sucrose analogs- an attractive (bio)source for glycodiversiﬁcation

7/30/2019 Sucrose analogs- an attractive (bio)source for glycodiversification

1/17

ISSN 0265-0568

Natural Product Reports Current developments in natural products chemist

www.rsc.org/npr Volume 29 | Number 9 | September 2012 | Pages 93710

0265-0568(2012)29:9;1

COVER ARTICLE

Isabelle Andr et al.Sucrose analogs: an attractive (bio)source or glycodiversifcation


2/17

Sucrose analogs: an attractive (bio)source for glycodiversification

David Daude,abc Magali Remaud-Simeonabc and Isabelle Andre*abc

Received 27th April 2012

DOI: 10.1039/c2np20054f

Covering: up to April 2012

Sucrose is a widespread carbohydrate in nature and is involved in many biological processes. Its natural

abundance makes it a very appealing renewable raw material for the synthetic production of

high-valued molecules. To further diversify the structure and the inherent properties of these molecules,

the access to sucrose analogs is of utmost interest and has historically been widely explored through

chemical means. Nature also offers a large panel of sucrose-scaffold derivatives, includingphosphorylated or highly substituted phenylpropanoid esters amenable to transformation.

Additionally, the use of microorganisms or enzymes could provide an alternative ecologically-

compatible manner to diversify sucrose-scaffold derivatives to enable the synthesis of oligo- or

polysaccharides, glycoconjugates or polymers that could exhibit original properties for

biotechnological applications. This review covers the main biological routes to sucrose derivatives or

analogs that are prevalent in nature, that can be obtained via enzymatic processes and the potential

applications of such sucrose derivatives in sugar bioconversion, in particular through the engineering of

substrates, enzymes or microorganisms.

1 Introduction

2 Natural occurrence of sucrose derivatives

2.1 Phosphate derivatives2.2 Phenylpropanoid derivatives

2.3 Glycosyl derivatives

2.3.1 Glucosyl derivatives

2.3.2 Fructosyl derivatives

2.3.3 Galactosyl derivatives

3 In vitro synthesis of sucrose derivatives

3.1 Keto derivatives

3.2 Ester derivatives

3.3 Glycosylation of sucrose

3.4 Phosphate derivatives

3.5 Sucrose analogs

4 Sucrose isomers as alternative sucrose skeletons

4.1 Leucrose4.2 Turanose

4.3 Trehalulose

4.4 Maltulose

4.5 Isomaltulose

5 Potential applications of sucrose derivatives in sugar

bioconversion

6 Conclusions7 Acknowledgements

8 References

1 Introduction

Sucrose (a-D-glucopyranosyl-1,2-b-D-fructofuranoside) is a

widespread carbohydrate among plants. This non-reducing

disaccharide is formed by an a-D-glucopyranosyl unit and a b-D-

fructofuranosyl moiety covalently linked by their respective

anomeric carbons through a highly energetic bond (Scheme 1).

Sucrose is known to be the most available low molecular weight

carbohydrate.1 The Food and Agriculture Organization (FAO)

estimated its annual production at around 167.5 million tons for

20102011, mainly ensured by extraction from sugar cane and

Scheme 1 Chemical structure of sucrose (a-D-glucopyranosyl-1,2-b-D-

fructofuranoside).

aUniversite de Toulouse, INSA, UPS, INP, LISBP, 135 Avenue deRangueil, F-31077 Toulouse, FrancebCNRS, UMR5504, F-31400 Toulouse, FrancecINRA, UMR792 Ingenierie des Systemes Biologiques et des Procedes,F-31400 Toulouse, France. E-mail: [email protected]; Fax:+33 561 559 400; Tel: +33 561 559 969

This journal is The Royal Society of Chemistry 2012 Nat. Prod. Rep., 2012, 29, 945960 | 945

Dynamic Article LinksC


3/17

sugar beet, which contain 20% and 15% of sucrose by weight and

ensures 77% and 22% of sugar production, respectively. The

extremely efficient purification process leads to a remarkably

pure product for a moderate final cost. Although sucrose has

been mainly used so far for nutrition purposes, as a food additive

or in the chemical industry, its natural abundance makes it a very

interesting renewable raw material for synthesis reactions. In

particular, with the anticipated oil shortage, sucrose could be

seen as an alternative sustainable feedstock for the chemical

industry.2

In the search for carbohydrates displaying novel properties,

the access to a large structural diversity is of utmost interest.

Aside from the variety offered (and often hidden) by nature,

artificial glycodiversification can be generated via chemical and

biochemical transformations. However, carbohydrates are

chemically difficult to handle due to the presence of numerous

reactive hydroxyl groups. Regio- and stereo-selective modifica-tions thus require appropriate protection and deprotection steps

of functional groups. Independent of these problems, the use of

microorganisms or enzymes may be an alternative to diversify

the sucrose-scaffold and synthesize, in an eco-compatible

manner, sucrose derivatives that could display original properties

for biotechnological applications. In particular, sucrose is used

for the production of biodegradable polymers,3 synthetic inter-

mediates or novel carbohydrate derivatives as sweeteners and

prebiotic oligosaccharides for the food industry.4 Indeed, sucrose

proves to be an interesting and accessible starting material for a

variety of biochemical reactions. Among enzymes utilizing

sucrose as donor substrate, glucansucrases (EC 2.4.1.4, EC

2.4.1.5, and EC 2.4.1.140) from the Glycoside-Hydrolase (GH)families 70 and 13, fructansucrases (EC 2.4.1.9, EC 2.4.1.10 and

3.2.1.26) from the GH68 family and some fructosyltransferases

(e.g. EC 2.4.1.10, EC 2.4.1.99 or EC 2.4.1.100) from the GH32

family have emerged as attractive synthetic tools.58 Given their

broad acceptor substrate promiscuity, these enzymes have been

widely used for the stereo- and regioselective synthesis of original

gluco-conjugates, oligo- and polysaccharides.9

Magali Remaud-Simeon

Magali Remaud-Simeon

received her PhD from theUniversity of Toulouse in 1988.

Then, she was a Post-Doctoral

Fellow in the Chemical Engi-

neering department of the

University of Pennsylvania and

became an associate professor at

The University of Toulouse in

1990. Since 2001, she has been a

Full Professor at the National

Institute of Applied Science of

Toulouse. As the head of the

Catalysis and Enzyme Molec-

ular Engineering group since2002, she is involved in enzyme

optimization by protein engineering to provide useful tools for

white biotechnology and synthetic biology. With her collaborators,

she has elucidated the mechanism of action of several glucansu-

crases synthesizing dextran, alternan or amylose from sucrose

substrate. Her work is currently focused on the search for enzymes

acting on unnatural substrates.

Isabelle Andre

Isabelle Andre received a PhD in

Molecular Chemistry (1995)from the University Joseph

Fourier of Grenoble (France).

She held a post-doctoral position

(19961997) in the crystallog-

raphy department at the Insti-

tuto Rocasolano-CSIC in

Madrid, Spain. From 1997 to

2003, she occupied several posi-

tions in the Computational

Chemistry group of GLYCO-

Design Inc. (Toronto, Canada).

Upon her return to France, she

joined the CNRS in 2005 as aResearch Scientist and she was

promoted to Research Director in 2011. She is working at the

Laboratoire dIngenierie des Systemes Biologiques et des Procedes

in Toulouse (France) where she manages the computational

biology research activities of the Catalysis and Molecular Enzyme

Engineering group. Her research interests include understanding

and exploiting enzyme mechanisms and structuredynamics

activity relationships, developing molecular modelling methodolo-

gies to investigate molecular motions and assist protein design, and

rational engineering of novel enzymes for chemo-enzymatic

synthetic pathways and synthetic biology.

David Daude

David Daude received an engi-

neers degree in biochemistry

from the National Institute of

Applied Science of Toulouse

(France). He received his

diploma in 2009. He is currently

finishing his PhD under the

supervision of Prof. Magali

Remaud-Simeon and Dr Isabelle

Andre at the Laboratoire

dIngenierie des Systemes Biol-

ogiques et des Procedes in Tou-

louse. His work is focused on the

generation of protein libraries

using original semi-rational

strategies and their screening in

the quest of enzymes with novel specificities. His research interests

include the structurefunction aspects and the molecular evolution

of glycoside-hydrolases.

946 | Nat. Prod. Rep., 2012, 29, 945960 This journal is The Royal Society of Chemistry 2012


4/17

Nevertheless, the sole use of natural sucrose limits the variety of

accessible products to glucosyl and fructosyl derivatives; therefore

limiting the production of original molecules. Efficient modifica-

tions of sucrose are thus important in order to envision their use as

alternative substrates of sucrose-utilizing transglycosidases and

enable the production of a larger panel of glycoderivatives, such as

prebiotics, tailor-made glycoconjugates and oligosaccharides.

Combined with the use of enzyme engineering techniques, one can

expect major advances in the development of novel biosyntheticways to access carbohydrates.10

Althoughextensive work has been done over theyears to utilize

sucrose as a raw material for chemical and/or biochemical

conversion into high-value molecules (e.g. 5-(hydroxymethyl)

furfural, polyhydric alcohols) not structurally related to sucrose,

we have chosen not to discuss these aspects here as they have

already been reviewed in detail elsewhere.1 The intention of this

reviewwas ratherto describe themain biological routes to sucrose

derivatives or analogs (up to trisaccharides) reported in the liter-

ature and that can either be found in nature or obtained via

enzymatic processes. As they were out of the scope,total chemical

derivatizations of sucrose have been voluntarily discarded from

this survey or only mentioned to discuss advantages of biologicalroutes. For further details, refer to articles by Khan11 and Que-

neau.3 An outlook on the potential applications of sucrose

derivatives in carbohydrate bioconversion is also given.

2 Natural occurrence of sucrose derivatives

Sucrose is synthesized by photosynthetic organisms, such as

plants and cyanobacteria. Precursors and derivatives of the

molecule are naturally found in these organisms as well as in

sucrose-utilizing ones.


Two types of sucrose phosphate derivatives are naturally

produced i.e. sucrose-60-phosphate (S60P) and sucrose-6-phos-

phate (S6P). The biosynthesis of sucrose in plants, reviewed by

Lunn and MacRae,12 involves two distinct enzymes and a

phosphorylated precursor. A sucrose phosphate synthase (EC

2.4.1.14) catalyzes first the conversion of UDP-glucose and

fructose-6-phosphate into S60P, which is then hydrolyzed by a

sucrose phosphatase (EC 3.1.3.24) to form sucrose (Scheme 2).

