Mammalian Mucosal a-Glucosidases Coordinate with a-Amylase in the Initial Starch Hydrolysis Stage to Have a Role in Starch Digestion beyond Glucogenesis

Starch digestion in the human body is typically viewed in a sequential manner beginning with a-amylase and followed by aglucosidase 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 a-glucosidases act with a-amylase to digest granular starch. Two types of enzyme extracts, pancreatic and intestinal extracts, were applied. The pancreatic extract containing predominantly a-amylase, and intestinal extract containing a combination of a-amylase and mucosal aglucosidase 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. a-Amylase combined with the mucosal a-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 a-glucosidases was observed which shows that these enzymes may work either independently or together with a-amylase to digest starch. Thus, mucosal aglucosidases can have a synergistic effect with a-amylase on granular starch digestion, consistent with a role in overall starch digestion beyond their primary glucogenesis function. Citation: Dhital S, Lin AH-M, Hamaker BR, Gidley MJ, Muniandy A (2013) Mammalian Mucosal a-Glucosidases Coordinate with a-Amylase in the Initial Starch Hydrolysis Stage to Have a Role in Starch Digestion beyond Glucogenesis. PLoS ONE 8(4): e62546. doi:10.1371/journal.pone.0062546 Editor: François Blachier, National Institute of Agronomic Research, France Received January 2, 2013; Accepted March 22, 2013; Published April 25, 2013 This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Funding: The Graduate School Research Travel Grant of the University of Queensland (Brisbane, Australia) funded SD to study at the Whistler Center for Carbohydrate Research at Purdue University (West Lafayette, Indiana, United States of America) for three months. This study was also supported internally by the Whistler Center for Carbohydrate Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected]