivities of flavanoids with different

6 358 INDIAN J EXP BIOL, APRIL 2007 substituents for the cleavage of DNA in the presence of Cu (II), Phytother Res, 13 (1999) Tebib K, Rouanet J M & Besancon P, Effect of grape seed tannins on the activity of some rat intestinal enzyme activities, Enzyme Protein, 48 ( ) Karasov W H, Meyer M W & Darken B W, Tannic acid inhibition of amino acid and sugar absorption by mouse and vole intestine: Tests following acute and subacute exposure, J Chem Ecology, 18 (1992) Mitjavila S, Lacombe C, Carrera G & Derache R, Tannic acid and oxidized tannic acid on the functional state of rat intestinal epithelium, J Nutr, 107 (1977) Semenza G, Carbohydrate metabolism and its disorders (Academic Press, London), 3 (1981) Welsch C A, Lachance P A & Wasserman B P, Effects of Native and Oxidized Phenolic Compounds on Sucrase Activity in Rat Brush Border Membrane, J Nutr, 119 (1989) Vasseur M, Frangne R, Cauzac M, Mahmood A & Alvarado F, ph dependent inhibitory effect of tris and lithium ions on intestinal brush border sucrase, J Enzyme Inhibition, 4 (1990) Kessler M, Acuto O, Storelli C, Murer M & Semenza G, A Modified Procedure for the rapid preparation of efficiently transporting vesicles from small intestinal brush border membrane. Their use in investigating some properties of D- glucose and choline transport systems, Biochem Biophys Acta, 506 (1978) Lowry H, Rosenbrough N J, Farr A L & Randall R J, Protein measurement with Folin Phenol Reagent, J Biol Chem, 193 (1951) Dahlqvist A, Methods for assay of intestinal disaccharidases, Anal Biochem, 7 (1964) Dowd J & Riggs D S, A comparison of estimates of Michaelis-Menten kinetic constants from various Linear Transformations, J Biol Chem, 240 (1965) Toda M, Kawabata J & Kasai T, Inhibitory effects of ellagi and gallotannins on rat intestinal alpha-glucosidase complexes, Biosci Biotechnol Biochem, 65 (2001) Mahmood A & Alvarado F, Harmaline interaction with Sodium-Binding sites in intestinal Brush Border Sucrase, Biochem Biophys Acta, 483 (1977) Kaur N, Kaur J & Mahmood A, Effect of harmaline on rat intestinal brush border sucrase activity, Indian J Biochem Biophys, 39 (2002) Vasseur M, Tellier C & Alvarado F, Sodium-Dependent Activation of Intestinal Brush Border Sucrase: Correlation with Activation by Deprotonation from ph 5 to 7, Arch Biochem Biophys, 218 (1982) Henning S J, Ontogeny of enzymes in the small intestine, Ann Rev Physiol, 47 (1985) Tadesse K, The effect of continued feeding on physiological amounts of lactose on the level of intestinal lactose and other disaccharidase enzyme activities in rat, Exp Physiol, 75 (1990) Buller H A, Rings E H, Pajkrt D, Montgomery R K & Grand R J, Glycosylation of lactase-phlorizin hydrolase in rat small intestine during development, Gastroenterology, 98 (1990) Kaur K, Mahmood S & Mahmood A, The susceptibility of lactase to luminal proteases in developing rat intestine, Indian J Gastroenterol, 25 (2006) 179.

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