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      Glucosinolate metabolism, functionality and breeding for the improvement of Brassicaceae vegetables

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          Abstract

          Unique secondary metabolites, glucosinolates ( S-glucopyranosyl thiohydroximates), are naturally occurring S-linked glucosides found mainly in Brassicaceae plants. They are enzymatically hydrolyzed to produce sulfate ions, D-glucose, and characteristic degradation products such as isothiocyanates. The functions of glucosinolates in the plants remain unclear, but isothiocyanates possessing a pungent or irritating taste and odor might be associated with plant defense from microbes. Isothiocyanates have been studied extensively in experimental in vitro and in vivo carcinogenesis models for their cancer chemopreventive properties. The beneficial isothiocyanates, glucosinolates that are functional for supporting human health, have received attention from many scientists studying plant breeding, plant physiology, plant genetics, and food functionality. This review presents a summary of recent topics related with glucosinolates in the Brassica family, along with a summary of the chemicals, metabolism, and genes of glucosinolates in Brassicaceae. The bioavailabilities of isothiocyanates from certain functional glucosinolates and the importance of breeding will be described with emphasis on glucosinolates.

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          Most cited references54

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          The chemical diversity and distribution of glucosinolates and isothiocyanates among plants.

          Glucosinolates (beta-thioglucoside-N-hydroxysulfates), the precursors of isothiocyanates, are present in sixteen families of dicotyledonous angiosperms including a large number of edible species. At least 120 different glucosinolates have been identified in these plants, although closely related taxonomic groups typically contain only a small number of such compounds. Glucosinolates and/or their breakdown products have long been known for their fungicidal, bacteriocidal, nematocidal and allelopathic properties and have recently attracted intense research interest because of their cancer chemoprotective attributes. Numerous reviews have addressed the occurrence of glucosinolates in vegetables, primarily the family Brassicaceae (syn. Cruciferae; including Brassica spp and Raphanus spp). The major focus of much previous research has been on the negative aspects of these compounds because of the prevalence of certain "antinutritional" or goitrogenic glucosinolates in the protein-rich defatted meal from widely grown oilseed crops and in some domesticated vegetable crops. There is, however, an opposite and positive side of this picture represented by the therapeutic and prophylactic properties of other "nutritional" or "functional" glucosinolates. This review addresses the complex array of these biologically active and chemically diverse compounds many of which have been identified during the past three decades in other families. In addition to the Brassica vegetables, these glucosinolates have been found in hundreds of species, many of which are edible or could provide substantial quantities of glucosinolates for isolation, for biological evaluation, and potential application as chemoprotective or other dietary or pharmacological agents.
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            A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure.

            Consumption of vegetables, especially crucifers, reduces the risk of developing cancer. Although the mechanisms of this protection are unclear, feeding of vegetables induces enzymes of xenobiotic metabolism and thereby accelerates the metabolic disposal of xenobiotics. Induction of phase II detoxication enzymes, such as quinone reductase [NAD(P)H:(quinone-acceptor) oxidoreductase, EC 1.6.99.2] and glutathione S-transferases (EC 2.5.1.18) in rodent tissues affords protection against carcinogens and other toxic electrophiles. To determine whether enzyme induction is responsible for the protective properties of vegetables in humans requires isolation of enzyme inducers from these sources. By monitoring quinone reductase induction in cultured murine hepatoma cells as the biological assay, we have isolated and identified (-)-1-isothiocyanato-(4R)-(methylsulfinyl)butane [CH3-SO-(CH2)4-NCS, sulforaphane] as a major and very potent phase II enzyme inducer in SAGA broccoli (Brassica oleracea italica). Sulforaphane is a monofunctional inducer, like other anticarcinogenic isothiocyanates, and induces phase II enzymes selectively without the induction of aryl hydrocarbon receptor-dependent cytochromes P-450 (phase I enzymes). To elucidate the structural features responsible for the high inducer potency of sulforaphane, we synthesized racemic sulforaphane and analogues differing in the oxidation state of sulfur and the number of methylene groups: CH3-SOm-(CH2)n-NCS, where m = 0, 1, or 2 and n = 3, 4, or 5, and measured their inducer potencies in murine hepatoma cells. Sulforaphane is the most potent inducer, and the presence of oxygen on sulfur enhances potency. Sulforaphane and its sulfide and sulfone analogues induced both quinone reductase and glutathione transferase activities in several mouse tissues. The induction of detoxication enzymes by sulforaphane may be a significant component of the anticarcinogenic action of broccoli.
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              Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells.

