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Bioavailability of Glucosinolates and Their Breakdown Products Bioavailability of glucosinolates and their breakdown products impact of processing Barba Orellana, Francisco Jose; Nikmaram, Nooshin; Roohinejad, Shahin; Khelfa, Anissa; Zhu, Zhenzhou; Koubaa, Mohamed Published in: Frontiers in Nutrition DOI: 10.3389/fnut.2016.00024 Publication date: 2016 Document version Publisher's PDF, also known as Version of record Citation for published version (APA): Barba Orellana, F. J., Nikmaram, N., Roohinejad, S., Khelfa, A., Zhu, Z., & Koubaa, M. (2016). Bioavailability of glucosinolates and their breakdown products: impact of processing. Frontiers in Nutrition, 3, [24]. https://doi.org/10.3389/fnut.2016.00024 Download date: 30. sep.. 2021 REVIEW published: 16 August 2016 doi: 10.3389/fnut.2016.00024 Bioavailability of Glucosinolates and Their Breakdown Products: Impact of Processing Francisco J. Barba1,2*, Nooshin Nikmaram3, Shahin Roohinejad4, Anissa Khelfa5, Zhenzhou Zhu6 and Mohamed Koubaa5 1 Department of Food Science, Faculty of Science, University of Copenhagen, Copenhagen, Denmark, 2 Nutrition and Food Science Area, Faculty of Pharmacy, Universitat de València, València, Spain, 3 Department of Food Science and Technology, Faculty of Agricultural Engineering, Islamic Azad University of Sabzevar, Sabzevar, Iran, 4Burn and Wound Healing Research Center, Division of Food and Nutrition, Shiraz University of Medical Sciences, Shiraz, Iran, 5 Sorbonne Universités, Université de Technologie de Compiègne, Laboratoire Transformations Intégrées de la Matière Renouvelable (UTC/ESCOM, EA 4297 TIMR), Centre de Recherche de Royallieu, Compiègne Cedex, France, 6 School of Food Science and Engineering, Wuhan Polytechnic University, Wuhan, China Glucosinolates are a large group of plant secondary metabolites with nutritional effects, and are mainly found in cruciferous plants. After ingestion, glucosinolates could be partially absorbed in their intact form through the gastrointestinal mucosa. However, the largest fraction is metabolized in the gut lumen. When cruciferous are consumed without Edited by: processing, myrosinase enzyme present in these plants hydrolyzes the glucosinolates António Manuel Peres, in the proximal part of the gastrointestinal tract to various metabolites, such as iso- Polytechnic Institute of Bragança, Portugal thiocyanates, nitriles, oxazolidine-2-thiones, and indole-3-carbinols. When cruciferous Reviewed by: are cooked before consumption, myrosinase is inactivated and glucosinolates transit Ligia R. Rodrigues, to the colon where they are hydrolyzed by the intestinal microbiota. Numerous factors, University of Minho, Portugal Ester Betoret, such as storage time, temperature, and atmosphere packaging, along with inactivation Università di Bologna, Italy processes of myrosinase are influencing the bioavailability of glucosinolates and their *Correspondence: breakdown products. This review paper summarizes the assimilation, absorption, and Francisco J. Barba elimination of these molecules, as well as the impact of processing on their bioavailability. [email protected], [email protected] Keywords: glucosinolates, isothiocyanates, bioavailability, brassicaceae, myrosinase, processing Specialty section: This article was submitted to Nutrition and Food Science Technology, INTRODUCTION a section of the journal Frontiers in Nutrition Glucosinolates are secondary metabolites synthesized by plants. They contain sulfur groups and Received: 03 June 2016 are present in numerous species belonging to Brassicaceae family (1). Chemically, glucosinolates Accepted: 21 July 2016 are composed of thiohydroximate-O-sulfonate group linked to glucose, and an alkyl, aralkyl, or Published: 16 August 2016 indolyl side chain (R) (2) (Figure 1). More than 200 side-groups have been identified and cited in Citation: the literature (2–4). Barba FJ, Nikmaram N, Glucosinolates are relatively stable in plant cell. However, when the plant tissue containing Roohinejad S, Khelfa A, Zhu Z and glucosinolates is damaged, as is the case in the preparation (cutting, chopping, mixing) or chewing Koubaa M (2016) Bioavailability of food, a β-thioglucosidase called myrosinase is released. The enzyme is normally stored separately Glucosinolates and Their Breakdown Products: Impact of Processing. Front. Nutr. 3:24. Abbreviations: ESP, epithiospecifier protein; ITCs, isothiocyanates; MAP: modified atmosphere packaging; NAC, doi: 10.3389/fnut.2016.00024 N-acetyl-l-cysteine. Frontiers in Nutrition | www.frontiersin.org 1 August 2016 | Volume 3 | Article 24 Barba et al. Impact of Processing on Glucosinolates FIGURE 1 | Enzymatic hydrolysis reaction of glucosinolates and their breakdown products. Adapted from Ref. (5). ESP, epithiospecifier protein; molecules between brackets indicate