S60P is a key intermediate of the sucrose biosynthetic pathway

and is found, for example, in plant leaves such as spinach,13 tea or

strawberry.14 The levels of S60P in strawberry leaves (Fragaria

vesca var. Royal Sovereign) and in tea leaves (Camellia sinensis

var. assemica) have been estimated at 0.36 and 0.05 mmol per100 g, respectively. A concentration of S60P of about 0.03 mM

has also been measured in the cytosol of spinach leaves. Chemical

synthesis of S60P has been described by Buchanan with an overall

yield of 6%,15 and further optimized by Kim up to 15%.16

Another phosphate derivative of sucrose, S6P, is commonly

found in sucrose-utilizing bacteria and results from phospho-

enolpyruvate-dependent phosphotransferase (PTS) sucrose

uptake.17 For instance, S6P is an intermediate of sucrose catab-

olism found in many Gram positive bacteria including B. subtilis,

cariogenic Streptococcus mutans or saccharolytic clostridia.18,19

As shown in Scheme 3, sucrose catabolism involves two steps.

The first one, involving the PTS system, allows sucrose trans-

portation into cells. The S6P formed is then hydrolyzed by the

specific sucrose-6-phosphate hydrolase into fructose and glucose-

6-phosphate (Scheme 3).20,21

2.2 Phenylpropanoid derivatives

The majority of naturally occurring sucrose phenylpropanoid

derivatives have not yet been experimentally synthesized in vitro

and only a few chemical syntheses have been reported.2224

Accessto most of these original molecules has been mainly achieved

from crude material to proceed to further use and characteriza-

tion. Phytochemical investigations have led to the isolation of

unusual phenolic glycosides. Among them, a variety of sucrose

derivatives have been characterized. These compounds listed in

Table 1 and captioned in Scheme 4 reveal a huge structural

diversity in terms of the nature and position of the substitutions.

Indeed, more than 70 phenolic sucrose esters have been identified

over the past 30 years. They have been extracted from various

plants, such as tobacco,25 bulbs of Lilium species,26,27 fruits of

Scheme 2 Sucrose-60-phosphate is a key precursor for sucrosebiosynthesis.

Scheme 3 Conversion of sucrose to sucrose-6-phosphate for internali-

zation into the cell.



5/17

Table 1 Naturally occurring phenylpropanoid esters of sucrose

R1 R2 R3 R4 R5 R6 R7 R8 References

(E)-Sin H H H H (E)-Sin H H 102H H H H p-(E)-cou p-(E)-cou H p-(E)-cou 103H H H H (E)-Sin (E)-Fer H H 30H H H H (E)-Sin (E)-Sin H HH H H H Ac (E)-Fer H HAc 3-methylvaleryl 3-methylvaleryl 3-methylvaleryl H H H H 104

H H H H H (E)-Fer H (E)-Fer 105Ac H H H H (E)-Fer H (E)-Fer(E)-Fer H H H H (E)-Fer H H 106(E)-Fer H H H H (E)-Fer Ac H(E)-Fer H H H H (E)-Fer H Ac(E)-Fer Ac H H H (E)-Fer H H(E)-Fer H H H H (E)-Fer Ac Ac(E)-Fer H Ac H H (E)-Fer H Ac(E)-Fer H Ac H H (E)-Fer Ac AcAc (S)-3-Methpenta (S)-3-Methpenta (S)-3-Methpenta H H H H 25(E)-Fer H H H H (E)-Fer H H 107(E)-Fer H H H H (E)-Fer Ac Hp-hydrobenz H H H H (E)-trimethocinna H H 31p-hydrobenz H H H H (E)-Sin H H(E)-Sin H H H H (E)-trimethocinna H HH H H H H (E)-Fer H H 26(E)-Fer Ac H H H (E)-Fer Ac H 27H p-(E)-cou H H H p-(E)-cou H HH p-(E)-cou H Ac H p-(E)-cou H HH p-(E)-cou Ac H H p-(E)-cou H Hp-(E)-cou H H H H p-(E)-cou H HAc Ac H Ac Ac p-(E)-cou H Ac 28Ac H Ac Ac Ac p-(E)-cou H AcAc H H Ac Ac p-(E)-cou H AcAc Ac H Ac H p-(E)-cou H AcAc H H Ac Ac p-(E)-cou H HH H H Ac Ac p-(E)-cou H AcAc H H Ac H p-(E)-cou H AcH Ac Ac H Ac p-(Z)-cou H AcH Ac H H Ac p-(Z)-cou H Ac(E)-Sin Ac H H H (E)-Sin H H 32(E)-Sin H Ac H H (E)-Sin H HAc Ac Ac Ac H (E)-Fer H (E)-Fer 108

Ac H H Ac Ac (E)-Fer H (E)-Fer 33Ac Ac H Ac Ac H H (E)-Ferdh-Fer H H H H H H H 34H H H H H (E)-trimethocinna H H 109Benzoyl H H H H (E)-trimethocinna H Hp-(E)-cou H H H H (E)-Sin H Hp-(E)-cou H H H H (E)-trimethocinna H H(E)-Sin H H H H (E)-Sin H H(E)-Sin H H H H (E)-trimethocinna H H(E)-trimethocinna H H H H (E)-trimethocinna H H(E)-Sin H H H H H H H 110(E)-trimethocinna H H H H H H Hp-hydrobenz H H H H H H HH (E)-Sin H H H (E)-Sin H H(E)-Fer H H H H H H H(E)-Sin H H H H H H HAc Ac H Ac (E)-Fer (E)-Fer H (E)-Fer 111

Ac H H Ac (E)-Fer (E)-Fer H (E)-FerAc Ac H Ac H (E)-Fer H (E)-FerAc Ac H Ac p-(E)-cou (E)-Fer H (E)-FerAc H H Ac p-(E)-cou (E)-Fer H (E)-Fer(E)-Fer H H H p-(E)-cou p-(E)-cou H p-(E)-cou 35(E)-Fer H H H (E)-Fer p-(E)-cou H p-(E)-couH H H H H H H p-(E)-cou 112p-(E)-cou H H H H H H p-(E)-coup-(E)-cou H H H H (E)-Fer H H 113(E)-Caf H H H H (E)-Fer H HH H H H H p-(E)-cou H (E)-Fer 114H H H H p-(E)-cou p-(E)-cou H (E)-Fer 115H H H Ac p-(E)-cou p-(E)-cou H (E)-FerAc H H H p-(E)-cou p-(E)-cou H (E)-Fer



6/17

Prunus sp.28 or plenty of medicinal plants, including Bistorta

manshuriensis,29 Polygala species,3032 Sparganium stoloniferum,33

or Vaccaria segetalis.34 These molecules are usually bioactive,

acting as plant growth inhibitors, insecticides, bactericides or

flavour precursors in the plant. Some of them have also shown

therapeutic properties. Two phenylpropanoid esters of sucrose,

namely vanicoside B and lapathoside A from Polygonum lapa-

thifolium, which exhibit anti-tumor-promoting effects and inhibit

Epstein-Barr virus early antigen induction, have been identified

as cancer chemo-preventive agents.35 Some phenylpropanoyl

sucrose compounds from Polygala tenuifolia also revealed their

efficiency in the prevention of memory disorders.36,37 Consid-

ering the potential applications of these glycoside derivatives and

their low natural abundance (less than 5% in plants),38 the

identification of genes39 involved in their biosynthesis could

enable the development of efficient microbial production

processes via metabolic engineering.40

2.3 Glycosyl derivatives

A variety of monoglycosylated derivatives of sucrose can be

found in nature. These trisaccharides differ in the nature of the

glycosyl unit linked to sucrose as well as in the specificity of the

glycosidic linkage between this unit and the sucrose moiety

(Fig. 1).

2.3.1 Glucosyl derivatives. Erlose (a-D-glucopyranosyl-(14)-

a-D-glucopyranosyl-(12)-b-D-fructofuranoside) is a trisaccha-

ride occurring in honeys and royal jelly.4145 The erlose content of

469 samples of honey was analyzed by Devillers and coworkers,

revealing an average proportion of 0.33% with values going up to

1.55% (e.g. for acacia honey). It crystallizes in two hydratedforms whose structures have been determined.46,47 Erlose is a

sucrose-like tasty carbohydrate but it is non-cariogenic.48,49

Along with erlose, melezitose (a-D-glucopyranosyl-(13)-b-D-

fructofuranosyl-(21)-a-D-glucopyranoside) is commonly found

in honey as well as in honeydews and saps of many trees and

plants (e.g. meleze). Melezitose is the main component of aphid

honeydew (59%).50 A correlation between the amount of

honeydew produced by aphids and the intensity of ant-atten-

dance has been underlined. Thus, ants are attracted by melezi-

tose-rich honeydew secreted by aphids and protect them against

natural predators creating a cooperative mutualism.5153

Scheme 4 Naturally occurring phenylpropanoid esters of sucrose.

Fig. 1 Naturally occurring mono-glycosylated sucrose compounds.

Table 1 (Contd. )

R1 R2 R3 R4 R5 R6 R7 R8 References

H H H H (E)-Fer p-(E)-cou H (E)-FerH H H Ac p-(E)-cou (E)-Fer H (E)-FerH H H H (E)-Fer (E)-Fer H (E)-FerH Ac H p-(E)-cou Ac p-(E)-cou H p-(E)-cou 116H H H H H (Z)-Fer H (Z)-Fer 29Ac H H H H (Z)-Fer H (Z)-Fer

p-(E)-cou H H H H p-(E)-cou p-(E)-cou H 117(E)-Caf H H H H p-(E)-cou p-(E)-cou H



7/17

Melezitose has been crystallized in two monohydrated forms.5456

Gentianose (b-D-glucopyranosyl-(16)-a-D-glucopyranosyl-

(12)-b-D-fructofuranoside) is another glucosyl derivative of

sucrose trisaccharide that was first extracted from Gentiana

lutea57 and is commonly found in gentian roots, hence its name.

