Article pubs.acs.org/JAFC
Dietary Phenolic Compounds Selectively Inhibit the Individual Subunits of Maltase-Glucoamylase and Sucrase-Isomaltase with the Potential of Modulating Glucose Release Meric Simsek,† Roberto Quezada-Calvillo,§,# Mario G. Ferruzzi,† Buford L. Nichols,# and Bruce R. Hamaker*,† †
Whistler Center for Carbohydrate Research and Department of Food Science, Purdue University, West Lafayette, Indiana 47907, United States § Department of Chemistry, Universidad Autonoma de San Luis Potosi, San Luis Potosi, Mexico # USDA-ARS, Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030, United States S Supporting Information *
ABSTRACT: In this study, it was hypothesized that dietary phenolic compounds selectively inhibit the individual C- and Nterminal (Ct, Nt) subunits of the two small intestinal α-glucosidases, maltase-glucoamylase (MGAM) and sucrase-isomaltase (SI), for a modulated glycemic carbohydrate digestion. The inhibition by chlorogenic acid, caffeic acid, gallic acid, (+)-catechin, and (−)-epigallocatechin gallate (EGCG) on individual recombinant human Nt-MGAM and Nt-SI and on mouse Ct-MGAM and Ct-SI was assayed using maltose as the substrate. Inhibition constants, inhibition mechanisms, and IC50 values for each combination of phenolic compound and enzymatic subunit were determined. EGCG and chlorogenic acid were found to be more potent inhibitors for selectively inhibiting the two subunits with highest activity, Ct-MGAM and Ct-SI. All compounds displayed noncompetitive type inhibition. Inhibition of fast-digesting Ct-MGAM and Ct-SI by EGCG and chlorogenic acid could lead to a slow, but complete, digestion of starch for improved glycemic response of starchy foods with potential health benefit. KEYWORDS: α-glucosidases, inhibition, maltase-glucoamylase, phenolics, sucrase-isomaltase
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INTRODUCTION Starchy foods are a major component of the human diet and provide a large portion of energy intake. Starch is digested into glucose by six different enzyme activities: salivary and pancreatic α-amylase and the α-glucosidases maltase-glucoamylase (MGAM) and sucrase-isomaltase (SI), each composed of two active subunits located on the respective C and N terminals (Ct, Nt) of their original protein. The first step in starch digestion is performed by salivary and pancreatic αamylases, with production of linear glucose oligomers and branched α-limit dextrins, and very little free glucose.1 The αamylase degradation products are further hydrolyzed into free glucose by the mucosal α-1,4-exoglucosidases MGAM and SI, located on the small intestinal brush border membrane.2 MGAM and SI enzyme complexes belong to the GH31 family of glucohydrolases. The Nt subunit of both MGAM and SI attaches these enzyme complexes to the apical membrane of small intestinal enterocytes through an O-glycosylated stalk domain. 3 Although all four subunits have high α-1,4exoglucosidic activity,4,5 each MGAM and SI subunit has different α-glucosidic catalytic properties related to their independent active sites; therefore, their contribution to glucose production from glycemic carbohydrates is different.1,6 Ct-SI and Nt-SI subunits display distinctive sucrase and isomaltase activities, respectively. In MGAM, Ct and Nt subunits share activities against linear glucose oligomers, but the higher activity of Ct-MGAM on longer glucose oligomers © 2015 American Chemical Society
led to the naming of this subunit as glucoamylase, whereas NtMGAM has been ascribed as the maltase subunit.1 Among the SI and MGAM subunits, Ct-MGAM recently has been shown to be the most active, with the ability to digest whole, undigested starch molecules,7 and with the highest maltase activity compared to the other subunits.4,5 Although SI is the predominant molecule in the apical membrane of human small intestinal epithelial cells, MGAM compensates its relatively low abundance with its higher hydrolytic activity.8 A possible strategy to control the rate of free glucose release from the digestion of starch is to inhibit the hydrolytic activity of salivary and pancreatic α-amylases or, preferably, of the intestinal α-glucosidases where glucose is actually generated. Through selective inhibition of the faster digesting αglucosidase Ct subunits, while leaving the slower digesting Nt subunits active, one could expect to achieve a slower starch digestion effect. Such selective inhibition of intestinal αglucosidases may have multiple positive health implications related to control of the glycemic response profile of starchy foods and perhaps eliciting the ileal brake and gut−brain axis response to reduce appetite and food intake.9 We recently showed that diverse synthetic compounds and acarbose can Received: Revised: Accepted: Published: 3873
November 17, 2014 March 28, 2015 March 29, 2015 March 30, 2015 DOI: 10.1021/jf505425d J. Agric. Food Chem. 2015, 63, 3873−3879
Journal of Agricultural and Food Chemistry
Article
selectively inhibit the most active α-glucosidases, Ct-MGAM and Ct-SI, causing slower digestion of the α-amylase degradation products of starch.10 The inhibition of α-glucosidic activity of specific individual subunits of MGAM and SI can be considered as a key approach for controlling glucose release, because the α-glucosidase catalytic activities are responsible for producing virtually all of the free glucose available for intestinal absorption. A variety of chemical compounds have been shown to have an inhibitory effect on mammalian intestinal α-glucosidases. These compounds are derived either from chemical synthesis11,12 or from natural sources such as fruits13,14 or plants.15−17 Naturally occurring plant phenolic compounds are one group of chemical metabolites reported to have an inhibitory effect on the α-glucosidases. For instance, caffeic and chlorogenic acids are typical hydroxycinnamic acids found in high concentration in potatoes18 and coffee beans.19,20 Chlorogenic acids are esters of caffeic