Mammalian mucosal α-glucosidases coordinate with α-amylase in the initial starch hydrolysis stage to have a role in starch digestion beyond glucogenesis.

Sushil Dhital,Anbuhkani Muniandy,Michael J Gidley,Bruce R Hamaker,Amy Hui-Mei Lin,François Blachier

doi:10.1371/journal.pone.0062546

Sushil Dhital, Anbuhkani Muniandy + Show 4 more

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https://doi.org/10.1371/journal.pone.0062546

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Abstract

Starch digestion in the human body is typically viewed in a sequential manner beginning with α-amylase and followed by α-glucosidase to produce glucose. This report indicates that the two enzyme types can act synergistically to digest granular starch structure. The aim of this study was to investigate how the mucosal α-glucosidases act with α-amylase to digest granular starch. Two types of enzyme extracts, pancreatic and intestinal extracts, were applied. The pancreatic extract containing predominantly α-amylase, and intestinal extract containing a combination of α-amylase and mucosal α-glucosidase activities, were applied to three granular maize starches with different amylose contents in an in vitro system. Relative glucogenesis, released maltooligosaccharide amounts, and structural changes of degraded residues were examined. Pancreatic extract-treated starches showed a hydrolysis limit over the 12 h incubation period with residues having a higher gelatinization temperature than the native starch. α-Amylase combined with the mucosal α-glucosidases in the intestinal extract showed higher glucogenesis as expected, but also higher maltooligosaccharide amounts indicating an overall greater degree of granular starch breakdown. Starch residues after intestinal extract digestion showed more starch fragmentation, higher gelatinization temperature, higher crystallinity (without any change in polymorph), and an increase of intermediate-sized or small-sized fractions of starch molecules, but did not show preferential hydrolysis of either amylose or amylopectin. Direct digestion of granular starch by mammalian recombinant mucosal α-glucosidases was observed which shows that these enzymes may work either independently or together with α-amylase to digest starch. Thus, mucosal α-glucosidases can have a synergistic effect with α-amylase on granular starch digestion, consistent with a role in overall starch digestion beyond their primary glucogenesis function.

Highlights

Starch is the major dietary carbohydrate source of glucose for the human, and the rate and extent of starch digestion is associated with glycemia-related problems such as diabetes and other metabolic syndrome conditions
We reported that recombinant Nt-MGAM aglucosidase can digest even granular starch and the four individual a-glucosidases digest gelatinized starch molecules to glucose without the aid of a-amylase, albeit at a slow rate for granular starch [7,8,9,10]
With the objective to understand whether there is a synergistic effect of the two enzyme types on granular starch digestion, we examined a-glucogenesis, released maltooligosaccharide amounts, and starch structural changes including granular morphology, molecular weight distribution, and changes in supramolecular structure, as monitored by X-ray diffraction patterns and thermal properties

Summary

Introduction

Starch is the major dietary carbohydrate source of glucose for the human, and the rate and extent of starch digestion is associated with glycemia-related problems such as diabetes and other metabolic syndrome conditions. To generate dietary glucose from starchy foods, salivary and pancreatic a-amylase and four small intestine mucosal a-glucosidase subunits are employed in the human body. Nand C-terminal subunits of MGAM and SI complexes, hydrolyze a-1,4 glucosidic linkages from the non-reducing end of a-amylasedegraded starch molecules and produce free glucose [2,3,4]. Ct-MGAM, digested starch molecules in vitro to nearly 80% [8] This supports the hypothesis that human mucosal a-glucosidases may act together with a-amylase to digest starch, or at the very least provide an alternative pathway for starch digestion when luminal salivary and pancreatic a-amylase activity is inhibited or reduced because of immaturity and malnutrition [11,12]. We proposed that human a-amylase is not required for granular starch digestion, but amplifies its digestion by providing favored substrates for mucosal a-glucosidases [10]

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