2.3.2 Fructosyl derivatives. Three fructosyl derivatives are

commonly found in nature, namely 1-kestose, 6-kestose and

neokestose. 1-kestose was first observed and isolated during theaction of yeast invertase on concentrated sucrose solutions.58 It

has been identified in honey, as well as in many plants. 5962 In

higher plants the synthesis of 1-kestose results from the enzy-

matic transfer of the fructosyl moiety of sucrose onto another

molecule of sucrose and is catalyzed by a sucrose:sucrose fruc-

tosyltransferase (1-SST EC 2.4.1.99).6265 In fructooligo-

saccharide-producing plants, the fructan synthesis starts with the

synthesis of 1-kestose. NMR studies have shown that both

neokestose and 1-kestose were present in plant extracts, such as

Asparagus, Festuca or Dactylis.66,67 Anion-exchange chroma-

tography with pulsed amperometric detection (HPAEC-PAD)

also allowed the detection of neokestose and 1-kestose in table

grapes.68 Neokestose and 1-kestose were also found in Agave veracruz.69 The less abundant 6-kestose has been isolated from the

seeds of the horse chestnut (Aesculus hippocastanum L.).70

2.3.3 Galactosyl derivatives. Raffinose (a-D-galactopyr-

anosyl-(16)-a-D-glucopyranosyl-(12)-b-D-fructofuranoside) is

another sucrose-scaffold based molecule that is encountered in

many plants though in small amounts. This water-soluble

trisaccharide can be found in cottonseed meal,71 jute plant,72

sugar beets,73,74 sunflower, Gramineae species,75 lupins,76

soybean,77 and many edible leguminous crops.78 Although

abundant in human nutrition, this oligosaccharide is non-

digestible but is fermented by intestinal bifidobacteria, thus

acting as a prebiotic molecule by stimulating the beneficial gutmicrobiota.79,80 Notably, raffinose is used as a functional food

ingredient in Japan.81 Raffinose also shows cryo-preserving

effects,82 and ameliorates atopic dermatitis in human subjects.83

Two enzymes are involved in the biosynthesis of raffinose in

plants, namely galactinol synthase, which catalyzes the biocon-

version of UDP-galactose into galactinol and raffinose synthase,

which catalyzes the synthesis of raffinose from galactinol and

sucrose.84 For Arabidopsis and the common bugle Ajuga reptans

L., these enzymes are located in the cytosol where raffinose

appears to be first synthesized before being translocated across

the envelope of the chloroplast by a specific transporter.85 The

presence of raffinose has also been detected in algal cells of

Chlorella vulgaris where a chilling shock stops the cell growth andleads to raffinose accumulation.86 On the industrial scale, raffi-

nose is extracted from molasses,87 in particular sugar beet

molasses. Raffinose usually represents 0.52% of beet molasses.

Upon desugaration, the blackstrap molasses contain up to 15%

raffinose,88 from which the molecule can be efficiently extracted

and crystallized.89,90

The a-galactosyl derivative loliose (a-D-galactopyranosyl-(1

3)-a-D-glucopyranosyl-(12)-b-D-fructofuranoside) has been

detected in Lolium sp. as well as in Festuca species.9193 Its

biosynthesis is ensured by a UDP-Gal:sucrose 3-galactosyl-

transferase.94

Another trisaccharide, namely planteose, was first extracted

from the seeds of Plantago sp.95 where it acts as a reserve

carbohydrate.96 It was first prepared from Plantaginaceae,97

tobacco or mint seeds,98 and has been identified as the major

carbohydrate in seeds of Fraxinus excelsior.99 Its structure

was determined ten years later as being the a-D-galactopyr-

anosyl-(16)-b-D-fructofuranosyl-(21)-a-D-glucopyranoside. It

has recently been reported in honey samples.60,100 Chemical

synthesis of planteose involving a low yield multistep mechanismhas been proposed.101

3 In vitro synthesis of sucrose derivatives

Due to a limited variety of sucrose derivatives available in nature

and their low level of natural abundance, the extraction of

natural compounds remains a tedious task. In vitro synthesis

using either microorganisms or enzymes appears thus to be a

solution of choice to access sucrose-like carbohydrates in mild

conditions with selective introduction of a variety of functional

groups at distinct reactive positions of sucrose-scaffold. An

overview of these modifications is proposed in Scheme 5.

3.1 Keto derivatives

Chemical synthesis of carbonyl-sucrose derivatives was first

demonstrated by Andersson using bromine oxidation of sucrose

in aqueous solution, a mixture of four keto-derivatives was

obtained.118 However, the process presented several drawbacks

as 10% of starting material and acidic compounds remained in

the final mixture. Furthermore, the keto-sugars showed a low

stability that required their subsequent conversion into more

stable O-methyloximes to proceed to their biochemical and

structural characterization. The specific etherification of sucrose

into 2-O-benzyl-sucrose has also been performed to produce a

precursor for the synthesis of 2-ketosucrose,119 albeit thissynthesis involved a low-yield multi-step process. To avoid such

problems, efficient enzymatic syntheses of carbonyl-derivatives

of sucrose have been proposed. Different categories of enzymes

have been used for either C-2 oxidation or C-3 dehydrogenation

of the sucrose glucosyl moiety (Scheme 6). The D-glucoside 3-

dehydrogenase (G3DH EC 1.1.99.13) from Agrobacterium

tumefaciens has been widely studied during the past decades for

its capacity to regioselectively produce the 3-ketosucrose (b-D-

fructofuranosyl a-D-ribo-hexopyranosid-3-ulose).120122 The

activity of this enzyme has been shown to be dependent on the

manganese concentration in the reaction medium, which can be

optimized to increase conversion yield.123 The enzyme activity is

also FAD-dependent, thus using whole cells of Agrobacteriumtumefaciens offers the possibility ofin vivo cofactor regeneration

but raises the problem of separating 3-ketosucrose from other

compounds present in culture medium. During 3-ketosucrose

purification, Hough et al. also obtained a clarified concentrate

containing a significant amount of 2-ketosucrose (b-D-fructo-

furanosyl-a-D-arabino-hexopyranosid-2-ulose) probably result-

ing from enolisation of 3-ketosucrose.124 An alternative synthetic

route to 3-ketosucrose consists of using a pyranose dehydroge-

nase (PDH) from Agaricus sp.125,126 Notably, PDH from Agar-

icus meleagris efficiently catalyzes dehydrogenation of a wide

range of carbohydrates (yields $ 90%), including sucrose.127,128



8/17

Nevertheless, the reaction necessitates an electron acceptor, such

as 1,4-benzoquinone, that has to be removed after reaction.127

The in vitro bioconversion of sucrose in 2-ketosucrose has

recently been described.129 A commercial pyranose-2-oxidase

(POase EC 1.1.3.10) has been used for the reaction catalysis in

water with oxygen aeration. This oxidation and the associated

reduction of O2 into H2O2were coupled to the action of a catalase

(EC 1.11.1.6.) used to degrade the neo-formed hydrogen

peroxide and prevent enzyme inhibition. A full conversion ofsucrose was observed within 24 h. The enzymes were removed by

ultrafiltration and the filtrate was dried into vacuum to obtain a

pure fraction of 2-ketosucrose. Of interest, sucrose keto-deriva-

tives can also be used as a starting material for other chemical

transformations including amination, silylation,130 cyanohydri-

nation,131 or epimerisation.123

3.2 Ester derivatives

Fatty acid monoesters of sucrose (reviewed by Polat and Lin-

hardt, 2001)132 have drawn considerable attention for their

pharmaceutical interest or potential applications as surfactants

or emulsifiers. The regioselective esterification of sucrose can be

achieved through chemical means. Industrial routes using basic

catalysts have been developed. They involve solvent or solvent-

free reactions yielding sucrose ester mixtures containing

predominantly monoesters (up to 70%). Among the eight

potential reactive hydroxyl groups, the primary hydroxyls at

carbons 6 and 60 exhibit the highest reactivity. Nonetheless, the

synthesis of selectively acylated sucrose in its pure form remainsdifficult. The synthesis of acylated sucrose at position 6 0 with a

yield of isolated product up to 43% has been described in DMF

in the presence of 1,4-diazobicyclo[2.2.2]octane (DABCO).

Prerequisite modifications of sucrose using dibutyltin oxide have

also been reported for the synthesis 6-O-acylsucroses and 6,30-di-

O-acylsucroses in DMF with good yields.133,134 The synthesis of

2-O-acylsucroses in anhydrous pyridine has also been achieved in

4564% yield.135,136

Numerous studies have shown that enzymatic catalysts can be

used as powerful tools for the selective acylation of sucrose.

Indeed, a wide variety of enzymes are able to convert sucrose into

Scheme 5 The in vitro synthesis of sucrose derivatives.



9/17

mono or di-esters mainly, depending on the acyl donor, the

reaction conditions and the catalyst used (Table 2). Among them,

lipases are commonly used to produce a large panel of sucrose

esters using a variety of acyl donors of different chain length in

distinct solvents. In particular, lipases from Candida antarc-

tica,137 Thermomyces lanuginosus,138 Mucor miehei,139 Byssochl-

amys fulva,140 Pseudomonas sp.,141 Penicillium chrysogenum,142

Aspergillus oryzae,143 Aspergillus terreus,144 or Rhizopus sp.143

have been shown to be highly efficient to acylate sucrose at

positions 6 and 60. Proteases from Bacillus subtilis and the met-

alloprotease thermolysin from Bacillus thermoproteolyticus also

lead to the production of sucrose esters modified at positions 10

and 2, respectively.145,146 A protease from Bacillus licheniformis

can also be used to generate sucrose acrylate esters,147 sucrose-

containing aromatic polymers,148 and sucrose amino acid

esters.149

Original chemo-enzymatic processes for sucrose acylation

have also been proposed by either coupling the use of lipases and

chemically-produced sucrose acetals,150 or by glucosylating a

glucose-6-acetate with a fructosyltransferase from Bacillus sub-

tilis.151 The preparation of the sweetener sucralose also involvesan ester derivative of sucrose, namely sucrose-6-acetate, which is

chlorinated and deacetylated to give the final product.152

Another way of retrieving a partially acetylated sucrose consists

of de-acetylating the easily chemically synthesized sucrose octa-

acetate using proteases and lipases in organic solvent.153,154 In

any case, one major difficulty in obtaining acylated molecules in

a pure form is related to the low solubility of sucrose in most

organic environments, thus requiring the use of non-environ-

mental friendly solvents in which the disaccharide is more soluble

(e.g. pyridine, dimethylsulfoxide (DMSO), dimethylformamide

(DMF), hexane).