acids and quinic acids.21 They were identified as the main α-glucosidase inhibitors found in the leaf extract of Nerium indicum, causing reduced postprandial rise in blood glucose after ingestion of 2 g of maltose or sucrose/kg body weight in rats administered either the leaf extract or pure chlorogenic acid (25 mg/kg body weight).22 A single serving of coffee can have 70−350 mg of chlorogenic acid, and a regular coffee drinker can take up to 1 g of chlorogenic acids per day.23 Caffeic acid was shown to be one of the most potent rat intestinal α-glucosidase inhibitors among different cinnamic acid derivatives.24 The oxidized form of gallic acid caused nearly 40% inhibition of rat brush border sucrase and maltase activities.25,26 (−)-Epigallocatechin gallate (EGCG), the main catechin found in green tea,27 was also observed to be a potent inhibitor of maltase activity in rat brush border membrane vesicles,28 rat intestinal acetone powder,29 and recombinant human intestinal maltase.30 It has been also shown that tea catechins, especially EGCG, may have potential for treating type 2 diabetes.31,32 Subjects who consumed more than 6 cups of green tea daily were at less risk for type 2 diabetes compared to subjects who drank less than a cup per week.33 Overall, this information suggests that natural phenolic compounds present as normal dietary components may exert selective and differential inhibition of the individual subunits of MGAM and SI for the potential modulation of digestion of starchy and other glycemic carbohydrate-rich foods. Although there are multiple publications describing inhibition of αglucosidases by phenolic compounds, the possibility of subunit selectivity for modulating glucose release has not been studied. In the present study, we analyzed the inhibitory properties and potential for the selective inhibition of the individual Ct and Nt subunits of MGAM and SI using five phenolic and polyphenolic compounds [chlorogenic acid, caffeic acid, gallic acid, (+)-catechin, EGCG] commonly found in Western diets and for which α-glucosidase inhibition has been previously described.
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human Nt-MGAM (maltase subunit),34 and human recombinant NtSI35 (isomaltase subunit) were reported previously. Mouse Ct-MGAM and Ct-SI were generated by recombinant expression in a baculovirusSf9 insect cell system.4 Human Nt-MGAM and Nt-SI were expressed in Drosophila S2 cells.34,35 Nickel-Sepharose resin was used to isolate the secreted proteins from the cell media that were further purified using anion exchange chromatography. Determination of Protein Concentration. Protein concentration of solutions was determined with the Bio-Rad Protein Assay kit (Hercules, CA, USA), using 10 μL of the protein solution and 200 μL of Bradford dye reagent, and allowed to sit for at least 5 min. Absorbance was read at 595 nm using a Synergy HT microplate reader (BioTek, Winooski, VT, USA). Standards of bovine serum albumin were used in the concentration range of 31.25−500 μg/mL. Enzyme and Inhibition Assays. Glucose release was measured according to the tris glucose oxidase (TGO) method36 modified for microplate wells. Maltose solution (10 μL) at final concentrations ranging from 2.1 to 16.7 mM (approximately 1−8 times the Km for maltose of Ct subunits and 0.3−3 times the Km for maltose of Nt subunits) was mixed with 10 μL of the enzyme solution containing 0.2 mU of activity for Ct-MGAM, Ct-SI, and Nt-MGAM and 0.1 mU of activity for Nt-SI. One unit (U) of enzyme activity was defined as the activity that cleaves 1 μmol of maltose per minute. The mixtures were incubated for 1 h at 37 °C, and then TGO (180 μL) was added and incubated for an additional 45 min.36 Absorbance was read at 450 nm in the microplate reader. For inhibition assays, 10 μL of the phenolic inhibitor solutions was added to the above reaction mixtures to attain final concentrations ranging from 0 to 666.7 μM for the gallic acid, caffeic acid, and (+)-catechin, whereas chlorogenic acid and EGCG were used at final concentrations of 0−83.3 μM for C terminals of both MGAM and SI or 0−666.7 μM for N terminals of MGAM and SI. Analyses were conducted in triplicate. To correct for the scavenger effect of phenolics on the oxidative intermediates generated during the glucose oxidase− peroxidase reaction, which can lead to possible misleading readings of optical density (OD),37 curves of glucose concentration versus OD in the presence of different concentrations of each individual phenolic compound were constructed and used to adjust the OD obtained during the assay of inhibition of the phenolics on the α-glucosidase enzymes. At the selected concentrations, phenolics caused 7.4) caused a significant decrease in their concentration.48−51 Those studies used alkaline pH (pH >7.4); however, it may not reflect the actual pH of the lumen of the entire small intestine because the pH measured in humans subjects was 6.4−6.6 in the duodenum or proximal small intestine and increased to 7.3−7.5 in the distal small intestine.52,53 This difference could be important as the glycemic spike seen in the response profile arises from rapid proximal digestion of glycemic carbohydrates, and at this lower pH the catechins could be found with good qualities and high inhibition potential. Of note, oxidative reactions in the gut lumen may lead to the formation of complex dimers including theasinesins.54 The ability of these larger phenolic forms to interact with enzymes at the brush border is unknown. In conclusion, the finding of selective inhibition by plantderived phenolic compounds of the individual mucosal αglucosidases implies that the digestion rate of starch, starch products, and sucrose can be differentially affected and modulated by these dietary components. The potential to control glycemic response profiles or sucrose hydrolysis rate using this selective inhibition concept with phenolic compounds warrants further study with an in vivo model.
