Feruloylated oligosaccharides: Structure, metabolism and function

JOURNAL OF FUNCTIONAL FOODS

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Feruloylated oligosaccharides: Structure, metabolism and function Juanying Oua, Zheng Sunb,* a

College of Life Science, South China Agricultural University, Guangzhou 510642, China College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China

b

A R T I C L E I N F O

A B S T R A C T

Article history:

Feruloylated oligosaccharides consist of a large group of compounds that are mainly pro-

Available online xxxx

duced from the hydrolysis of feruloylated polysaccharides. Some are commercially available in the market. In the bound form, ferulic acid is usually esterified at position C-2 or

Keywords:

C-5 to L-arabinofuranosyl residues, at position C-6 to b-D-galactopyranosyl residues, and

Ferulic acid

at position C-4 to D-xylopyranosyl residues. This review summarises current knowledge

Functional ingredient

on feruloylated oligosaccharides, including their structures, physiological functions, prep-

Antioxidant activity

aration methods, metabolism and absorption in the colon. Future research trends are also

Enzymatic synthesis

discussed.

Absorption in the colon

1.

Introduction

Ferulic acid, a natural antioxidant with free radical scavenging activities, is a major phenolic acid found in many cereals (Liyana-pathirana & Shahidi, 2004; Shahidi & Wanasundara, 1992). The main form of ferulic acid is the bound form as feruloylated oligosaccharides from the hydrolysis of polysaccharides. Members of feruloylated oligosaccharides may differ from each other in terms of the composition and number of glycosylated monosaccharides, the species of sugar residues linked by ferulic acid and the linking position, the contents of ferulic acid, and whether they contain di-, tri-, tetra-ferulic acid or p-coumaric acid. The first feruloylated oligosaccharide product (GRAS Notice 000343) was developed as the wheat bran extract and was approved by the Division of Biotechnology and GRAS Notice Review, United States Food and Drug Administration (FDA) in 2010. This product is composed of xylo- and arabinoxylo-oligosaccharides derived from arabinoxylan with 1–3% of bound ferulic acid. Feruloylated oligosaccharides owe their nutritional

Ó 2013 Elsevier Ltd. All rights reserved.

functions to both ferulic acid and oligosaccharides. They are stable under low pH and high temperature. As excellent functional ingredients, feruloylated oligosaccharides have a wide range of applications in food industry, such as in baked goods, beverage bases, breakfast cereals, frozen dairy desserts, gelatine and puddings, grain products, jams and jellies, milk products, processed fruits and vegetables, and so on. In this review, an exhaustive overview involving the most updated research activities on feruloylated oligosaccharides is given, introducing their structures, physiological functions, preparation methods, metabolism as well as obstacles and future research trends.

2.

Structure

The identification of free feruloylated oligosaccharides in plants is rarely reported, except for trans- and cis-feruloyl4-b-glucoside found in the stems of Equisetum hyemale (Park & Tomohiko, 2011) and leucosceptoside A, a derivative

* Corresponding author. Tel./fax: +86 21 61900424. E-mail address: [email protected] (Z. Sun). 1756-4646/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jff.2013.09.028

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of feruloylated oligosaccharide found in Eremostachys glabra (Delazar et al., 2004). Feruloylated oligosaccharides are usually gained from the esterified polysaccharides of plant cell walls by mild acid hydrolysis or treatment with a mixture of polysaccharide-hydrolysing enzymes without the esterase activity, such as driselase (Ishii, 1997). In dicotyledons, ferulic acid is associated with pectic polysaccharides via ester linkages at position C-2 to arabinofuranose or position C-6 to galactopyranose residues. These linkages have been found in spinach and sugar beet. In sugar beet pulp, approximately 45–50% of ferulic acid was found to be linked at position C-6 of galactose residues whilst 50–55% was linked at position C-2 of arabinose residues (de O. Buanafina, 2009). Compared with dicots, monocots have lower amounts of pectins, usually less than 5% (w:w). Ferulic acid in monocots is mainly linked to cell wall polymers by either ester bonds through their carboxylic acid group with the a-L-arabinosyl side chains of xylans or via ether bonds linked to lignin monomers (de O. Buanafina et al., 2009; Ishii, 1997). p-Coumaric acid is a phenolic acid that exists abundantly in the cell walls of monocots. Although it is primarily associated with lignin, it can be esterified to polysaccharides (Scheller & Ulvskov, 2010). Feruloylation is believed to occur co-synthetically with the polymerisation of sugars and stops one day after cessation of polysaccharide accumulation (Ishii, 1997). Feruloylation to arabinoxylan occurs intracellularly by feruloyl transferases with feruloyl glucose as a substrate (Obel, Celia, Henrik, & Scheller, 2003). Different plants show differences in polysaccharide structures, ferulic and coumaric acid contents, and the linkage position of phenolic acids to the sugar residues of polysaccharides (Harris & Trethewey, 2010). Some typical feruloylated oligosaccharides prepared from plant sources are listed in Table 1. As shown in the table, ferulic acid is linked at position C-5 to L-arabinofuranosyl side groups in arabinoxylans, C-2 to a-L-arabinofuranosyl residues in arabinans, C-6 to b-D-galactopyranosyl residues in galactans and C-4 to a-D-xylopyranosyl side groups in xyloglucans (Kylli et al., 2008). p-Coumaric acid is mainly esterified at position C-5 to arabinose in barley straw, bamboo shoot and Cynodom dactylon. With the exception of cellulose, b-1,3–1,4-linked glucan in grasses and glycoproteins in cell walls, the O-acetylation of sugar residues in polysaccharides may occur in almost all cell wall polymers, including O-2 and O-5 of arabinose, O-6 of glucose, O-2 and O-3 of xylose, mannose and galacturonic acid, O-3, O-4, O-6 of galactose and O-3 of rhamnose in both backbone and side chains of polysaccharides (Gille & Pauly, 2012). Acetylated arabinose at O-2 is detected in sugarcane bagasse and bamboo shoot after linkage with ferulic and coumaric acids (Allerdings, Ralph, Steinhart, & Bunzel, 2006; Ishii, 1997). Feruloylated oligosaccharides from different plants have distinct monosaccharide compositions. Xylose and arabinose are the most common monosaccharides in feruloylated oligosaccharides, although some of them also contain galactose and glucose (Table 1). Feruloylated arabinotetraose with ferulic acid esterified to two neighbouring arabinose residues at positions O-5 and O-2 (Fig. 1) has been identified from sugar beet cell walls (Levigne et al., 2004). A highly feruloylated, low-molecular-weight arabinoxylan with high arabinose:xylose ratio (nearly 1:1) has been found in wheat and