3.3 Glycosylation of sucrose

Sucrose can be used as a glycosyl donor or acceptor for the

enzymatic synthesis of short oligosaccharides, such as functional

galacto-derivatives or short chain fructooligosaccharides (FOS)

acting and classified as prebiotics.155157 We will limit our review

to both naturally-occurring and tailor-made trisaccharides

synthesized in vitro using transglycosidases. We did not consideroligosaccharide production resulting from additional elongation.

Galactosyl transfer onto disaccharides has been proposed

using both activated and non-activated carbohydrates. Besides

its extraction from plants, raffinose can also be efficiently

obtained by in vitro synthesis using the galactinol-sucrose gal-

actosyltransferase from Vicia faba and sucrose and galactinol (a-

D-galactopyranosyl-(13)-1D-myo-inositol) or p-nitrophenyl- a-

D-galactopyranoside as substrates.84 Reverse hydrolysis activity

of the a-galactosidase from Absidia corymbifera, which acts on

sucrose and galactose was also investigated to produce raffinose

with an overall conversion ratio improved up to 10% (w/v)

(Scheme 7).158 b-galactosidase from Bacillus circulans has been

used for the synthesis of lactosucrose (b-D-galactopyranosyl-(14)-a-D-glucopyranosyl-(12)-b-D-fructofuranoside) as well as its

b(13) isomer.159 Biosynthesis of planteose has also been

proposed with the cell-free extract of sesame seeds (Sesasum

indicum) involving either UDP-galactose or galactinol as donors

and sucrose as the acceptor.160 Synthesis of planteose has also

been described with an a-galactosidase from Plantago ovato

using galactose.161

The biosynthesis of umbelliferose has also been demonstrated

in an enzyme preparation from leaves ofAegopodium podagraria

L. using sucrose as the acceptor and UDP-galactose as the

donor.162 An original trisaccharide derived from sucrose has been

Scheme 6 The biosynthesis of carbonyl-derivatives of sucrose.



10/17

synthesized by transglycosylation using a recombinant b-glyco-

sidase from Sulfolobus shibatae. This reaction involved lactose as

the donor and sucrose as the acceptor to form a new product

whose structure was determined to be the b-D-galactopyranosyl

(16)-a-D-glucopyranosyl-(12)-b-D-fructofuranoside. The yield

was calculated as 20% from the acceptor sucrose.

The biosyntheses of melezitose and erlose have also been

performed by incubating, in an artificial phloem sap, isolated

Table 2 Esters derivatives of sucrose and their synthesis conditions

Enzymes Species Acylating agents Solvents Main ProductsYield(%) References

Lipase Candida antarctica Ethyl butanoate tert-butanol 6 and 60-O-butanoylsucrose

1 137

Ethyl laurate tert-butanol 6,60-di-O-lauroylsucrose 35Vinyl laurate tert-butanol:DMSO

(80 : 20)6,60-di-O-lauroylsucrose 170

Thermomyceslanuginosus

Vinyl laurate tert-butanol:DMSO(80 : 20)

6-O-lauroylsucrose 98 170

Vinyl laurate tert-butanol:DMSO(80 : 20)

6-O-lauroylsucrose 70 138

Vinyl palmitate tert-butanol:DMSO(80 : 20)

6-O-palmitoylsucrose 80 138

Mucor miehei Capric acid solvent free 6-O-capryloylsucrose


11/17

guts of Metropeurum fuscoviride and Macrosiphoniella tanace-

taria, respectively.163

The in vitro fructosylation of various disaccharides involving a

fructosyltransferase or a fructofuranosidase has been

described.164 The enzymatic synthesis of lactosucrose has been

performed using levansucrases as catalysts, and sucrose and

lactose as the fructofuranosyl donor and acceptor, respectively.

With the levansucrase from Aerobacter levanicum, a yield of

32.9% (w/w) was obtained.165 The fructofuranosyl moiety ofsucrose is cleaved and transferred onto the glucopyranosyl

moiety of lactose via the reformation of the sucrose characteristic

a(12)b linkage. Lactosucrose bioconversion from lactose and

sucrose using whole cells ofPaenibacillus polymyxa has also been

reported.166 More recently, the efficiency of lactosucrose

conversion has been raised to 43.2% using a mixed-enzyme

system containing a levansucrase from Zymomonas mobilis and a

glucose oxidase for increasing conversion by removing

glucose.167 The levansucrase ofPseudomonas aurantiaca has also

been used for this purpose.168 The use of b-fructofuranosidase

from Arthrobacter sp. K-1 also enabled the synthesis of lacto-

sucrose from sucrose and lactose with an overall yield close to

27% (Scheme 8).169 The conversion has been improved up to 50%in a batch process with an equimolar ratio of substrates. Kang

and coworkers have reported the synthesis of erlose from sucrose

as a donor and maltose as an acceptor using levansucrase from

Leuconostoc mesenteroides B-512 FMC (25% reaction

product).174 A similar synthesis involving the levansucrase from

Bacillus subtilis has also been described with an optimized yield

of 45% (calculated from the donor sucrose).175

The production of 1-kestose using the intact mycelium of

Aspergillus phoenicis containing a sucrose fructosyltransferase

has been described from a 750 g L1 sucrose solution with a yield

of 300 g L1 of 1-kestose in 8 h.176 A continuous production

involving an immobilized b-fructofuranosidase from Aureobasi-

dium has also been proposed with a 1-kestose concentration of 90g L1 for up to 168 h, allowing a synthesis of 287 g during this

time.177 1-kestose production has also been performed using a

fructosyltransferase from Aspergillus foetidus expressed in an

invertase-deficient mutant of Saccharomyces cerevisiae.178

Levansucrase from Lactobacillus sanfranciscencis also mainly

synthesizes 1-kestose.179 Recently, a combination of both genetic

and substrate engineering has been used for the preparative

synthesis of fructooligosaccharides, notably 1-kestose.180

The conversion of sucrose into FOS using whole Penicillium

citrinum led to the conversion of sucrose into both 1-kestose and

neokestose. Kritzinger and coworkers have optimized the

production parameters of the trisaccharide neokestose by Xan-

thophyllomyces dendrorhous (Phaffia rhodozyma) to reach a

production yield of 0.85 g of neokestose per g of sucrose and aproportion of 95% neokestose of the total oligosaccharides.181,182

The production of the other fructooligosaccharide 6-kestose

has also been demonstrated using, for example, the b-fructo-

furanosidase from Thermoascus aurantiacus or Schwanniomyces

occidentalis.183,184 The b-fructofuranosidases from Saccharo-

myces cerevisae and Rhodotorula dairenensis are also known for

producing mainly 6-kestose.185,186


Sucrose-6-phosphate (S6P) was obtained using permeabilized

cells of different strains. Martin et al. have first identified a

phosphoenolpyruvate-dependent phosphotransferase system inStreptococcus mutans.187 Two enzymes are involved in the

catabolism of sucrose by S. mutans, a sucrose phosphotransfer-

ase (PTS) and a sucrose-6-phosphate hydrolase. Permeabilized

cells of a mutant strain constitutive for the PTS system and

missing hydrolytic activity have been isolated and used for the

biosynthesis of sucrose-6-phosphate.188 More recently, Thomp-

son et al. showed that phosphorylation of sucrose as well as that

of its five linkage isomers was possible using permeabilized cells

ofKlebsellia pneumoniae at low pH (Scheme 9).189 Previous work

by Kunst et al. showed that sucrose-6-phosphate can be

synthesized from glucose-6-phosphate (G6P) and sucrose using a

levansucrase, which under the operating conditions led to the

conversion of 45% of the G6P into S6P.190

3.5 Sucrose analogs

The sucrose derivatives described previously conserve the

sucrose-scaffold, which constitutes a fructofuranosyl unit linked

Scheme 8 The biosynthesis of lactosucrose using the b-fructofuranosidase from Arthrobacter sp.



12/17

to a glucopyranosyl unit via an a(12)b glycosidic bond.

However, another way to modify sucrose is to replace the glu-

cosyl unit by alternative glycosyl moieties. Following this idea,

sucrose-like disaccharides which conserve the characteristic a(1

2)b glycosidic bond have been produced by fructosylation of

various monosaccharides using fructosyltransferases (e.g.

levansucrase) (Scheme 10). The synthesis of four sucrose analogs

by fructosylation of D-glycopyranosides, such as D-galactose, D-

mannose, D-xylose and D-fucose, was first described using a

levansucrase from Bacillus subtilis with yields of 54, 4, 62 and

21%, respectively.191 Further biocatalytic investigations enabled,

fructosylation from sucrose as a fructosyl donor to othercarbohydrates, including monosaccharides (e.g. 2-deoxy-D-

glucose, D-allose, 3-ketoglucose) and disaccharides (e.g. iso-

maltose, maltose, melibiose, cellobiose or lactose) with yields

going from 0.01% for D-allose to 53% for isomaltose. Using

raffinose as fructosyl donor, the fructosylation ofL-sugars (e.g. L-

glucose, L-rhamnose, L-galactose, L-fucose and L-xylose) was also

successfully achieved with yields going from 0.1% for L-rham-

nose up to 27% for L-xylose.175 Interestingly, some of these

sucrose analogs a-D-xylopyranosyl-b-D-fructofuranoside (Xyl-

Fru), a-D-mannopyranosyl-b-D-fructofuranoside (Man-Fru) and

a-D-galactopyranosyl-b-D-fructofuranoside (Gal-Fru) were

further tested as acceptor substrates by the highly active

recombinant b-fructofuranosidase from Aspergillus niger,

leading to fructosylated products, such as 1-kestose and 1-nys-

tose analogs. Of note, two analogs were previously described by

Avigad et al. using a levansucrase from Aerobacter levani-

cum.192,193 In this report, Xyl-Fru and Gal-Fru were synthesizedfrom 10 g of raffinose as the fructosyl donor and xylose or

galactose, respectively, as the fructosyl acceptors to produce pure

Xyl-Fru (400 mg) and Gal-Fru (70 mg).