              Sulforaphane is an isothiocyanate that is present naturally in widely consumed vegetables and has a particularly high concentration in broccoli. This compound has been shown to block the formation of tumors initiated by chemicals in the rat. Although sulforaphane has been proposed to modulate the metabolism of carcinogens, its mechanism of action remains poorly understood. We have previously demonstrated that sulforaphane inhibits the reinitiation of growth and decreases the cellular viability of quiescent human colon carcinoma cells (HT29). Moreover, the weak effect observed on differentiated CaCo2 cells suggests a specific anticancer activity for this compound. Here we investigated the effect of sulforaphane on the growth and viability of HT29 cells during their exponentially growing phase. We observed that sulforaphane induced a cell cycle arrest in a dose-dependent manner, followed by cell death. This sulforaphane-induced cell cycle arrest was correlated with an increased expression of cyclins A and B1. Moreover, we clearly demonstrated that sulforaphane induced cell death via an apoptotic process. Indeed, a large proportion of treated cells display the following: (a) translocation of phosphatidylserine from the inner layer to the outer layer of the plasma membrane; (b) typical chromatin condensation; and (c) ultrastructural modifications related to apoptotic cell death. We also showed that the expression of p53 was not changed in sulforaphane-treated cells. In contrast, whereas bcl-2 was not detected, we observed increased expression of the proapoptotic protein bax, the release of cytochrome c from the mitochondria to the cytosol, and the proteolytic cleavage of poly(ADP-ribose) polymerase. In conclusion, our results strongly suggest that in addition to the activation of detoxifying enzymes, induction of apoptosis is also involved in the sulforaphane-associated chemoprevention of cancer.
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                Author and article information

                Journal
                Breed Sci
                Breed. Sci
                Breeding Science
                Japanese Society of Breeding
                1344-7610
                1347-3735
                May 2014
                May 2014
                : 64
                : 1
                : 48-59
                Affiliations
                [1 ]NARO Institute of Vegetable and Tea Science, Tsukuba Vegetable Research Station , 3-1-1 Kannondai, Tsukuba, Ibaraki 305-8666, Japan
                [2 ]Research Institute of Green Science and Technology, Shizuoka University , 836 Ohya, Shizuoka 422-8529, Japan
                [3 ]NARO Institute of Vegetable and Tea Science , 360 Kusawa, Ano, Tsu, Mie 514-2392, Japan
                [4 ]The Department of Food and Nutritional Sciences, The Graduate School of Humanities and Sciences, Ochanomizu University , 2-1-1 Otsuka, Bunkyo, Tokyo 112-8610, Japan
                Author notes
                [* ]Corresponding author (e-mail: ishimame@ 123456affrc.go.jp )

                Communicated by T. Nishio

                Article
                64_48
                10.1270/jsbbs.64.48
                4031110
                24987290
                b9630472-09c9-428e-81a3-df9ac1b08fcc
                Copyright © 2014 by JAPANESE SOCIETY OF BREEDING

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 20 September 2013
                : 24 February 2014
                Categories
                Review

                Animal agriculture
                glucosinolate,isothiocyanate,biosynthesis,gene,health,brassica,plant breeding
                Animal agriculture
                glucosinolate, isothiocyanate, biosynthesis, gene, health, brassica, plant breeding

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