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barley flour, malted rice and ragi. In this substance, some of the xylose residues are disubstituted with arabinose at positions C-2 (highly feruloylated) and C-3 (non-feruloylated) (Cleemput et al., 1995; Rao & Muralikrishna, 2007; Trogh, Courtin, & Delcour, 2004). In addition to esterification to sugar residues, ferulic acid molecules can link to each other to form dehydrodiferulic acids (DFAs) via oxidative and/or photochemical dimerisation processes. Up to nine DFAs have been identified in different plant materials, namely, 8-O-4-DFA, 8–5 cyclic-DFA, 5 non-cyclic-DFA, 8–5 decarboxylated-DFA, 5–5-DFA, 8–8 non-cyclic-DFA, 8–8 cyclic-DFA, 8–8-tetrahydrofuran-DFA and 4-O-5-DFA (Bunzel, 2010; Dobberstein & Bunzel, 2010; Grabber, Ralph, & Hatfield, 2000). After hydrolysis of feruloylated polysaccharides, di-feruloylated oligosaccharide is produced. Three types of feruloylated oligosaccharides with 8O-4-coupled DFA, as well as one feruloylated oligosaccharide with 8–8 (cyclic)-coupled DFA have been separated from maize bran through mild acidic hydrolysis (Allerdings et al., 2005). The total DFA content ranges from 0.24 to 1.26% of the insoluble fibre, with the 8–5 link as the dominant species (Wong, 2006). Total DFA contents in whole grains of maize, wheat, spelt, rice, wild rice, barley and millet were found to be 12,596, 2372, 2601, 4042, 2840, 3658, 3647, 3599 and 5693 lg/g, respectively (Bunzel, Ralph, Marita, Hatfield, & Steinhart, 2001). DFAs in maize bran, sugar beet pulp, rye bran and wheat bran are 25, 14, 0.98 and 0.89 mg/g, respectively (Andreasen, Christensen, Meyer, & Hansen, 2000; Kroon, Garcia-Cones, Fillingham, Hazlewood, & Williamson, 1999; Saulnier & Thibault, 1999). Previous studies have also identified a dehydrotrimer and two tetramers of ferulic acid from the alkaline hydrolysates of maize bran (Bunzel, Ralph, Bruning, & Steinhart, 2006; Fry, Willis, & Paterson, 2000; Rouau et al., 2003) (Fig. 2). However, no tri- and tetramer-linking oligosaccharides have yet been separated.

3.

Physiological functions

Feruloylated oligosaccharides are water-soluble and thermally stable, acting as the promising materials for applications in food, pharmaceutical and cosmetic industries. Feruloylated oligosaccharides contain both hydrophobic ferulic acid moieties and hydrophilic oligosaccharide moieties, and therefore possess the physiological functions of both including antioxidant activity, probiotic effects as well as inhibition against glycation.

3.1.

Antioxidant activity

As a major phenolic acid found in cereals, ferulic acid is well known for its ability to scavenge free radicals (Shahidi, 1997, 2000). Its combination with oligosaccharides, a novel antioxidant, results in the synergistic antioxidant capacities of feruloylated oligosaccharides (Lyons, Chen, & Yan, 2005; Ngo, Lee, Kim, & Kim, 2009). Kylli et al. (2008) evaluated various ferulic acid glycoside esters (e.g. at positions C-2, C-3 and C-6). It was found that the esterification in the primary

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Table 1 – Structure of feruloylated and P-coumaroylated oligosaccharides prepared from plant cell walls. Plant source

Structure

References

Wheat

(5-O-FA-a-L-Ara)-1,3-D-Xyl

Ishii (1997)