4 Sucrose isomers as alternative sucrose skeletons

Some properties of sucrose isomers, such as sweetness, solubility,

or cariogenic effect, differ significantly from those of sucrose,

thus offering novel opportunities for the development of prebi-

otics or edulcorants. Five sucrose isomers are naturally accessible

and can be produced either in vitro using carbohydrate-active

enzymes (CAZy)194 or in vivo using selected microorganisms. Of

note, the fructosyl moiety in sucrose isomers has been found inmany different forms (e.g. acyclic, cyclic, furanose, pyranose).

Hereafter are described the biochemical syntheses of leucrose,

turanose, trehalulose, maltulose and isomaltulose (palatinose).

4.1 Leucrose

a-D-glucopyranosyl-1,5-b-D-fructose, commonly named leu-

crose, is a reducing disaccharide derived from sucrose. Although

half as sweet as sucrose, leucrose is fully digestible and non-

cariogenic. It was firstly isolated from dextran-producing

cultures of Leuconostoc mesenteroides and Streptococcus

bovis.195,196 Different experimental conditions have been tested,

allowing high product yield and the proposition of a kinetic

model.197 Production of leucrose from sucrose using immobilized

dextransucrase entrapped in calcium alginate beads has been

carried out, showing its best results in a tubular reactor.198,199

More recently, immobilization of the dextransucrase from

Leuconostoc mesenteroides NRRL B-512F using a convenient

affinity interaction with resin showed promising results by

increasing conversion rate up to 74% after one day.200

4.2 Turanose

a-D-glucopyranosyl-1,3-b-D-fructose or turanose was first

discovered by Alekhine in 1889. It resulted from the hydrolysis of

melezitose, a trisaccharide extracted from Turkestan Manna,

giving an equimolar mixture of glucose and turanose.201 Likeleucrose, it is non-cariogenic and half as sweet as sucrose. Tur-

anose has also been identified as a by-product of the polymeri-

zation reaction catalyzed by amylosucrases.202204 The synthesis

of turanose from sucrose using Neisseria polysaccharea amylo-

sucrase has been improved by increasing the substrate concen-

tration up to 2.5 M. The production of turanose was thus

favoured and allowed a maximal production yield of 56.2% after

a 120 h at 35 C. Turanose was further purified using preparative

HPLC.205 The amylosucrase from Deinococcus geothermalis has

been described to synthesize equimolar amounts of turanose and

trehalulose.204,206

Scheme 9 The synthesis of sucrose-6-phosphate using permeabilized

cells from S. mutans or K. pneumoniae.

Scheme 10 A schematic representation of sucrose analogs synthesized

using a levansucrase from B. subtilis.



13/17

4.3 Trehalulose

In 1973, Lund and Wyatt identified the a-D-glucopyranosyl-1,1-

b-D-fructose in cultures of Erwinia carotovora var. atroseptica

grown on medium containing 24% sucrose.207 This compound,

also known as trehalulose, is a highly soluble reducing disac-

charide nearly 70% as sweet as sucrose.208 It has been found in

honeydew from Bemisia tabaci (Gennadius), thus relating its

production to Insecta.

209

The presence of trehalulose has beeninvestigated for various plantinsect couples going from 0.3%

up to 70% of the total carbohydrates.210 The biochemical

synthesis of trehalulose was previously described in 1959 using

a-glucosidases from yeast strains.211 Novel methods have since

been developed for the in vitro production of trehalulose.

Among others, sucrose isomerase from Erwinia rhapontici

NCPPB 1578 or immobilized cells of Pseudomonas

mesoacidophila MX-45 have been used for the conversion of

sucrose into trehalulose with yields of 60% and 83%,

respectively.212,213

4.4 Maltulose

a-D-glucopyranosyl-1,4-b-D-fructose, or maltulose, is a natural

sucrose isomer. It was isolated in low yield from a-amylase

hydrolysates of waxy corn starch214 and rabbit liver-glycogen.215

Its presence was also detected during saccharification of

starch.216 It was identified in honey in 1959 thanks to its previ-

ously reported infrared analysis.217,218 The in vitro synthesis of

maltulose from sucrose using intestinal a-glucosidases has also

been described.219

4.5 Isomaltulose

Isomaltulose (a-D-glucopyranosyl-1,6-b-D-fructose or pala-

tinose) was discovered in 1957 in Protaminobacter rubrum iso-

lated from sugar beet raw juice.220 It is about half as sweet as

sucrose but less soluble, less hygroscopic and much more

stable to acidity.221223 The US Food and Drink

Association approved the non-cariogenic health claim for iso-

maltulose in 2007. Moreover, the slow hydrolysis of the glyco-

sidic linkage limits the diffusion of glucose into the blood,

avoiding glycaemia and insulin peaks,224 and making it suitable

as a sweetener for industrial applications.225 Isomaltulose

naturally occurs in honey and sugar cane.226,227 Its biochemical

synthesis has been widely studied and various methods of

production have been proposed.228 Glucosyltransferase-producing microorganism Klebsiella sp. can be used for the

conversion of sucrose into isomaltulose with yields up to 86%.

Strains of Erwinia sp. are also likely to perform this

bioconversion and various processes have been proposed, such

as immobilized cells,229 free cells,230 fermentation,231

potato tubers as bioreactors and high isomaltulose yields

were obtained.232 Bioconversions involving microorganisms

such as Pantoea dispersa UQ68J,233 Enterobacter sp. FMB-1234

and Serratia plymuthica,229,235 have also been investigated

leading to a remarkable increase of conversion rates up to 98

100%.

5 Potential applications of sucrose derivatives in

sugar bioconversion

If recognized by the enzyme, sucrose-like molecules could offer

new opportunities as potential substrates of sucrose-utilizing

a-transglycosidases. Among them, glucansucrases, classified in

families 13 and 70 of glycoside-hydrolases are naturally able to

either polymerize glucose from solely sucrose or glucosylate a

wide variety of hydroxylated acceptors.5,236,237

These enzymes arehighly specific for the glucosyl moiety from sucrose and only a

few examples can be found in the literature where a sucrose

derivative has been used as an alternative glycosyl donor. A

sucrose epimer, namely a-D-galactopyranosyl-1,2-b-D-fructofur-

anoside, has been earlier described as a substrate for a prepara-

tion of amylosucrase from cells ofNeisseria perflava producing a

mixture of galactose, fructose, and an aldosidoketoside, likely

being a trisaccharide.193 Another example concerns the utiliza-

tion by a dextransucrase (E.C.2.4.1.5) of the 2-ketosucrose for

the synthesis of novel carbonyl-group-containing dextrans.129

The last example, to our knowledge, uses allosucrose (a-D-allo-

pyranosyl-1,2-b-D-fructofuranoside) and an amylosucrase func-

tioning as an allosyltransferase to glycosylate low mass acceptormolecules.238

The three sucrose analogs reported to date as an alternative

donor substrate for native glucansucrases only bear subtle

chemical modifications compared to parental sucrose. None-

theless, such successful examples of novel catalytic reactions are

full of promise and one could envision extending the concept to

sucrose-active enzymes in general in order to enlarge accessible

glycodiversification.

6 Conclusions

The main purpose of this article was to review the main biolog-

ical routes reported to date to produce sucrose derivatives oranalogs either by direct isolation from natural sources or in vitro

enzymatic synthesis. These structures may differ in the type of

regio- and/or chemo-modifications of sucrose, the type of

glycosidic linkage, or the nature of the glycosyl moiety linked to

the fructofuranosyl moiety. Libraries of sucrose-related classes

of molecules are thus accessible. Within this pool, sucrose-

derivatives are all attractive intermediates for further glyco-

diversification through carbohydrate chemistry and/or

biochemistry. Such future developments may represent prom-

ising sources for novel oligosaccharides, polysaccharides, sugar-

derived synthons, rare sugars, alternative sweeteners, or biolog-

ically active molecules.

However, all these molecules may not be accessible yet atyields compatible with industrial applications or further deriva-

tization. In addition, regarding biological transformation, the

diversity often remains limited by the substrate specificity of

the enzymes. These drawbacks could be circumvented through

the engineering of enzymes to generate more efficient catalysts

with adequate substrate specificity for non-natural donor or

acceptor substrates,239 although this has not been explored yet

for sucrose-utilizing enzymes. Another major evolution that

could be considered is coming from the rising field of synthetic

biology. Indeed, optimization of native metabolic pathway as

well as redesigning of synthetic metabolic pathways can now be



14/17

investigated for the development of novel synthetic processes to

access carbohydrates displaying original properties and the

multiple products derived from them.

7 Acknowledgements

D. Daude was supported by a grant from the French Ministry of

Research.

8 References

1 S. Peters, T. Rose and M. Moser, Top. Curr. Chem., 2010, 294, 123.2 F. W. Lichtenthaler and S. Peters, C. R. Chim., 2004, 7, 6590.3 Y. Queneau, S. Jarosz, B. Lewandowski and J. Fitremann, Adv.

Carbohydr. Chem. Biochem., 2008, 61, 217292.4 P. Monsan and F. Ouarne in Prebiotics and Probiotics science and

technology, Springer, New York, 2009, pp. 293336.5 I. Andre, G. Potocki-Veronese, S. Morel, P. Monsan and

M. Remaud-Simeon, Top. Curr. Chem., 2010, 294, 2548.6 A. Homann and J. Seibel, Nat. Prod. Rep., 2009, 26, 1555

1571.7 I. Chlubnova, L. Legentil, R. Dureau, A. Pennec, M. Almendros,

R. Daniellou, C. Nugier-Chauvin and V. Ferrieres, Carbohydr.Res., 2012, 356, 4461.

8 S. A. van Hijum, S. Kralj, L. K. Ozimek, L. Dijkhuizenand I. G. vanGeel-Schutten, Microbiol. Mol. Biol. Rev., 2006, 70, 157176.

9 P. Monsan, M. Remaud-Simeon and I. Andre, Curr. Opin.Microbiol., 2010, 13, 293300.

10 E. Champion, I. Andre, C. Moulis, J. Boutet, K. Descroix, S. Morel,P. Monsan, L. A. Mulard and M. Remaud-Simeon, J. Am. Chem.Soc., 2009, 131, 73797389.

11 R. Khan andP. A. Konowicz, Sugar, sugar derivatives, JohnWiley &Sons, Inc., 2000.

12 J. E. Lunn and E. MacRae, Curr. Opin. Plant Biol., 2003, 6, 208214.13 R. R. Selvendran and F. A. Isherwood, Phytochemistry, 1970, 9,

553536.14 K. P. Krause and M. Stitt, Phytochemistry, 1992, 31, 11431146.15 J. G. Buchanan, D. A. Cummerson and D. M. Turner, Carbohydr.

