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Zingiber Officinale Roscoe foods Review Bioactive Compounds and Bioactivities of Ginger (Zingiber officinale Roscoe) Qian-Qian Mao 1, Xiao-Yu Xu 1, Shi-Yu Cao 1, Ren-You Gan 2,* , Harold Corke 2, Trust Beta 3,4 and Hua-Bin Li 1,* 1 Guangdong Provincial Key Laboratory of Food, Nutrition and Health, Department of Nutrition, School of Public Health, Sun Yat-sen University, Guangzhou 510080, China; [email protected] (Q.-Q.M.); [email protected] (X.-Y.X.); [email protected] (S.-Y.C.) 2 Department of Food Science & Technology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China; [email protected] 3 Department of Food & Human Nutritional Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada; [email protected] 4 Richardson Centre for Functional Foods and Nutraceuticals, University of Manitoba, Winnipeg, MB R3T 2N2, Canada * Correspondence: [email protected] (R.-Y.G.); [email protected] (H.-B.L.); Tel.: +86-21-3420-8517 (R.-Y.G.); +86-20-873-323-91 (H.-B.L.) Received: 12 May 2019; Accepted: 28 May 2019; Published: 30 May 2019 Abstract: Ginger (Zingiber officinale Roscoe) is a common and widely used spice. It is rich in various chemical constituents, including phenolic compounds, terpenes, polysaccharides, lipids, organic acids, and raw fibers. The health benefits of ginger are mainly attributed to its phenolic compounds, such as gingerols and shogaols. Accumulated investigations have demonstrated that ginger possesses multiple biological activities, including antioxidant, anti-inflammatory, antimicrobial, anticancer, neuroprotective, cardiovascular protective, respiratory protective, antiobesity, antidiabetic, antinausea, and antiemetic activities. In this review, we summarize current knowledge about the bioactive compounds and bioactivities of ginger, and the mechanisms of action are also discussed. We hope that this updated review paper will attract more attention to ginger and its further applications, including its potential to be developed into functional foods or nutraceuticals for the prevention and management of chronic diseases. Keywords: phytochemicals; antioxidant; antinausea; antiobesity; anticancer; anti-inflammatory 1. Introduction Ginger (Zingiber officinale Roscoe), which belongs to the Zingiberaceae family and the Zingiber genus, has been commonly consumed as a spice and an herbal medicine for a long time [1]. Ginger root is used to attenuate and treat several common diseases, such as headaches, colds, nausea, and emesis. Many bioactive compounds in ginger have been identified, such as phenolic and terpene compounds. The phenolic compounds are mainly gingerols, shogaols, and paradols, which account for the various bioactivities of ginger [2]. In recent years, ginger has been found to possess biological activities, such as antioxidant [3], anti-inflammatory [4], antimicrobial [5], and anticancer [6] activities. In addition, accumulating studies have demonstrated that ginger possesses the potential to prevent and manage several diseases, such as neurodegenerative diseases [7], cardiovascular diseases [8], obesity [9], diabetes mellitus [10], chemotherapy-induced nausea and emesis [11], and respiratory disorders [12]. In this review, we focus on the bioactive compounds and bioactivities of ginger, and we pay special attention to its mechanisms of action. Foods 2019, 8, 185; doi:10.3390/foods8060185 www.mdpi.com/journal/foods Foods 2019, 8, 185 2 of 21 2. Bioactive Components and Bioactivities of Ginger 2.1. Bioactive Components Ginger is abundant in active constituents, such as phenolic and terpene compounds [13]. The phenolic compounds in ginger are mainly gingerols, shogaols, and paradols. In fresh ginger, gingerols are the major polyphenols, such as 6-gingerol, 8-gingerol, and 10-gingerol. With heat treatment or long-time storage, gingerols can be transformed into corresponding shogaols. After hydrogenation, shogaols can be transformed into paradols [2]. There are also many other phenolic compounds in ginger, such as quercetin, zingerone, gingerenone-A, and 6-dehydrogingerdione [14,15]. Moreover, there are several terpene components in ginger, such as β-bisabolene, α-curcumene, zingiberene, α-farnesene, and β-sesquiphellandrene, which are considered to be the main constituents of ginger essential oils [16]. Besides these, polysaccharides, lipids, organic acids, and raw fibers are also present in ginger [13,16]. 