Maize bran

(5-O-FA-a-L-Ara)-1,3-Xyl-1,4-D-Xyl; O-b-D-Xyl-1,2-(O-5-O-FA-L-Ara)-O-b-D-Xyl-1,3-b-D-Xyl-1,2-O-(5-O-FA-L-Ara); O-L-Gal-1,4-O-D-Xyl-1.2-(5-O-FA-L-Ara)-O-4-O-FA-a-D-Xyl-1,6-D-Gluc; a-D-Xyl-1,3-a-L-Gal-1,2-b-D-Xyl-1,2–5-O-FA-L-Ara; a-D-Gal-1,3-a-L-Gal-1,2-b-D-Xyl-1,2–5-O-FA-L-Ara; 5-O-CA-L-Ara

Ishii (1997), Allerdings et al. (2006), Saulnier et al. (1995), Saulnier and Thibault (1999), Quemener and Ralet (2004)

Sugarcane bagasse

5-O-FA-a-L-Ara-1,3-Xyl-1,4-D-Xyl; O-b-D-xyl-1,4-O-(2-O-Ace-5-O-FA)–L-Ara-1,3- Xyl-1,4-D-Xyl; b-D-Xyl-1,4-O-(5-FA-a-D-Ara-1,3)-O-D-Xyl-1,4-D-Xyl O-2-FA-a-L-Ara-1,5-Ara;6-FA-b-D-Gal-1,4-Gal; a-L-Ara-1,3-O-(2-FA–L-Ara)-1,5-Ara; O-(5-O-FA-a-L-Ara)-1.3-D-Xyl

Ishii (1997)

Spinach

O-2-FA–L-Ara-1,5-Ara;6-FA-b-D-Gal-1,4-Gal; -L-Ara-1,3-O-(2-FA–L-Ara)-1,5-Ara; O-(5-O-FA–L-Ara)-1.3-D-Xyl

Ishii (1997)

Barley straw

(5-O-FA–L-Ara)-1,3-Xyl-1,4-D-Xyl; (5-O-CA)–L-Ara-1,3-b-D-Xyl-1,4-D-Xyl

Ishii (1997)

Bamboo shoot

(5-O-FA–L-Ara-1,3)-Xyl-1,4-D-Xyl; b-D-Xyl-1,4-O-(5-FA–L-Ara-1,3)-O-D-Xyl-1,4-D-Xyl; (5-O-CA)–L-Ara-1,3-b-D-Xyl-1,4-D-Xyl; O-b-D-Xyl-1,4-O-(5-CA–L-Ara-1,3)-O-b-D-Xyl-1,4-D-Xyl; O-(2-O-Ace-5-O-FA–L-Ara-1,3)-O-b-D-Xyl-1,4-D-Xyl; O-4-FA–D-Xyl-1,6-Gluc; 4-O-FA–D-Xyl-1,6-Gluc

Ishii (1997)

Rice

4-b-D-Xyl-(-D-Ara-1,2)(5-O-FA–L-Ara-1,3)-b-D-Xyl; 4-b-D-Xyl-(5-O-FA–L-Ara-1,3)-b-D-Xyl

Rao and Muralikrishna (2007)

Cynodon dactylon

O-(5-O-CA-a-L-Ara)-1,3-O-b-D-Xyl-1,4-D-Xyl; O-(5-O-FA-a-L-Ara)-1,3-O-b-D-Xyl-1,4-D-Xyl

Hartley, Morrison, Himmelsbach, and Borneman (1990), Scheller and Ulvskov (2010)

Festuca

O-b-D-Xyl-1,2-(O-5-O-FA-L-Ara)-O-b-D-Xyl-1,3-b-D-Xyl-1,2-O-(5-O-FA-L-Ara); O-b-D-Xyl-1,3-b-D-Xyl-1,2-O-FA-L-Ara 5-O-FA-O-b-D-Xyl-1,2–L-Ara-1,3-O-b-D-Xyl-1,4-D-Xyl

Ishii (1997)

Sugarbeet pulp

Cynodom dactylon

hydroxyl group of glycoside resulted in the improved scavenging activity against 1,1-diphenyl-2-picrylhydrazyl (DPPH) radicals. The inhibitory effects on the oxidation of liposomes and emulsions were also enhanced. These findings suggested that ferulic acid glycoside esters were more efficient antioxidants than their free forms. Feruloylated oligosaccharides obtained from maize bran (Lin, Ou, & Wen, 2012; Ohta, Yamasaki, Egaehira, & Sanada, 1994; Shen et al., 2012), wheat bran or wheat flour (Katapodis et al., 2003; Zhang, Ou, & Zhang, 2005) and barley (Szwajgier, Pielecki, & Targon´ski, 2005) also exhibited higher antioxidant activity than ferulic acid. Feruloylated oligosaccharides obtained from different materials have diverse antioxidant activities. For example, ragi feruloylated oligosaccharides exhibited favourable antioxidant activity by scavenging 12% DPPH at a minimum threshold concentration of 10 lg/mL. In this study, all other oligosaccharide mixtures from wheat, rice and maize showed no antioxidant activity at concentrations below 100 lg/mL. The antioxidant activity of maize feruloylated oligosaccharides was relatively lower than that of ragi, rice and wheat (Veenashri & Muralikrishna, 2011). Similar results were also obtained with ferric reducing antioxidant power (FRAP) as-