Res., 1972, 21, 283292.16 K. B. Kim and E. J. Behrman, Carbohydr. Res., 1995, 270, 7175.17 S. J. Reid and V. R. Abratt, Appl. Microbiol. Biotechnol., 2005, 67,

312321.18 M. Tangney, C. Rousse, M. Yazdanian and W. J. Mitchell, J. Appl.

Microbiol., 1998, 84, 914919.19 L. Jiang, J. Cai, J. Wang, S. Liang, Z. Xu and S. T. Yang, Bioresour.

Technol., 2010, 101, 304309.20 K. Hiratsukaand H. K. Kuramitsu, J. Dent. Res., 1996, 75, 633633.21 K. Hiratsuka, B. Wang, Y. Sato and H. Kuramitsu, Infect. Immun.,

1998, 66, 37363743.22 P. J. Garegg, S. Oscarson and H. Ritzen, Carbohydr. Res., 1988, 181,

8996.23 S. Oscarson and H. Ritzen, Carbohydr. Res., 1990, 205, 6170.24 S. Oscarson and H. Ritzen, Carbohydr. Res., 1996, 284, 271277.25 I. Wahlberg, E. B. Walsh, I. Forsblom, S. Oscarson, C. R. Enzell,

R. Ryhage and R. Isaksson, Acta Chem. Scand., Ser. B, 1986, 40,724730.

26 Y. Mimaki and Y. Sashida, Phytochemistry, 1991, 30, 937940.27 Y. Sashida, K. Ori and Y. Mimaki, Chem. Pharm. Bull., 1991, 39,

23622368.28 N. Shimazaki, Y. Mimaki and Y. Sashida, Phytochemistry, 1991, 30,

14751480.29 K. I. M. Ki Hyun, C. Sang Wook and L. E. E. Kang Ro, Can. J.

Chem., 2010, 88, 519523.30 M. Hamburger and K. Hostettmann, Phytochemistry, 1985, 24,

17931797.31 Y. Ikeya, K. Sugama, M. Okada and H. Mitsuhashi, Chem. Pharm.

Bull., 1991, 39, 26002605.32 A. Bashir, M. Hamburger, J. D. Msonthi and K. Hostettmann,

Phytochemistry, 1993, 32, 741745.33 O. Shirota, S. Sekita and M. Satake, Phytochemistry, 1997, 44, 695

698.34 S. M. Sang, A. N. Lao, H. C. Wang, Z. L. Chen, J. Uzawa and

Y. Fujimoto, Phytochemistry, 1998, 48, 569571.

35 M. Takasaki, T. Konoshima, S. Kuroki, H. Tokuda andH. Nishino,Cancer Lett., 2001, 173, 133138.

36 I. Yukinobu, T. Shigefumi, T. Mitsuo, K. Humito, T. Kouin,Y. Takuji and A. Masaki, Biol. Pharm. Bull., 2004, 27, 10811085.

37 G. M. She, Y. Y. Ba, Y. Liu, H. Lv, W. Wang and R. B. Shi,Molecules, 2011, 16, 55075513.

38 J. Robin and Y. Rolland, World Pat, WO/2004/069218 (France).39 V. Vontimitta, D. A. Danehower, T. Steede, H. S. Moon and

R. S. Lewis, J. Agric. Food Chem., 2010, 58, 294300.40 A. Lopez-Munguia, Y. Hernandez-Romero, J. Pedraza-Chaverri,

A. Miranda-Molina, I. Regla, A. Martinez and E. Castillo, PLoSOne, 2011, 6.

41 K. Astwood, B. Lee and M. Manley-Harris, J. Agric. Food Chem.,1998, 46, 49584962.

42 A. Deifel, Apidologie, 1983, 14, 276277.43 R. Mateo and F. BoschReig, Food Chem., 1997, 60, 3341.44 F. L. Wackers, J. Insect Physiol., 2001, 47, 10771084.45 G. Daniele and H. Casabianca, Food Chem, 2012, 134, 10251029.46 T. Taga, E. Inagaki, Y. Fujimori and S. Nakamura, Carbohydr. Res.,

1993, 240, 3945.47 T. Taga, E. Inagaki, Y. Fujimori and S. Nakamura, Carbohydr. Res.,

1994, 251, 203212.48 T. Yamada, K. Igarashi and M. Mitsutomi, J. Dent. Res., 1980, 59,

21572162.49 T. Yamada, S. Kimura and K. Igarashi, Caries Res., 1980, 14, 239

247.50 M. K. Fischer, W. Volkl, R. Schopf and K. H. Hoffmann, J. Insect

Physiol., 2002, 48, 319326.51 A. Vantaux, T. Parmentier, J. Billen and T. Wenseleers, Anim.

Behav., 2012, 83, 257262.52 A. Vantaux, W. Van den Ende, J. Billen and T. Wenseleers, J. Insect

Physiol., 2011, 57, 16141621.53 B. Stadler and A. F. G. Dixon, Annu. Rev. Ecol., Evol. Syst., 2005,

36, 345372.54 K. Hirotsu and A. Shimada, Chem. Lett., 1973, 8386.55 D. Avenel, A. Neuman and H. Gillierpandraud, Acta Crystallogr.,

Sect. B: Struct. Crystallogr. Cryst. Chem., 1976, 32, 25982605.56 J. Becquart, A. Neuman and H. Gillierpandraud, Carbohydr. Res.,

1982, 111, 921.57 A. Meyer, Arch. Pharm., 1883, 221, 561576.58 N. Albon, D. Bell, P. Blanchard, D. Gross and J. Rundell, J. Chem.

Soc., 1953, 2427.59 I. Siddiqui and B. Furgala, J. Apicult. Res., 1968, 7, 5159.

60 E. de la Fuente, A. I. Ruiz-Matute, R. M. Valencia-Barrera, J. Sanzand I. M. Castro, Food Chem., 2011, 129, 14831489.61 G. Hendry, New Phytol., 1987, 106, 201216.62 C. J. Pollock and T. L. Housley, Plant Physiol., 1993, 102, 537539.63 A. J. Cairns, New Phytol., 1993, 123, 1524.64 N. J. Chatterton, P. A. Harrison, W. R. Thornley and J. H. Bennett,

New Phytol., 1988, 109, 2933.65 P. Chuankhayan, C. Y. Hsieh, Y. C. Huang, Y. Y. Hsieh,

H. H. Guan, Y. C. Hsieh, Y. C. Tien, C. D. Chen, C. M. Chiangand C. J. Chen, J. Biol. Chem., 2010, 285, 2324923262.

66 K. L. Forsythe and M. S. Feather, Carbohydr. Res., 1989, 185, 315319.

67 K. L. Forsythe, M. S. Feather, H. Gracz and T. C. Wong, PlantPhysiol., 1990, 92, 10141020.

68 M. Blanch, M. T. Sanchez-Ballesta, M. I. Escribano andC. Merodio, Food Chem., 2011, 129, 724730.

69 L. Dorland, J. Kamerling, J. Vliegenthart and M. Satyanarayana,

Carbohydr. Res., 1977, 54, 275284.70 W. Kahl, A. Roszkowski and A. Zurowska, Carbohydr. Res., 1969,

10, 586588.71 D. Englis, R. Decker and A. Adams, J. Am. Chem. Soc., 1925, 47,

27242726.72 H. Annett, Biochem. J., 1917, 11, 16.73 V. Loiseau, J. Fabr. Sucre, 1889.74 W. Stone and W. Baird, J. Am. Chem. Soc., 1897, 19, 116

124.75 T. M. Kuo, J. F. Vanmiddlesworth and W. J. Wolf, J. Agric. Food

Chem., 1988, 36, 3236.76 M. Muzquiz, C. Burbano, M. M. Pedrosa, W. Folkman and

K. Gulewicz, Ind. Crops Prod., 1999, 9, 183188.77 I. R. Kennedy, O. D. Mwandemele and K. S. Mcwhirter, Food

Chem., 1985, 17, 8593.



15/17

78 S. Allen and W. Hitz, United States Pat, US8071591 (United States).79 T. Sako, K. Matsumoto andR. Tanaka, Int. Dairy J., 1999, 9, 6980.80 C. E. Rycroft, M. R. Jones, G. R. Gibson and R. A. Rastall, J. Appl.

Microbiol., 2001, 91, 878887.81 N. Takakuwa, M. Tamura, M. Ohnishi and Y. Oda, World J.

Microbiol. Biotechnol., 2007, 23, 587591.82 N. Tada, M. Sato, E. Amann and S. Ogawa, Theriogenology, 1993,

40, 333344.83 K. Sonoyama, H. Watanabe, J. Watanabe, N. Yamaguchi,

A. Yamashita, H. Hashimoto, E. Kishino, K. Fujita, M. Okada,

S. Mori, S. Kitahata and J. Kawabata, J. Nutr., 2005, 135, 538543.84 L. Lehle and W. Tanner, Eur. J. Biochem., 1973, 38, 103110.85 T. Schneider and F. Keller, Plant Cell Physiol., 2009, 50, 21742182.86 G. L. Salerno and H. G. Pontis, Plant Physiol., 1989, 89, 648651.87 E. Hungerford and A. Nees, Ind. Eng. Chem., 1934, 26, 462464.88 H. Olbrich, The molasses, Biotechnology-Kempe GmbH, Berlin,

2006 edn, 1963.89 K. Sayama, T. Kamada, S. Oikawaand T. Masuda, Zuckerindustrie,

1992, 117, 893898.90 H. Inoue, Y. Semba, O. Suda and O. Y., United States Pat,

US8071591 (United States).91 A. MacLeod and H. McCorquodale, Nature, 1958, 4638, 815816.92 N. Pavis, N. J. Chatterton, P. A. Harrison, S. Baumgartner,

W. Praznik, J. Boucaud and M. P. Prudhomme, New Phytol.,2001, 150, 8395.

93 N. Chatterton, P. Harrison and W. Thornley, Plant Physiol., 1993,12, 113116.

94 V. Amiard, A. Morvan-Bertrand, J. P. Billard, C. Huault, F. Kellerand M. P. Prudhomme, Plant Physiol., 2003, 132, 22182229.