instable intermediate. from glucosinolates in different cells, or in different intracellular previous studies also reported their action as inhibitors of mitosis compartments, depending on the plant species (6). The hydroly- and stimulator of the apoptosis in human tumor cells (13–15). sis of glucosinolate by myrosinase produces a molecule of β-d- ITCs revealed also fungicidal, fungistatic, nematicidal, and glucose and an unstable aglycone; thiohydroximate-O-sulfonate bactericidal activities (16–18). Table 1 shows some biological (Figure 1). Spontaneous reorganization of this intermediate activities of selected glucosinolate breakdown products. Due to (chemical rearrangement of Lossen) results in the release of the biological properties associated with glucosinolates and their sulfate ion and in the formation of metabolites, the structures of breakdown products, especially ITCs, understanding, on the one which depend on the nature of the side chain (R) of glucosinolate, hand, the absorption routes of these molecules and their metabo- and the physico-chemical conditions of the medium (Figure 1). lism and, on the other hand, the impact of processing parameters The formation of nitriles is favored by acidic pH and the presence on their presence in food products is of great importance. This in the environment of ferrous ions (Fe2+), and a particular plant review is, thus, dealing to summarize both aspects. protein called epithiospecifier protein (ESP) (7). In addition, the existence of terminal unsaturation in the side chain of the glucosinolate molecule leads to a distinct form of nitriles called BIOAVAILABILITY OF GLUCOSINOLATES epithionitriles. A neutral pH favors the formation of isothiocy- AND THEIR BREAKDOWN PRODUCTS anates (ITCs) (8). If the side chain has a β-hydroxyl function, ITCs cyclize spontaneously into oxazolidin-2-thione (1, 9, 10). Digestion in the Human Digestive Tract Similarly, ITCs deriving from the hydrolysis of glucosinolates are Bioaccessibility represents the amount or fraction that is released unstable and they easily split into thiocyanate ion and indole- in the digestive tract, from a food product, and is becoming avail- 3-carbinol (Figure 1). able for absorption (90). The digestive transformations of the food Isothiocyanates are highly reactive and present potent in vivo material until assimilation and its enterocytic metabolism are action as inducers of Phase II enzymes (11, 12). Numerous also included in this definition. Bioavailability, on the other hand, Frontiers in Nutrition | www.frontiersin.org 2 August 2016 | Volume 3 | Article 24 Barba et al. Impact of Processing on Glucosinolates TABLE 1 | Some biological activities of selected glucosinolate breakdown instance, intact glucosinolates could be partially absorbed in the products. stomach, the remaining glucosinolates will transit through the Biological Glucosinolate breakdown products Reference gastrointestinal tract to reach the small intestine where they could activities be hydrolyzed by plant myrosinase, and the breakdown products Fungicidal Allyl-ITC (19–24) could be absorbed. The remaining non-hydrolyzed glucosinolates effects Alkenyl aliphatic ITCs (methyl-ITC, propenyl- (22, 25) will then transit to reach the colon where they could be hydro- ITC, butenyl-ITC, pentenyl-ITC) (propenyl-ITC, lyzed with bacterial myrosinase, and the generated breakdown ethyl-ITC) molecules are absorbed or/and excreted. Benzyl-ITC (21, 25–28) It has been shown that the incubation of human feces in Butenyl-ITC (19, 23) Glucoerucin-derived ITC (29) presence of pure glucosinolates or cruciferous vegetable juices, in Glucoiberin-derived ITC (28) which myrosinase was inactivated by heating, leads to the forma- 3-Indolylacetonitrile (30) tion of ITCs (94, 98). These metabolites are also formed in the 3-Methylsulfinylpropyl ITC (28) germ-free colon of rats, following the colonization with human Propenyl-ITC (19, 31–34) intestinal bacteria, and feeding with a pure glucosinolate (99). Phenylethyl-ITC (25, 35, 36) In humans, urinary excretion of conjugated metabolites of ITCs Sinalbin (p-Hydroxybenzylglucosinolate) (37) derived-ITC was observed following the consumption of cruciferous cooked Sinigrin (prop-2-enylglucosinolate)-derived ITC (38) vegetables (94, 95, 97). 5-Vinyloxazolidine-2-thione (39) The formation of other breakdown products from glucosi- Bactericidal Allyl-ITC (40–45) nolates by intestinal microbiota is very likely, but still poorly effects Benzyl-ITC (45) documented. The formation of amines from the secondary 2-Phenylethyl-ITC (45) degradation of ITCs has been demonstrated after the incuba- 4-hydroxybenzyl-ITC (46, 47) tion of human feces with glucosinolates (100). Bifidobacterium Methyl-ITC (42) strains belonging to the human intestinal microbiota are able
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