Ishii (1997), Saulnier and Thibault (1999), Quemener and Ralet (2004)

Ishii (1997)

says. These findings suggested that the antioxidant activity of feruloylated oligosaccharides may be related to their structure and ferulic acid content. For example, Kylli et al. (2008) reported the effects of linking position of ferulic acid to glucose. In that study, 6-O feruloyl-glucoside exhibited the highest antioxidant activity, followed by free ferulic acid, 2-O-, and 3-O-feruloyl-glucosides. Cos et al. (2002) reported that phenolic species esterified to sugar residues may also affect the antioxidant activity. They found sinapic acid had higher efficiency than ferulic acid and p-coumaric acid, which was consistent with the findings of Veenashri and Muralikrishna (2011), who reported a large amount of sinapic acids present in ragi bran. Wang, Sun, Cao, Song, and Tian (2008) reported that at the concentration of 10–500 lmol/L, feruloylated oligosaccharides from wheat bran had no cytotoxic and genotoxic effects to normal human lymphocytes after exposure to hydrogen peroxide (H2O2). By contrast, almost all cells in the control group were highly damaged by the H2O2 treatment. Zhang et al. (2005) found that the feruloylated oligosaccharides from wheat bran were more effective than ferulic acid in protecting against DNA damage by H2O2. Similar protective effects against free radical-induced oxidative damage were also observed in in rats and human

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Fig. 1 – Structure of feruloylated arabinotetraose with ferulic acid esterified to two neighbouring arabinose residues identified from sugar beet cell walls.

Fig. 2 – The structure of dehydrotrimer and dehydrotetramers from maize bran.

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erythrocytes (Wang, Sun, Cao, & Tian, 2009a; Yuan, Wang, Yao, & Chen, 2005a). Feruloylated oligosaccharides extracted from maize bran, containing 4.5% of ferulic acid on the basis of dry matter, had protective effects against the injury induced by H2O2 in pheochromocytoma (PC12) cell (Shen et al., 2012). It was found that feruloylated oligosaccharides (800 lmol/L) significantly increased the cell viability as well as the superoxide dismutase activity, but decreased the release of lactate dehydrogenase and malondialdelyde. Ferulic dehydrodimers released from plant walls also possess antioxidant activity. According to Garcia-Conesa, Plumb, Waldron, Ralph, and Williamson (1997), the 8-O-4-diferulic acid prepared from wheat bran had higher antioxidant activity than free ferulic acid in both aqueous and lipid phases. The Trolox equivalent antioxidant capacity (TEAC) and IC50 values for the inhibition of lipid peroxidation by 8-O-4-diferulic acid were 2.9 and 15.0 lM, respectively, whereas those for ferulic acid were 1.96 and 26.6 lM. However, the antioxidant activity of diferuloylated oligosaccharides has rarely been reported.

3.2.

Inhibition against glycation

Non-enzymatic glycation, also known as the Maillard reaction, is a process in which reducing sugars react spontaneously with amino groups of proteins (Schalkwijk, Stehouwer, & van Hinsbergh, 2004). Glycation is a chain reaction and the final product is called advanced glycation endproduct (AGE). Once formed in living organisms, AGEs can generate crosslinks between key molecules or interact with their receptors, causing structural modifications and functional impairments of proteins (Vlassara & Palace, 2002). It is worthy of note that free radicals and oxidative steps play key roles in the formation of AGEs. Glycation and AGEs are widely recognised as important factors contributing to a number of human diseases, especially diabetes and its complications. In recent years, the exploration of anti-glycative agents has received much attention. Given the tight connection between glycation and oxidation, various strong antioxidants including feruloylated oligosaccharides have been evaluated. Wang, Sun, Cao, and Tian (2009b) found that in a bovine serum albumin (BSA)–glucose system, the protein glycation was suppressed by ferulic acid (0.25 mg/mL) and feruloylated oligosaccharides (1.0 mg/mL) from wheat bran. The amount of AGEs was markedly decreased. The observed effects may be related to radical scavenging and iron-chelating activities. In animal studies, ferulic acid showed protective and therapeutic effects against diabetic nephropathy through suppressing the oxidative stress (Choi et al., 2011), the elevated plasma lipids as well as blood glucose levels (Sri Balasubashini, Rukkumani, & Menon, 2003). Ou et al. (2007) investigated the effect of feruloylated oligosaccharides from wheat bran in alloxaninduced diabetic Sprague–Dawley rats. The intragastric administration of feruloylated oligosaccharides significantly increased the total antioxidant level as well as the activity of glutathione peroxidase and superoxide dismutase. Meanwhile, xanthine oxidase activity, blood glucose and malondialdehyde levels were decreased in diabetic rats. Feruloylated oligosaccharides were far more