95 N. Wattiez and M. Hans, Bull. Acad. R. Med. Belg., 1943, 8, 386.96 D. Rohrer, Acta Crystallogr., Sect. B: Struct. Crystallogr. Cryst.

Chem., 1972, 28, 425433.97 H. Herissey, Bull. Soc. Chim. Biol., 1957, 39, 15531555.98 D. French, J. Am. Chem. Soc., 1955, 77, 10241025.99 C. Jukes and D. Lewis, Phytochemistry, 1974, 13, 15191521.

100 A. I. Ruiz-Matute, M. L. Sanz and I. Martinez-Castro, J.Chromatogr., A, 2007, 1157, 480483.

101 T. Suami, T. Otake, T. Nishimura and T. Ikeda, Bull. Chem. Soc.Jpn., 1973, 46, 10141016.

102 M. Linscheid, D. Wendisch and D. Strack, Z. Naturforsch, 1980, 35,907914.

103 Y. Fukuyama, T. Sato, I. Miura, Y. Asakawa and T. Takemoto,Phytochemistry, 1983, 22, 549552.

104 R. F. Severson, R. F. Arrendale, O. T. Chortyk, C. R. Green,F. A. Thome, J. L. Stewart and A. W. Johnson, J. Agric. FoodChem., 1985, 33, 870875.

105 K. Nakano, K. Murakami, Y. Takaishi and T. Tomimatsu, Chem.Pharm. Bull., 1986, 34, 50055010.

106 H. Shimomura, Y. Sashida and Y. Mimaki, Phytochemistry, 1986,25, 28972899.

107 Y. Shoyama, K. Hatano, I. Nishioka and T. Yamagishi,Phytochemistry, 1987, 26, 29652968.

108 L. J. Harrison, G. L. Sia, K. Y. Sim, H. T. W. Tan, J. D. Connolly,C. Lavaud and G. Massiot, Phytochemistry, 1995, 38, 14971500.

109 D. M. Zhang, T. Miyase, M. Kuroyanagi, K. Umehara andH. Noguchi, Phytochemistry, 1998, 47, 4552.

110 T. Miyase, H. Noguchi andX. M. Chen, J. Nat. Prod., 1999,62, 993996.

111 T. Chen, J. X. Li and Q. Xu, Phytochemistry, 2000, 53, 10511055.112 N. L. Wang, X. S. Yao, R. Ishii and S. Kitanaka, Phytochemistry,

2003, 62, 741746.113 M. I. Choudhary, A. Begum, A. Abbaskhan, R. Shafiq ur and

R. Atta ur, Carbohydr. Res., 2006, 341, 23982405.114 Y.Wang, W.Y. Gao,T. J.Zhangand Y.Q. Guo, Chin. Chem. Lett.,

2007, 18, 548550.115 L. Zhang, C. C. Liao, H. C. Huang, Y. C. Shen, L. M. Yang and

Y. H. Kuo, Phytochemistry, 2008, 69, 13981404.116 P. Wang, S. Y. Li, S. Ownby, Z. Z. Zhang, W. Yuan, W. L. Zhang

and R. S. Beasley, Phytochemistry, 2009, 70, 430436.117 L. Lepore, N. Malafronte, F. B. Condero, M. J. Gualtieri, S. Abdo,

F. Dal Piaz and N. De Tommasi, Fitoterapia, 2011, 82, 178183.118 R. Andersson, O. Larm, E. Scholander andO. Theander, Carbohydr.

Res., 1980, 78, 257265.119 F. W. Lichtenthaler and S. Mondel, Pure Appl. Chem., 1997, 69,

18531866.

120 W. M. Kurowski, J. Appl. Chem. Biotechnol., 1976, 26, 579580.121 W. M. Kurowski and J. Darbyshire, J. Appl. Chem. Biotechnol.,

1978, 28, 638640.122 E. Stoppok,J. Walter andK. Buchholz, Appl. Microbiol. Biotechnol.,

1995, 43, 706712.123 C. Simiand, E. Samain, O. R. Martin and H. Driguez, Carbohydr.

Res., 1995, 267, 115.124 L. Hough and E. Obrien, Carbohydr. Res., 1981, 92, 314317.125 P. Sedmera, P. Halada, E. Kubatova, D. Haltrich, V. Prikrylova and

J. Volc, J. Mol. Catal. B: Enzym., 2006, 41, 3242.

126 C. K. Peterbauer and J. Volc, Appl. Microbiol. Biotechnol., 2010, 85,837848.

127 C. Sygmund, R. Kittl, J. Volc, P. Halada, E. Kubatova, D. Haltrichand C. K. Peterbauer, J. Biotechnol., 2008, 133, 334342.

128 J. Volc, P. Sedmera, P. Halada, G. Daniel, V. Prikrylova andD. Haltrich, J. Mol. Catal. B: Enzym., 2002, 17, 91100.

129 H. Seto, H. Kawakita, K. Ohto, H. Harada and K. Inoue,Carbohydr. Res., 2008, 343, 24172421.

130 M. Pietsch, M. Walter and K. Buchholz, Carbohydr. Res., 1994, 254,183194.

131 V. Timme, R. Buczys and K. Buchholz, Chem. Ing. Tech., 2001, 73,13571361.

132 T. Polat and R. J. Linhardt, J. Surfactants Deterg., 2001, 4, 415421.133 R. Ratnam, M. Mofizuddin and S. Aurora, World Pat,

WO2006120697 (India).134 Q. H. Wang, S.F. Zhang and J. Z. Yang, Carbohydr. Res., 2007, 342,

26572663.

135 C. Chauvin, K. Baczko and D. Plusquellec, J. Org. Chem., 1993, 58,22912295.

136 Y. Queneau, S. Chambert, C. Besset and R. Cheaib, Carbohydr.Res., 2008, 343, 19992009.

137 M. Woudenberg-van-Oosterom, F. vanRantwijk and R. A. Sheldon,Biotechnol. Bioeng., 1996, 49, 328333.

138 M. Ferrer, M. A. Cruces, M. Bernabe, A. Ballesteros and F. J. Plou,Biotechnol. Bioeng., 1999, 65, 1016.

139 J. E. Kim, J. J. Han, J. H. Yoon and J. S. Rhee, Biotechnol. Bioeng.,1998, 57, 121125.

140 M. A. Ku and Y. D. Hang, Biotechnol. Lett., 1995, 17, 10811084.

141 J. O. Rich, B. A. Bedell and J. S. Dordick, Biotechnol. Bioeng., 1995,45, 426434.

142 F. J. Plou, M. A. Cruces, M. Ferrer, G. Fuentes, E. Pastor,M. Bernabe, M. Christensen, F. Comelles, J. L. Parra and

A. Ballesteros, J. Biotechnol., 2002, 96, 5566.143 R. Ratnam and B. Chandrashekar, World Pat, WO/2007/066356062007 (India).

144 R. Gulati, R. K. Saxena, R. Gupta, R. P. Yadav andW. S. Davidson, Process Biochem., 2000, 35, 459464.

145 S. Riva, J. Chopineau, A. P. G. Kieboom and A. M. Klibanov,J. Am. Chem. Soc., 1988, 110, 584589.

146 P. Potier, A. Bouchu, G. Descotes and Y. Queneau, TetrahedronLett., 2000, 41, 35973600.

147 H. G. Park and H. N. Chang, Biotechnol. Lett., 2000, 22, 3942.148 H. G. Park, H. N. Chang and J. S. Dordick, Biotechnol. Bioeng.,

2001, 72, 541547.149 O. J. Park, G. J. Jeon and J. W. Yang, Enzyme Microb. Technol.,

1999, 25, 455462.150 D. B. Sarney, M. J. Barnard, D. A. MacManus and E. N. Vulfson,

J. Am. Oil Chem. Soc., 1996, 73, 14811487.151 J. D. Jones, A. J. Hacking and P. S. J. Cheetham, Biotechnol.

Bioeng., 1992, 39, 203210.152 Y. W. Han, G. M. Liu, D. Y. Huang, B. J. Qiao, L. P. Chen,

L. H. Guan and D. B. Mao, New Biotechnol., 2011, 28, 1418.153 D. C. Palmer and F. Terradas, Tetrahedron Lett., 1994, 35, 1673

1676.154 G. T. Ong, K. Y. Chang, S. H. Wu and K. T. Wang, Carbohydr.

Res., 1993, 241, 327333.155 M. Bednarczyk, M. Urbanowski, P. Gulewicz, K. Kasperczyk,

G. Maiorano and T. Szwaczkowski, Bull. Vet. Inst. Pulawy, 2011,55, 465469.

156 G. Kunova, V. Rada, I. Lisova, S. Rockova and E. Vlkova, Czech J.Food Sci., 2011, 29, S49S54.

157 M. Sabater-Molina, E. Larque, F. Torrella and S. Zamora,J. Physiol. Biochem., 2009, 65, 315328.

158 S. H. Baik, Food Sci. Biotechnol., 2010, 19, 8387.



16/17

159 W. Li, X. L. Xiang, S. F. Tang, B. Hu, L. Tian, Y. Sun, H. Ye andX. X. Zeng, J. Agric. Food Chem., 2009, 57, 39273933.

160 P. M. Dey, FEBS Lett., 1980, 114, 153156.161 J. Courtois, F. Petek and T. Dong, Bull. Soc. Chim. Biol., 1961, 43,

11891196.162 H. Hopf and O. Kandler, Plant Physiol., 1974, 54, 1314.163 J. Woodring, R. Wiedemann, W. Volkl and K. H. Hoffmann, J.

Appl. Entomol., 2007, 131, 17.164 A. Pilgrim, M. Kawase, M. Ohashi, K. Fujita, K. Murakami and

K. Hashimoto, Biosci., Biotechnol., Biochem., 2001, 65, 758765.

165 G. Avigad, J. Biol. Chem., 1957, 229, 121129.166 H. J. Choi, C. S. Kim, P. Kim, H. C. Jung and D. K. Oh, Biotechnol.

Prog., 2004, 20, 18761879.167 W. C. Han, S. H. Byun, M. H. Kim, E. H. Sohn, J. D. Lim,

B. H. Um, C. H. Kim, S. A. Kang and K. H. Jang, J. Microbiol.Biotechnol., 2009, 19, 11531160.

168 W. C. Han, S. H. Byun, J. C. Lee, M. H. Kim, S. A. Kang,C. H. Kim, E. W. Son and K. H. Jang, J. Biotechnol., 2007, 131,S113S113.