regulation of appetite, with potential impact on obesity and associated diseases.9,42,43 Our findings reveal that the four subunits of the intestinal αglucosidases, SI and MGAM, can be selectively and differentially inhibited by certain plant-derived phenolics. This introduces the potential to induce different rates or profiles of digestion for starches, starch products, and sucrose. For instance, selective inhibition of the most active starch degrading subunit, Ct-MGAM (or glucoamylase), was achieved with EGCG and chlorogenic acid. This implies that the reducing activity of this enzyme could slow the rate of starch digestion and reduce particularly the glycemic spike, as was proposed in a recent paper by our group.44 Chlorogenic acid had the highest binding affinity (Ki1) for Ct-SI (sucrase). This suggests the possibility of slowing the rate of digestion of sucrose-rich foods. Third, (+)-catechin showed higher inhibition for Nt-SI, the only subunit with endogenous α-1,6 branch hydrolyzing activity. The combination of (+)-catechin with a highly branched starch or starch products, such as a highly branched maltodextrin,45 could obtain a slow glucose release effect. The results imply that the low inhibitory effect of phenolics on the slower acting Nt-MGAM and SI subunits may allow for the slow digestion of starch in diets containing such phenolics, but avoiding the inhibition of all four subunits caused by stronger inhibitors such as acarbose, which, although effectively reducing glycemic carbohydrate digestion, causes the delivery of large quantities of carbohydrates into the colon. The tested phenolics were shown to affect the ability of the substrate to bind the active site of all enzyme subunits (Ki1); in some cases, phenolics may also bind an already formed enzyme−substrate complex, although this is with lesser affinity (Ki2). It has been reported that the catalytic pockets of CtMGAM, Nt-MGAM, and Nt-SI are surrounded by several aromatic amino acids, which may comprise the substrate binding motifs of these enzymes.4 Therefore, it may be speculated that phenolic compounds could interact with or bind to these aromatic motifs in proximity to the active site, impairing the binding of the substrate with a correct orientation. The substantially higher values for Ki1 of phenolics than those found for other competitive inhibitors10 make unlikely the possibility for the existence of a typical competitive binding component in the interaction and therefore discards the possibility of the existence of classic mixed-type inhibition. Thus, the model of typical noncompetitive inhibition was the one that most closely described the effects of phenolics. Therefore, phenolic and polyphenolic inhibitors bind to at least a second additional site. Mathematical fittings of the experimental data indicated that only 5 (Nt-SI/caffeic acid; Nt-SI/(+)-catechin; Ct-MGAM/chlorogenic acid; Nt-MGAM/ chlorogenic acid; and Ct-SI/EGCG) of the 20 different inhibitor-subunit combinations studied showed the same values for Ki1 and Ki2. In these cases, therefore, the binding affinity of phenolic compounds to the free enzyme and enzyme−substrate complex was essentially the same, implying that there was a single binding site for phenolics, and the binding of substrate did not interfere with the binding of phenolics at their binding site. This also implies the occurrence of conformational changes in the enzyme after binding of these phenolics, with an effect on their substrate binding capability or catalytic mechanism.38 Another study, using rat intestinal powder, showed that chlorogenic acid has a noncompetitive inhibition behavior on maltase and sucrose activities, which agreed with our results.22 However, the IC50 values of chlorogenic acid for maltase and
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ASSOCIATED CONTENT
* Supporting Information S
Reaction mechanisms for each of the different inhibition types and corresponding equations. This material is available free of charge via the Internet at http://pubs.acs.org. 3877
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AUTHOR INFORMATION
Corresponding Author
*(B.R.H.) Phone: (765) 494-5668. Fax: (765) 494-7953. Email:
[email protected]. Funding
This work was funded by CONACYT, Mexico, Projects 80448 and 173965. We thank the Whistler Center for Carbohydrate Research at Purdue University for its partial support of the project. Notes
The authors declare no competing financial interest.
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ABBREVIATIONS USED MGAM, maltase-glucoamylase; SI, sucrase-isomaltase; Ct, Cterminal end of proteins; Nt, N-terminal end of proteins; EGCG, (−)-epigallocatechin gallate; Vmax, maximal rate of reaction; Ki, inhibition constant; IC50, concentration required to inhibit 50% of the enzymatic activity; CI, confidence interval
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