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efficient in mitigating the oxidative damage in diabetic rats than sodium ferulate or vitamin C. As oligosaccharides may improve the altered blood glucose metabolism in diabetic rats through various mechanisms, e.g. through accelerated proliferation or neogenesis of b-cells and increased secretory capacity of insulin (Sreevidya et al., 2006; Thakur & Dixit, 2008), the mitigating effects of feruloylated oligosaccharides may not be solely derived from the esterified ferulic acid. A Sanger sequencing experiment showed that bacterial communities in stool samples from bio-breeding diabetes-prone and bio-breeding diabetes-resistant rats differed at the genus or species levels. This study also showed that the abundance of Lactobacillus and Bifidobacterium in the bio-breeding diabetes-resistant group was higher than that in the diabetes-prone group (Roesch et al., 2009). These findings suggested that feruloylated oligosaccharides may provide beneficial effects for diabetics through inducing probiotic effects in the colon. Trapping of reactive carbonyl species is another possible mechanism. Ferulic acid exhibited inhibitory effects on a number of a-dicarbonyl compounds which are highly reactive and acting as key intermediates in the AGE formation, such as glyoxal, methyglyoxal and 3-deoxyglucosone (Bousova´ et al., 2005; Silva´n, Assar, Srey, del Castillo, & Ames, 2011; Wu, Hsieh, Wang, & Chen, 2009).

3.3.

Probiotic effects

Non-digestible oligosaccharides can only be consumed by a limited number of bacteria such as probiotic bacteria, biofidobacteria and lactobacilli to stimulate their growth. Mussatto and Mancilha (2007) reviewed the physiological roles of non-digestible oligosaccharides. These oligosaccharides may inhibit diarrhoea through protecting the gastrointestinal, respiratory and urogenital tracts from infection. Also, they may increase the absorption of minerals and decrease cholesterol, triglyceride and phospholipid concentrations in the blood, leading to the reduced risks of diabetes, obesity and cancer (especially colon cancer). The physiological properties of cereal-derived oligosaccharides have been discussed previously (Broekaert et al., 2011). Moreover, Niewold, Schroyen, Geens, Verhelst, and Courtin (2012) found that feeding piglet with arabinoxylan oligosaccharides regulated immune responses by affecting the expression of particular innate response proteins. Feruloylated oligosaccharides play physiological roles similar to those of pure non-digestible oligosaccharides. Yuan, Wang, and Yao (2005b) first proved feruloyl oligosaccharides from wheat bran can stimulate the growth of Bifidobacterium bifidum. Muralikrishna, Schwarz, Dobleit, Fuhrmann, and Krueger (2011) compared the fermentation of xylooligosaccharides from birch wood and feruloylated xylooligosaccharides from wheat bran using mixed faecal cultures of human and cow. They found that feruloyl and non-feruloyl substrates were effectively used by faecal microorganisms. Furthermore, bovine faecal bacteria utilised both types of oligosaccharides more effectively than human faecal bacteria. However, as xylooligosaccharides from birch wood were more easily fermented than feruloyl xylooligosaccharides from

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wheat bran, cultures using xylooligosaccharides as a substrate produced more short-chain fatty acids than those using feruloylated oligosaccharides (11.55 vs. 9.65 lmol/mL after fermentation for 24 h). Oligosaccharides linked by ferulic acid are fermented more slowly than free oligosaccharides in the colon. Ferulic acid in the feruloylated oligosaccharides must first be released by the esterase produced by microorganisms in the colon before the microorganisms can use the free oligosaccharides as a carbon source. Wende, Buchanan, and Stephen (1997) described this successive process using isotope-labelled 2-O-b-D-xylopyranosyl (5-O-feruloyl)-L-arabinose prepared from spinach. Fang, Chen, Chen, Lin, and Fang (2012) reported that feruloylated oligosaccharides from rice bran can directly stimulate the immunological response of unstimulated macrophages. RAW264.7 cells were cultured in DMEM and incubated with different concentrations of feruloylated oligosaccharides at 37 °C for 24 h. The cell viability, cytokines and prostaglandin E2 (PGE2) were then determined. Results showed that after the treatment with 100 lg/mL of feruloylated oligosaccharides, the production of TNF-a, IL-1b, IL-6, nitric oxide and PGE2 increased by 18, 28.5, 18.5, 2.2 and 183 times, respectively.

4.

Preparation of feruloyated oligosaccharides

4.1. Preparation of feruloylated hydrolysis of plant cell walls

oligosaccharides

by

Feruloylated oligosaccharides can be obtained from the hydrolysis of plant cell walls by enzymes, acids and heat treatments. Several polysaccharide hydrolases can be used to release feruloylated oligosaccharides from plant cell walls (e.g. brans and straws). Theoretically, endo-b-1, 4-D-xylanases (EC 3.2.1.8, EXs) can randomly cleave the xylan backbone chain of arabinoxylan at non-substituted regions and consequently generate esterified xylo-oligosaccharides. However, as hemicelluloses are highly branched and bridged with cellulose or lignin, these complicated structures cause steric hindrance by preventing the formation of enzyme–substrate intermediates (Gottschalk, Oliveira, & da Silva Bon, 2010; Katapodis & Christakopoulos, 2008) and yield low levels of feruloylated oligosaccharides when subjected to single enzyme treatment. Yuan, Wang, and Yao (2006) used xylanases from Bacillus subtilis and the response surface methodology to produce feruloylated oligosaccharides from wheat bran. They found that under the optimal condition (42 °C and pH 5.2) for 35 h, only half of the bound ferulic acid in the bran was moved to feruloylated oligosaccharides. Mixtures of polysaccharide hydrolysing enzymes without esterase activity such as driselase (mixture of laminarinas, xylanas and cellulase), b-galactosidase, endo-b-1,4-xylanases (endoxylanases, EC 3.2.1.8) and endo-b-1,3–1,4-glucanase (endo-b-glucanases, EC 3.2.1.6) are often used to hydrolyse polysaccharides. Physical pre-treatments, e.g. sonication and autoclaving, have also been applied to increase the efficiency of enzymatic hydrolysis (Agger, Viksø-Nielsen, & Meyer, 2010; Fry, 1983; Gottschalk et al., 2010; Katapodis &

