Bound Substrate in the Structure of Cyanobacterial Branching Enzyme Supports a New Mechanistic Model

Hayashi, Makio; Suzuki, Ryuichiro; Colleoni, Christophe; Ball, Steven; Fujita, Naoko; Suzuki, Eiji

doi:10.1074/jbc.m116.755629

Cited by 45 publications

(38 citation statements)

References 46 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The transferase action of a BE may happen locally within the glucan molecule, as BEs probably bind the donor chain (from which the transferred segment derives) and the acceptor chain simultaneously-this would help prevent BEs from transferring the cut chain segment to water (i.e., simply hydrolyzing the glucan). Indeed, crystal structures of rice and cyanobacterial BEs suggest that glucans are not only bound to the active site, but also to additional starchbinding sites at the protein surface, although the actual intermediate with at least one covalently bound chain has not been captured (Chaen et al 2012;Hayashi et al 2017). Furthermore, the accessibility of potential cleavage and paste sites of BEs could be reduced by the formation of double helices and crystalline lamellae, i.e., both Ω C and Ω p would drop.…”

Section: Introduction Of Branches By Bes-increasing the Complexitymentioning

confidence: 99%

Theoretical and experimental approaches to understand the biosynthesis of starch granules in a physiological context

et al. 2020

View full text Add to dashboard Cite

Starch, a plant-derived insoluble carbohydrate composed of glucose polymers, is the principal carbohydrate in our diet and a valuable raw material for industry. The properties of starch depend on the arrangement of glucose units within the constituent polymers. However, key aspects of starch structure and the underlying biosynthetic processes are not well understood, limiting progress towards targeted improvement of our starch crops. In particular, the major component of starch, amylopectin, has a complex three-dimensional, branched architecture. This architecture stems from the combined actions of a multitude of enzymes, each having broad specificities that are difficult to capture experimentally. In this review, we reflect on experimental approaches and limitations to decipher the enzymes' specificities and explore possibilities for in silico simulations of these activities. We believe that the synergy between experimentation and simulation is needed for the correct interpretation of experimental data and holds the potential to greatly advance our understanding of the overall starch biosynthetic process. We furthermore propose that the formation of glucan secondary structures, concomitant with its synthesis, is a previously overlooked factor that directly affects amylopectin architecture through its impact on enzyme function. Keywords Starch • Amylopectin • Biosynthesis • Mathematical modeling Abbreviations ADP-glucose Adenosine diphosphate glucose BE Branching enzyme CLD Chain-length distribution DBE Debranching enzyme DP Degree of polymerisation HPAEC-PAD High-performance anion exchange chromatography coupled with pulsed amperometric detection ISA Homomeric isoamylase 1 enzyme or heteromeric isoamylase 1-isoamylase 2 enzyme SS Starch synthase Electronic supplementary material The online version of this article (

show abstract

Section: Introduction Of Branches By Bes-increasing the Complexitymentioning

confidence: 99%

Theoretical and experimental approaches to understand the biosynthesis of starch granules in a physiological context

et al. 2020

View full text Add to dashboard Cite

show abstract

“…Also, the minimal length of the donor glucan, the length of the transferred glucan, and the distance between two successive branch points differ from one BE to another (Hayashi et al 2015;Jo et al 2015;Palomo et al 2009;Roussel et al 2013;Sawada et al 2014;Takata et al 2003). Several experimental approaches including sitedirected mutagenesis (Hayashi et al 2017;Liu et al 2017), domain-swapping and truncation experiments (Jo et al 2015;Palomo et al 2009; Welkie, Lee, and Sherman 2015) and X-ray crystallography studies (Abad et al 2002;Feng et al 2015;Hayashi et al 2015;Na et al 2017;Pal et al 2010;Palomo et al 2011) have been used to understand the mechanism of branching activity. Very recently the Cyanothece sp.…”

Section: Branching Enzymesmentioning

confidence: 99%

“…Very recently the Cyanothece sp. ATCC 51142 BE1 structure with an oligosaccharide bound in the active site cleft has been solved providing a better understanding of the reaction catalyzed by these enzymes (Hayashi et al 2017). However, the relationship between the reaction specificity (e.g.…”

Section: Branching Enzymesmentioning

confidence: 99%

“…However, the relationship between the reaction specificity (e.g. preferred chain lengths transferred) and the BE protein structure remains unclear, and it is possible that variation exists in the mode of oligosaccharide binding depending on the BE species (Hayashi et al 2017). This information may allow a better control of the degree of branching and the average length of branches of the reaction product by the engineering of BE with altered specificity.…”

Section: Branching Enzymesmentioning

confidence: 99%

See 1 more Smart Citation

Synthesis of novel α-glucans with potential health benefits through controlled glucose release in the human gastrointestinal tract