2.2. Antioxidant Activity It has been known that overproduction of free radicals, such as reactive oxygen species (ROS), plays an important part in the development of many chronic diseases [17]. It has been reported that a variety of natural products possess antioxidant potential, such as vegetables, fruits, edible flowers, cereal grains, medicinal plants, and herbal infusions [18–24]. Several studies have found that ginger also has high antioxidant activity [14,25]. The antioxidant activity of ginger has been evaluated in vitro via ferric-reducing antioxidant power (FRAP), 2,2-diphenyl-1-picrylhydrazyl (DPPH), and 2,20-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) methods. The results revealed that dried ginger exhibited the strongest antioxidant activity, because the number of phenolic compounds was 5.2-, 1.1-, and 2.4-fold higher than that of fresh, stir-fried, and carbonized ginger, respectively. The antioxidant activity of different gingers had a tendency to be the following: dried ginger > stir-fried ginger > carbonized ginger > fresh ginger. This was mainly associated with their polyphenolic contents. When fresh ginger was heated, dried ginger with higher antioxidant activity was obtained, because fresh ginger contains a higher moisture content. However, when dried ginger was further heated to obtain stir-fried ginger and carbonized ginger, the antioxidant activity decreased, because the processing could change gingerols into shogaols [26]. Additionally, a fraction of the dried ginger powder abundant in polyphenols showed high antioxidant activity based on data from FRAP, oxygen radical absorbance capacity, and cellular antioxidant activity assays [27]. Besides, the type of extraction solvent could have an effect on the antioxidant activity of ginger. An ethanolic extract of ginger showed high Trolox-equivalent antioxidant capacity and ferric-reducing ability, and an aqueous extract of ginger exhibited strong free radical scavenging activity and chelating ability [16]. Moreover, ethanolic, methanolic, ethyl acetate, hexane, and water extracts of ginger respectively inhibited 71%, 76%, 67%, 67%, and 43% of human low-density lipoprotein (LDL) oxidation induced by Cu2+ [28]. Results from a xanthine/xanthine oxidase system showed that an ethyl acetate extract and an aqueous extract had higher antioxidant properties than ethanol, diethyl ether, and n-butanol extracts did [3]. Several studies have indicated that ginger was effective for protection against oxidative stress. The underlying mechanisms of antioxidant action were investigated in cell models [14,29]. Ginger extract showed antioxidant effects in human chondrocyte cells, with oxidative stress mediated by interleukin-1β (IL-1β). It stimulated the expression of several antioxidant enzymes and reduced the generation of ROS and lipid peroxidation [30]. Additionally, ginger extract could reduce the production of ROS in human fibrosarcoma cells with H2O2-induced oxidative stress [31]. In stressed rat heart homogenates, ginger extract decreased the content of malondialdehyde (MDA), which was related to lipid peroxidation [29]. Ginger and its bioactive compounds (such as 6-shogaol) exhibited antioxidant activity via the nuclear factor erythroid 2-related factor 2 (Nrf2) signaling pathway (Figure1)[ 32]. In human colon cancer cells, 6-shogaol increased intracellular glutathione/glutathione Foods 2019, 8, 185 3 of 21 disulfide (GSH/GSSG) and upregulated Nrf2 target gene expression, such as with heme oxygenase-1 Foods 2019, 8, x FOR PEER REVIEW 3 of 21 (HO-1), metallothionein 1 (MT1), aldo-keto reductase family 1 member B10 (AKR1B10), ferritin light chainchain ( (FTLFTL),), and and γ-glutamyltransferase-like activityactivity 4 4 ( GGTLA4(GGTLA4).). Besides, Besides, 6-shogaol 6-shogaol also also enhanced enhanced the theexpression expression of genesof genes involved involved in glutathione in glutathione synthesis, synthesis, such assuch the glutamate-cysteineas the glutamate-cysteine ligase catalytic ligase catalyticsubunit (subunitGCLC) and (GCLC the glutamate-cysteine) and the glutamate-cysteine ligase modifier ligase subunit modifier (GCLM subunit). Further (GCLM analysis). Further revealed analysisthat 6-shogaol revealed and that its metabolite6-shogaol and activated its metabolite Nrf2 via theactivated alkylation Nrf2 of via cysteine the alkylation residues ofof Kelch-likecysteine residuesECH-associated of Kelch-like protein ECH-asso 1 (Keap1)ciated [33]. protein Moreover, 1 (Keap1) ginger [33]. phenylpropanoids Moreover, ginger improved phenylpropanoids Nrf2 activity improvedand enhanced Nrf2 theactivity levels and of glutathione enhanced the S-transferase levels of glutathione P1 (GSTP1) S-transferase as well as the P1 downstream (GSTP1) as e ffwellector as of thethe downstream Nrf2 antioxidant effector response of the elementNrf2 antioxidant in foreskin resp fibroblastonse element cells [15 in]. foreskin In a human fibroblast mesenchymal cells [15]. stem In acell human model, mesenchymal ginger oleoresin stem wascell model, investigated ginger for oleoresin its effects was on investigated injuries
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