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Christakopoulos, 2008). Mild acid in combination with enzymatic hydrolysis has been employed to obtain feruloylated oligosaccharides (Sørensen, Pedersen, & Meyer, 2007). Fig. 3 shows the preparation procedure of wheat bran extract consisting of feruloylated oligosaccharides by Fugeia NV. The procedure includes four steps: (1), the wheat bran is suspended in water containing a-amylase to remove starch; (2), with a hemicellulase enzyme preparation consisting of endo-b-1,4-xylanases and endo-b-1,3–1,4-glucanase released by feruloylated oligosaccharides, the de-starched bran comprising water-unextractable hemicelluloses is separated from the soluble material, washed and re-suspended in water; (3), the feruloylated oligosaccharide-containing liquid is filtered and purified by ion exchange resin treatment; and (4) the purified liquid fraction is concentrated and spraydried. Products prepared by this process also contain soluble non-feruloylated oligosaccharides. Amberlite XAD-2, a polymeric adsorbent binding aromatic compound, is often employed to efficiently purify the target products. The separation process is as follows: the supernatant of the centrifugated enzymatic hydrolysis solution is loaded onto an Amberlite XAD-2 column and eluted with water (A1), 1:1 methanol–water (A2) and methanol (A3). Elution using A1 removes non-feruloylated oligosaccharides. Feruloylated oligosaccharides and free ferulic acid may be respectively collected from A2 and A3 elution fractions (Allerdings et al., 2006; Saulnier, Vigouroux, & Thibault, 1995). Native heteroxylan is insoluble in the cell wall and resistant to enzymatic hydrolysis. Even enzyme mixtures are unable to solubilise significant amounts of heteroxylan fragments (Saulnier et al., 1995). To solubilise feruloylated heteroxylan fragments, controlled mild acid hydrolysis has been extensively studied because ferulic acid is unstable

Fig. 3 – Preparation process for feruloylated oligosaccharides.

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and will be released when subjected to strong acid treatment (Verardo, Bonoli, Marconi, & Caboni, 2008). For example, trifluoroacetic acid (50 mM) is often used to hydrolyse feruloyl polysacchrides for structural characterisation (Allerdings et al., 2005, 2006; Li, Lai, Lu, Fang, & Chen, 2008; Saulnier et al., 1995). However, trifluoroacetic acid is not allowed to be used for food grade feruloylated oligosaccharides, at least in China. Oxalic acid was used to release feruloylated oligosaccharides from maize bran by autoclaving the bran in 0.6% oxalic acid solution (Huang & Ou, 2012). Microwave treatment is also helpful for the extraction. When the maize bran was treated with microwave irradiation at 180 or 200 °C, 50% of the original arabinoxylan content can be released as highly feruloylated arabinoxylo-oligosaccharides, containing 60% of the initial ferulic acid content (Rose & Inglett, 2010a). However, the microwaved hydrolysates may still contain large amounts of water-soluble polysaccharides, whose molecular weights may be over 10 KD, or even larger (58.2 KD) when the microwave was set at 210 °C (Benko et al., 2007). The degree of hydrolysis achieved depends on the raw material. In the case of wheat bran, the microwave treatment at 200 °C released 63.7% of the total oligosaccharides with molecular weights lower than 1338 (Rose & Inglett, 2010b). These studies suggest that microwave treatment might be a promising technique for the preparation of feruloylated oligosaccharides. As no chemical reagents remain in the hydrolysates after microwave treatment, enzymes can be directly used to further cleave the residual soluble feruloylated polysaccharides, and the yield of target products can be significantly increased.

lic acid as feruloyl donors. Couto, St-Louis, and Karboune (2011) optimised the esterification procedure of L-arabinobiose, L-galactobiose, L-xylobiose, flactose, sucrose, raffinose, fructooligosaccharide and xylooligosaccharide using multienzymatic preparation, such as Depol 740L from Humicola spp. The highest bioconversion yield (27%) was obtained from the reaction of galactose with ferulic acid in a buffer mixture containing n-hexane, 1,4-dioxane and 3-(N-morpholino) ethanesulphonic acid–NaOH. Enzymatic esterification of ferulic acid to oligosaccharides yields high contents of ferulic acid in feruloylated oligosaccharides. It is easier than other methods and offers a viable alternative to the poor selectivity of traditional chemical synthesis methods. However, without hydroxyl protection or suitable feruloyl donors, the selectivity of this method is not satisfactory. Feruloyl transferase is another enzyme used for feruloylation catalysis. Previous studies indicated that the feruloylation of polysaccharides can be catalysed by feruloyl transferase, including the feruloylation of cell wall sugar residues, amines or hydroxyl-fatty acids (de O. Buanafina et al., 2009). In addition, feruloyl transferase may also be used to synthesise feruloylated oligosaccharides. Yoshida-Shimokawa, Yoshida, Kakegawa, and Ishii (2001) successfully obtained a feruloylated trisaccharide, 5-O-feruloyl-a-L-arabinose-b-D-xylose-(1,4)-D-xylose, using feruloyl-CoA:arabinoxylan-trisaccharide O-hydroxylcinnamoyl transferase. The enzyme was prepared from suspension-cultured cells rice.