Gangoiti

Corwin

Lamothe

et al. 2018

Critical Reviews in Food Science and Nutrition

View full text Add to dashboard Cite

The glycemic carbohydrates we consume are currently viewed in an unfavorable light in both the consumer and medical research worlds. In significant part, these carbohydrates, mainly starch and sucrose, are looked upon negatively due to their rapid and abrupt glucose delivery to the body which causes a high glycemic response. However, dietary carbohydrates which are digested and release glucose in a slow manner are recognized as providing health benefits. Slow digestion of glycemic carbohydrates can be caused by several factors, including food matrix effect which impedes a-amylase access to substrate, or partial inhibition by plant secondary metabolites such as phenolic compounds. Differences in digestion rate of these carbohydrates may also be due to their specific structures (e.g. variations in degree of branching and/or glycosidic linkages present). In recent years, much has been learned about the synthesis and digestion kinetics of novel a-glucans (i.e. small oligosaccharides or larger polysaccharides based on glucose units linked in different positions by a-bonds). It is the synthesis and digestion of such structures that is the subject of this review.

show abstract

“…X-ray crystallography has been used to determine the tertiary structures of prokaryotic and eukaryotic BEs. The authors have solved the structures of cyanobacterial BE in complex with maltooligosaccharides at the active site and proposed a mechanistic model of BE reactions (8). However, the structure-function relationships of BEs in eukaryotes remain unclear because only a limited number of structures have been solved: OsBEI from rice (9) and HsBE from human (10).…”

mentioning

confidence: 99%

Structure and Function of Branching Enzymes in Eukaryotes

Suzuki

2020

TIGG

Self Cite

View full text Add to dashboard Cite

Brancihing enzymes (BEs) catalyze the transglycosylation reactions to form a new branching point consisting of an α-1,6glucosidic linkage by cleaving an α-1,4-glucosidic linkage of an α-glucan chain. BEs are ubiquitous throughout the prokaryotes but are only found in limited taxa in the eukaryotes. Prokaryotic and eukaryotic BEs are classified into distinct families based on similarities in their primary structures. Land plants have multiple BE isoforms, whose function in vivo has been identified using mutants. Recent studies have revealed that plant BEs form protein-protein complexes with related enzymes involved in α-glucan metabolism in vivo. Although their biological significance is unclear, it is proposed that they are essential for efficient amylopectin biosynthesis. Crystal structures of BEs from eukaryotes (rice and human) are now available. These two structures have the same domain organization, containing a catalytic domain common to all members of glycoside hydrolase family 13. Recently, the authors have reported the structures of BE from a cyanobacterium (a photosynthetic prokaryote) in complex with maltooligosaccharides at the active site. On the other hand, little is known about the structure-function relationship of eukaryotic BEs. This review describes recent progress in research on the structure and function of eukaryotic BEs. A. Introduction Haworth et al. isolated an enzyme preparation from potato and discovered enzymatic activity that produced amylopectin-like branched glucan from amylose; this enzyme was named the Qenzyme (1), but the group of enzymes is now generally called the branching enzymes (BEs; EC 2.4.1.18). The transglycosylation reaction catalyzed by BE is accomplished by cleavage of an α-1,4glucosidic bond of the donor substrate and transfer of the glucan chain to the acceptor substrate to form a new branching point composed of an α-1,6-glucosidic linkage. It has been suggested that, in this reaction, both inter-and intramolecular transglycosylation is possible (Fig. 1) (2, 3). Starch and glycogen are α-glucans composed solely of glucose units, but they differ in terms of their structure and properties. Amylopectin, the main component of starch, has a repetitive structure (referred to as a tandem-cluster structure) consisting of regions with high (amorphous lamellae) and low branch frequency (crystalline lamellae) (Fig. 2, left panel). The structure makes the amylopectin to become insoluble, and thus amylopectin displays crystallinity, gelatinization, and paste viscosity. In contrast, randomly branched glycogen has high water solubility and does not display properties like amylopectin (Fig. 2, right panel). The branching structures of the glucans determine their properties (4, 5). BEs play key roles in α-glucan biosynthesis by determining the branching patterns of α-glucans (3, 5-7). BEs are distributed among prokaryotes and some eukary-MINIREVIEW

show abstract

Bound Substrate in the Structure of Cyanobacterial Branching Enzyme Supports a New Mechanistic Model

Cited by 45 publications

References 46 publications

Theoretical and experimental approaches to understand the biosynthesis of starch granules in a physiological context

Theoretical and experimental approaches to understand the biosynthesis of starch granules in a physiological context

Synthesis of novel α-glucans with potential health benefits through controlled glucose release in the human gastrointestinal tract

Structure and Function of Branching Enzymes in Eukaryotes

Contact Info

Product

Resources

About