Phylogenetic analysis reveals key residues in substrate hydrolysis in the isomaltase domain of sucrase-isomaltase and its role in starch digestion.


Journal

Biochimica et biophysica acta. General subjects
ISSN: 1872-8006
Titre abrégé: Biochim Biophys Acta Gen Subj
Pays: Netherlands
ID NLM: 101731726

Informations de publication

Date de publication:
09 2019
Historique:
received: 28 01 2019
revised: 19 06 2019
accepted: 24 06 2019
pubmed: 30 6 2019
medline: 9 4 2020
entrez: 30 6 2019
Statut: ppublish

Résumé

Starch constitutes one of the main sources of nutrition in the human diet and is broken down through a number of stages of digestion. Small intestinal breakdown of starch-derived substrates occurs through the mechanisms of small intestinal brush border enzymes, maltase-glucoamylase and sucrase-isomaltase. These enzymes each contain two functional enzymatic domains, and though they share sequence and structural similarities due to their evolutionary conservation, they demonstrate distinct substrate preferences and catalytic efficiency. The N-terminal isomaltase domain of sucrase-isomaltase has a unique ability to actively hydrolyze isomaltose substrates in contrast to the sucrase, maltase and glucoamylase enzymes. Through phylogenetic analysis, structural comparisons and mutagenesis, we were able to identify specific residues that play a role in the distinct substrate preference. Mutational analysis and comparison with wild-type activity provide evidence that this role is mediated in part by affecting interactions between the sucrase and isomaltase domains in the intact molecule. The sequence analysis revealed three residues proposed to play key roles in isomaltase specificity. Mutational analysis provided evidence that these residues in isomaltase can also affect activity in the partner sucrase domain, suggesting a close interaction between the domains. The sucrase and isomaltase domains are closely interacting in the mature protein. The activity of each is affected by the presence of the other. There has been little experimental evidence previously of the effects on activity of interactions between the sucrase-isomaltase enzyme domains. By extension, similar interactions might be expected in the other intestinal α-glucosidase, maltase-glucoamylase.

Sections du résumé

BACKGROUND
Starch constitutes one of the main sources of nutrition in the human diet and is broken down through a number of stages of digestion. Small intestinal breakdown of starch-derived substrates occurs through the mechanisms of small intestinal brush border enzymes, maltase-glucoamylase and sucrase-isomaltase. These enzymes each contain two functional enzymatic domains, and though they share sequence and structural similarities due to their evolutionary conservation, they demonstrate distinct substrate preferences and catalytic efficiency. The N-terminal isomaltase domain of sucrase-isomaltase has a unique ability to actively hydrolyze isomaltose substrates in contrast to the sucrase, maltase and glucoamylase enzymes.
METHODS
Through phylogenetic analysis, structural comparisons and mutagenesis, we were able to identify specific residues that play a role in the distinct substrate preference. Mutational analysis and comparison with wild-type activity provide evidence that this role is mediated in part by affecting interactions between the sucrase and isomaltase domains in the intact molecule.
RESULTS
The sequence analysis revealed three residues proposed to play key roles in isomaltase specificity. Mutational analysis provided evidence that these residues in isomaltase can also affect activity in the partner sucrase domain, suggesting a close interaction between the domains.
MAJOR CONCLUSIONS
The sucrase and isomaltase domains are closely interacting in the mature protein. The activity of each is affected by the presence of the other.
GENERAL SIGNIFICANCE
There has been little experimental evidence previously of the effects on activity of interactions between the sucrase-isomaltase enzyme domains. By extension, similar interactions might be expected in the other intestinal α-glucosidase, maltase-glucoamylase.

Identifiants

pubmed: 31254546
pii: S0304-4165(19)30160-6
doi: 10.1016/j.bbagen.2019.06.011
pii:
doi:

Substances chimiques

Starch 9005-25-8
Sucrase-Isomaltase Complex EC 3.2.1.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1410-1416

Informations de copyright

Copyright © 2019 Elsevier B.V. All rights reserved.

Auteurs

Marcia M Chaudet (MM)

Department of Biology, University of Waterloo, 200 University Avenue West, Waterloo, ON N2L 3G1, Canada.

Mahdi Amiri (M)

Department of Physiological Chemistry, University of Veterinary Medicine Hannover, D-30559 Hannover, Germany.

Nathalie Marth (N)

Department of Physiological Chemistry, University of Veterinary Medicine Hannover, D-30559 Hannover, Germany.

Hassan Y Naim (HY)

Department of Physiological Chemistry, University of Veterinary Medicine Hannover, D-30559 Hannover, Germany.

David R Rose (DR)

Department of Biology, University of Waterloo, 200 University Avenue West, Waterloo, ON N2L 3G1, Canada; Department of Physiological Chemistry, University of Veterinary Medicine Hannover, D-30559 Hannover, Germany. Electronic address: drrose@uwaterloo.ca.

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Classifications MeSH