5.

Absorption and metabolism

4.2.

5.1.

Absorption and metabolism of free ferulic acid

Enzymatic synthesis

In addition to the hydrolysis of plant cell walls, feruloylated oligosaccharides may also be obtained from enzymatic synthesis. There are two well-studied enzymes, namely ferulic acid esterase and feruloyl transferase. Ferulic acid esterase (FAE, EC 3.1.1.73) is a subclass of carboxylic acid esterases. It catalyses the cleavage of ester bonds between hydroxycinnamic acids and glycosides in plant cell walls (Topakas, Vafiadi, & Christakopoulos, 2007; Wong, 2006). Similar to lipase, it shows reversible catalytic activity and can catalyse the esterification of ferulic acid (Topakas et al., 2007). In contrast to the hydrolytic process, esterification must take place in an organic solvent/water medium. A number of studies have investigated the esterification of ferulic acid with sugars. For example, Topakas, Vafiadi, Stamatis, and Christakopoulos (2005) first reported that ferulic acid esterase type C from Sporotrichum thermophile (StFaeC) can catalyse the transfer of feruloyl group to Larabinose and L-arabinobiose. Vafiadi, Topakasm, and Christakopoulos (2006) successfully obtained O-[5-O-(trans-feruloyl)-a-L-arabinofuranosyl]-(1!5)-L-arabinofuranose from S. thermophile using alkyl ferulates as feruloyl donors. Mastihubova, Mastihuba, Bilanicova, and Borekova (2006) prepared various feruloyl glycosides with ferulic acid linked at the primary position by employing different alkyl glycosides and active vinyl or 2, 2, 2-trifluoroethyl esters of feru-

The absorption and pharmacokinetic properties of ferulic acid have been reviewed previously (Zhao & Moghadasian, 2008). Ferulic acid can be absorbed by the stomach, jejunum, ileum and colon. Most of the consumed ferulic acid is absorbed in the upper gastrointestinal tract and only 0.5–0.8% was found in the faeces of rats (Zhao & Moghadasian, 2008, 2010). The absorption of ferulic acid occurs rapidly. After intake, ferulic acid was detected in plasma within 5 min (in rats) or 10 min (in human), and reached the maximum value in 30 min (Yang, Tian, Zhang, Xu, & Chen, 2007; Zhao & Moghadasian, 2008). Ferulic acid is absorbed mainly in the free form together with a small percentage of its conjugated and reduced forms (Yang et al., 2007). After absorption, ferulic acid is processed into numerous metabolites, including glucuronide, sulphate, diglucuronide, sulphoglucuronide (conjugate with sulphate and glucuronide), m-hydroxyphenylpropionic acid, feruloylglycine, dihydroferulic acid, vanillic acid and vanilloylglycine in the plasma and urine of rats. Glucuronide, sulphate and sulphoglucuronide are the major metabolites (Rondini, Peyrat-Maillard, Marsset-Baglieri, & Berset, 2002; Zhao & Moghadasian, 2008). The conjugated metabolites are formed immediately after absorption. Glucuronides and sulphates of ferulic acid were detected in the plasma of rats within 10 min and peaked within 30 min after intake of 5.15 mg/kg.bw of free ferulic

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acid. The consumed ferulic acid was excreted in the urine within 1.5 h (Rondini et al., 2002). After oral administration of relatively low (70 lmol/kg.bw) and high (462 lmol/kg.bw) doses of ferulic acid in rats, 2.9% and 14.3% of free ferulic acid were detected in urine samples, respectively (Zhao & Moghadasian, 2008), suggesting that most of the consumed ferulic acid may be transformed into its conjugates after absorption.

5.2.