169 K. Fujita, K. Hara, H. Hashimoto and S. Kitahata, Agric. Biol.Chem., 1990, 54, 26552661.

170 M. Ferrer, J. Soliveri, F. J. Plou, N. Lopez-Cortes, D. Reyes-Duarte,M. Christensen, J. L. Copa-Patino and A. Ballesteros, EnzymeMicrob. Technol., 2005, 36, 391398.

171 B. R. Somashekar and S. Divakar, Enzyme Microb. Technol., 2007,40, 299309.

172 G. Y. Li, Y. J. Cai, Z. K. Hao and X. R. Liao, Eng. Life Sci., 2011,

11, 615619.173 N. R. Pedersen, P. J. Halling, L. H. Pedersen, R. Wimmer,

R. Matthiesen and O. R. Veltman, FEBS Lett., 2002, 519, 181184.

174 H. K. Kang, M. Y. Seo, E. S. Seo, D. Kim, S. Y. Chung, A. Kimura,D. F. Day and J. F. Robyt, Biochim. Biophys. Acta, Gene Struct.Expression, 2005, 1727, 515.

175 J. Seibel, R. Moraru, S. Gotze, K. Buchholz, S. Naamnieh,A. Pawlowski and H. J. Hecht, Carbohydr. Res., 2006, 341, 23352349.

176 J. A. M. Vanbalken, T. J. G. M. Vandooren, W. J. J. Vandentweel,J. Kamphuis and E. M. Meijer, Appl. Microbiol. Biotechnol., 1991,35, 216221.

177 S. Hayashi, J. Kinoshita, M. Nonoguchi, Y. Takasaki andK. Imada,Biotechnol. Lett., 1991, 13, 395398.

178 J. Rehm, L. Willmitzer and A. G. Heyer, J. Bacteriol., 1998, 180,

13051310.179 M. Tieking, W. Kuhnl and M. G. Ganzle, J. Agric. Food Chem.,2005, 53, 24562461.

180 A. Zuccaro, S. Gotze, S. Kneip, P. Dersch and J. Seibel,ChemBioChem, 2008, 9, 143149.

181 S. M. Kritzinger, S. G. Kilian, M. A. Potgieter and J. C. du Preez,Enzyme Microb. Technol., 2003, 32, 728737.

182 D. Linde, B. Rodriguez-Colinas, M. Estevez, A. Poveda, F. J. Plouand M. Fernandez Lobato, Bioresour. Technol., 2012, 109, 123130.

183 P. Katapodis and P. Christakopoulos, World J. Microbiol.Biotechnol., 2004, 20, 667672.

184 M. Alvaro-Benito, M. de Abreu, L. Fernandez-Arrojo, F. J. Plou,J. Jimenez-Barbero, A. Ballesteros, J. Polaina and M. Fernandez-Lobato, J. Biotechnol., 2007, 132, 7581.

185 S. Farine, C. Versluis, P. J. Bonnici, A. Heck, C. Lhomme,A. Puigserver and A. Biagini, Appl. Microbiol. Biotechnol., 2001,

55, 5560.186 P. Gutierrez-Alonso, L. Fernandez-Arrojo, F. J. Plou and

M. Fernandez-Lobato, FEMS Yeast Res., 2009, 9, 768773.187 E. J. St Martin and C. L. Wittenberger, Infect. Immun., 1979, 24,

865868.188 E. J. St Martin and C. L. Wittenberger, Infect. Immun., 1979, 26,

487491.189 J. Thompson, S. A. Robrish, A. Pikis, A. Brust and

F. W. Lichtenthaler, Carbohydr. Res., 2001, 331, 149161.190 F. Kunst, M. Pascal, J. A. Lefesant, J. Walle and R. Dedonder, Eur.

J. Biochem., 1974, 42, 611620.191 J. Seibel, R. Moraru and S. Gotze, Tetrahedron, 2005, 61, 7081

7086.192 G. Avigad, D. S. Feingold and S. Hestrin, Biochim. Biophys. Acta,

1956, 20, 129134.

193 G. Avigad, D. S. Feingold and S. Hestrin, J. Biol. Chem., 1957, 224,295307.

194 P. M. Coutinho and B. Henrissat, Recent Advancesin CarbohydrateBioengineering, 1999, pp. 312.

195 F. Stodola, E. Sharpe and H. Koepsell, J. Am. Chem. Soc., 1956, 78,25142518.

196 R. Bailey and E. Bourne, Nature, 1959, 184, 904905.197 M. Boker, H. J. Jordening and K. Buchholz, Biotechnol. Bioeng.,

1994, 43, 856864.198 K. D. Reh, M. NollBorchers and K. Buchholz, Enzyme Microb.

Technol., 1996, 19, 518524.199 K. Buchholz, M. Noll-Borchers and D. Schwengers, Starch/Staerke,

1998, 50, 164172.200 N. S. Han, S. Y. Kang, S. B. Lee and J. F. Robyt, Food Sci.

Biotechnol., 2005, 14, 317322.201 C. Hudson and E. Pacsu, J. Am. Chem. Soc., 1930, 52, 25192524.202 G. P. de Montalk, M. Remaud-Simeon, R. M. Willemot,

P. Sarcabal, V. Planchot and P. Monsan, FEBS Lett., 2000, 471,219223.

203 S. Pizzut-Serin, G. Potocki-Veronese, B. A. van der Veen,C. Albenne, P. Monsan and M. Remaud-Simeon, FEBS Lett.,2005, 579, 14051410.

204 F. Guerin, S. Barbe, S. Pizzut-Serin, G. Potocki-Veronese,D. Guieysse, V. Guillet, P. Monsan, L. Mourey, M. Remaud-Simeon, I. Andre and S. Tranier, J. Biol. Chem., 2012, 287, 66426654.

205 R. Wang, J. Bae, J. Kim, B. Kim, S. Yoon, C. Parkand S. Yoo, Food

Chem., 2012, 132, 773779.206 S. Emond, S. Mondeil, K. Jaziri, I. Andre, P. Monsan, M. Remaud-

Simeon and G. Potocki-Veronese, FEMS Microbiol. Lett., 2008,285, 2532.

207 B. Lund and G. Wyatt, J. Gen. Microbiol., 1973, 78, 331336.208 T. Ooshima, A. Izumitani, T. Minami, T. Fujiwara, Y. Nakajima

and S. Hamada, Caries Res., 1991, 25, 277282.209 R. B. Bates, D. N. Byrne, V. V. Kane, W. B. Miller andS. R. Taylor,

Carbohydr. Res., 1990, 201, 342345.210 D. N. Byrne, D. L. Hendrix and L. H. Williams, Physiol. Entomol.,

2003, 28, 144149.211 G. Avigad, Biochem. J., 1959, 73, 587593.212 T. Veronese, A. Bouchu and P. Perlot, Biotechnol. Tech., 1999, 13,

4348.213 Y. Nagai, T. Sugitani, K. Yamada, T. Ebashi and S. Kishihara,

Nippon Shokuhin Kagaku Kogaku Kaishi, 2003, 50, 488492.

214 M. Radomski and M. Smith, Cereal Chem., 1962, 39, 30.215 S. Peat, P. Roberts and W. Whelan, Biochem. J., 1952, 51, XVIIXVIII.

216 F. F. Dias and D. C. Panchal, Starch/Staerke, 1987, 39, 6466.217 J. White and N. Hoban, Arch. Biochem. Biophys., 1959, 80, 386392.218 J. White, C. Eddy, J. Petty and N. Hoban, Anal. Chem., 1958, 30,

506.219 A. Taufel, H. Ruttloff and K. Taufel, Carbohydr. Res., 1967, 5, 223

225.220 R. Weidenhagen and S. Lorenz, Z. Zuckerind., 1957, 7, 533534.221 T. Kaga and T. Mizutani, Seito Gitjutsu Kenkyukaishi, 1985, 34, 45

57.222 H. Schiweck, M. Munir, K. M. Rapp, B. Schneider and M. Vogel,

Zuckerindustrie, 1990, 115, 555565.223 B. A. R. Lina, D. Jonker and G. Kozianowski, Food Chem. Toxicol.,

2002, 40, 13751381.224 K. Kawai, H. Yoshikawa, Y. Murayama, Y. Okuda and

K. Yamashita, Horm. Metab. Res., 1989, 21, 338340.225 I. Takazoe, G. Frostell, K. Ohta, V. Topitsoglou and N. Sasaki,

Swed. Dent. J., 1985, 9, 8187.226 I. Siddiqui and B. Furgala, J. Apic. Res., 1967, 6, 139145.227 I. Takazoe, Int. Dent. J., 1985, 35, 5865.228 E. J. Vandamme and W. Soetaert, FEMS Microbiol. Rev., 1995, 16,

163186.229 H. Y. Kawaguti and H. H. Sato, Food Chem., 2010, 120, 789793.230 H. Y. Kawaguti, M. F. Buzzato and H. H. Sato, J. Ind. Microbiol.

Biotechnol., 2007, 34, 261269.231 H. Y. Kawaguti and H. H. Sato, Process Biochem., 2007, 42, 472

479.232 F. Bornke, M. Hajirezaei and U. Sonnewald, J. Biotechnol., 2002, 96,

119124.233 L. Wu and R. G. Birch, J. Appl. Microbiol., 2004, 97, 93103.



17/17

234 M. H. Cho, S. E. Park, J. K. Lim, J. S. Kim, J. H. Kim, D. Y. Kwonand C. S. Park, Biotechnol. Lett., 2007, 29, 453458.

235 A. Krastanov, D. Blazheva, I. Yanakieva and M. Kratchanova,Enzyme Microb. Technol., 2006, 39, 13061312.

236 G. T. Richard, S. Yu, P. Monsan, M. Remaud-Simeon andS. Morel,Carbohydr. Res., 2005, 340, 395401.

237 A. Bertrand, S. Morel, F. Lefoulon, Y. Rolland, P. Monsan andM. Remaud-Simeon, Carbohydr. Res., 2006, 341, 855 863.

238 J. Schneider and B. Hofer, FEBS J., 2007, 274, 373373.239 G. J. Williams, R. W. Gantt and J. S. Thorson, Curr. Opin. Chem.

Biol., 2008, 12, 556564.

sucrose analogs- an attractive (bio)source for glycodiversiﬁcation

Documents