Absorption and metabolism of bound ferulic acid

Ferulic acid mainly exists in the bound form with polysaccharides and oligosaccharides, so that they cannot be directly absorbed by gastrointestinal tract. The esterase activity is necessary to cleave ester bonds and release ferulic acid for absorption and further metabolism (Ou & Kwok, 2004). Both small and large intestines have esterase activity (Andreasen, Kroon, Williamson, & Garcia-Conesa, 2001). In rats, esterase activity accounted for 50–95% of total activity in the large intestine but only 5–10% of that in the small intestine. Similarly, the esterase activity detected in faecal cell-free extracts from healthy human volunteers was about 10-fold higher than that in small intestine samples (Andreasen et al., 2001). These results indicated that large intestine may be the main site for the release of ferulic acid. Among over 1000 species of microorganisms in the colon, the probiotic genera Bifidibacterium and Lactobacillus are known as the best ferulic esterase producers (Couteau, Gibson, Williamson, & Faulds, 2001; Lai, Lorca, & Gonzalez, 2009; Szwajgier & Dmowska, 2010). Ferulic esterases exhibit different activities for releasing ferulic acid from different substrates. Water-insoluble dietary fibres are much less accessible to digestion or fermentation in the digestive tract than water-soluble ones and release much less ferulic acid after fermentation in the colon. In a project conducted by Karppinen, Liukkonen, Aura, Forssell, and Poutanen (2000), it was found that 39% of wheat bran and 42% of rye bran were degraded by fermentation using fresh faeces from healthy human volunteers for 24 h, and only 25 and 18% of bound ferulic acid were released. Another study found that 100 and 64% of bound ferulic acid were released by micro-biota after solubilisation of brans by enzymatic digestion using a Trichoderma viride xylanase (Novozym 431 L, Novo Nordisk A/S) (Andreasen et al., 2001). The ferulic acid in feruloylated oligosaccharides is released more easily and much faster than that in feruloylated polysaccharides (both soluble and insoluble). Wende et al. (1997) found that after the incubation of feruloyl-U-14C-labelled feruloylated oligosaccharide and 2-O-b-D-xylopyranosyl-(5-O-feruloyl)-L-arabinose, ferulic acid was completely released from rat faecal contents in 16 min with a half-life of 0.2 min. Previous studies indicated that the release of ferulic acid was efficiently transported in its free form with only a small amount of feruloyl-glucuronide or sulphate through the colonic epithelium (Poquet, Clifford, & Williamson, 2008). The peak concentration of ferulic acid in human plasma appeared between 1 and 3 h after high-bran cereal administration (Kern, Bennett, Mellon, Kroon, & Garcia-Conesa, 2003). The

x x x ( 2 0 1 4 ) x x x –x x x

consumption of bound ferulic acid from the food matrix increases with the continuous release of ferulic acid in the colon, making bound ferulic acid from bran more bioavailable than the free ferulic acid (Rondini et al., 2004). DFAs could also be released by ferulic esterase. Kroon et al. (1999) released DFAs from oligosaccharide diesters of ferulic acid solubilised from wheat bran and sugar beet pulp using purified feruloyl esterases. Feruloylated esterases from Aspergillus niger and Pseudomonas y´uorescens can release 93 and 36% of total 5,5-diferulic acid from solubilised wheat bran whilst 12 and 15% of the same acid from solubilised sugar beet pulp. Diferulic acids can be absorbed by the small intestine. After oral administration of a mixture of 5,5-, 8-O-4- and 8,5-diferulic acid along with sunflower oil, 0.3–2.5 lM of diferulic acid was detected in rat plasma (Andreasen et al., 2001). The authors therefore supposed that diferulates released by intestinal enzymes may be absorbed and enter the circulatory system. However, Kern et al. (2003) did not detect diferulic acid in human plasma after cereal bran intake, suggesting that diferulic acid may not be easily absorbed by the colon. In addition to absorption, ferulic acid could also be metabolised by microorganisms in the colon through reduction, demethylation and dehydroxylation at C-4 position to yield products of m-hydroxyphenylpropionic acid, hydroxyphenylpropionic acid and phenylpropionic acid, respectively (Zhao & Moghadasian, 2008).

6.

Conclusions and outlook

Feruloylated oligosaccharides are water-soluble and thermally stable. They contain hydrophobic ferulic acid moieties and hydrophilic oligosaccharide moieties, and therefore possess the nutritional and physiological functions of both of them. As excellent functional ingredients, feruloylated oligosaccharides provide great potential health benefits, having a wide range of applications in food and pharmaceutical industries. The fermentation properties of feruloylated oligosaccharides as well as their high contents of ferulic acid present many new directions for future investigation: (1) the impact on micro-ecology and health of the colon. It is important to investigate whether the ferulic acid released from feruloylated oligosaccharides exhibits antimicrobial activity in the colon. Moreover, as phenolic compounds have been proved to potentially influence colonic cellular regulation, further studies are necessary to determine the effect of released ferulic acid, including FDAs, on colon health; (2) health effects of absorbed ferulic acid. The bound ferulic acid may be absorbed by the colonic epithelium, maintaining high concentrations in the plasma after long-term intake. Whether this is beneficial to human health remains unexplored; (3) in addition to ferulic acid, studies remain limited on di-, tri- and tetramers of ferulic acid. Their metabolic pathway and toxicology should also be explored to determine whether they can be used as safe food additives and nutritional ingredients; and (4) effects of p-coumaroylated oligosaccharides. p-Coumaric acid is not approved as a food ingredient in some countries such as China. It is necessary to evaluate whether p-

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coumaroylated oligosaccharides existing along with feruloylated oligosaccharides can be fully released by ferulic acid esterase in the colon. Their absorption, metabolism, toxicology and health effects should also be investigated.

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Please cite this article in press as: Ou, J., & Sun, Z., Feruloylated oligosaccharides: Structure, metabolism and function, Journal of Functional Foods (2014), http://dx.doi.org/10.1016/j.jff.2013.09.028