Antioxidant Effects of Schisandra Chinensis Fruits and Their Active Constituents

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Antioxidant Effects of Schisandra Chinensis Fruits and Their Active Constituents antioxidants Review Antioxidant Effects of Schisandra chinensis Fruits and Their Active Constituents Dalia M. Kopustinskiene 1 and Jurga Bernatoniene 1,2,* 1 Institute of Pharmaceutical Technologies, Faculty of Pharmacy, Medical Academy, Lithuanian University of Health Sciences, Sukileliu pr. 13, LT-50161 Kaunas, Lithuania; [email protected] 2 Department of Drug Technology and Social Pharmacy, Faculty of Pharmacy, Medical Academy, Lithuanian University of Health Sciences, Sukileliu pr. 13, LT-50161 Kaunas, Lithuania * Correspondence: [email protected] Abstract: Schisandra chinensis Turcz. (Baill.) fruits, their extracts, and bioactive compounds are used in alternative medicine as adaptogens and ergogens protecting against numerous neurological, cardiovascular, gastrointestinal, liver, and skin disorders. S. chinensis fruit extracts and their active compounds are potent antioxidants and mitoprotectors exerting anti-inflammatory, antiviral, anti- cancer, and anti-aging effects. S. chinensis polyphenolic compounds—flavonoids, phenolic acids and the major constituents dibenzocyclooctadiene lignans are responsible for the S. chinensis antioxidant activities. This review will focus on the direct and indirect antioxidant effects of S. chinensis fruit extract and its bioactive compounds in the cells during normal and pathological conditions. Keywords: Schisandra chinensis; lignan; schisandrin B; antioxidant; pro-oxidant; mitochondria Citation: Kopustinskiene, D.M.; 1. Introduction Bernatoniene, J. Antioxidant Effects Schisandra chinensis Turcz. (Baill.) belongs to the Schisandraceae family. The plants of Schisandra chinensis Fruits and are native to northeastern China, Japan, Korea, Manchuria, and the Far East part of Russia. Their Active Constituents. Their purple-red berries are called five-flavor fruits because of the sweet, bitter, pungent, Antioxidants 2021, 10, 620. https:// salty, and sour taste [1–5]. S. chinensis is widely used as an herbal supplement in traditional doi.org/10.3390/antiox10040620 Chinese medicine and in Western phytotherapy [1,2,4,5], whereas in Russia—as a potent adaptogen, improving disease and stress tolerance, and increasing energy, endurance, and Academic Editor: Stefania D’Angelo physical performance [2,3]. S. chinensis is used as a preservative and an additive in food technology to enhance the Received: 25 March 2021 flavor, taste, and nutritional value to the food [2]. The dried fruits of the S. chinensis and their Accepted: 16 April 2021 extracts are helpful in the treatment of neurological, cardiovascular, and gastrointestinal Published: 18 April 2021 disorders, in decreasing fatigue, reducing obesity, and protecting from mitochondrial dysfunction, insomnia, and the excessive sweating [1,2,5]. They stimulate immunity, act Publisher’s Note: MDPI stays neutral as a tonic, and exert antioxidant, anti-inflammatory, antiviral, anticancer, anti-aging, anti- with regard to jurisdictional claims in diabetic, and liver- and skin-protecting activities [1–5]. published maps and institutional affil- iations. 2. Chemical Properties of Schisandra chinensis Fruit Constituents S. chinensis fruits contain about 1.5% sugars (polysaccharides and monosaccharides; glucose, fructose, galactose, and arabinose), tannins (hydrolysable, e.g., gallic acid es- ters, and condensed, e.g., proanthocyanidins and catechol-type tannins), color substances Copyright: © 2021 by the authors. (mainly anthocyanins), and about 3% essential oils, with sesquiterpenes as the dominant Licensee MDPI, Basel, Switzerland. compounds [6]. α-Bergamotene, β-chamigrene, β-himachalene, and ylangene are the main This article is an open access article components of essential oils (about 75%), whereas oxygenated sesquiterpenes, monoter- distributed under the terms and penes, and oxygenated monoterpenes comprise the smaller part (about 5%) [6]. Chemical conditions of the Creative Commons investigations also revealed the presence of triterpenoids (lanostane and cycloartane-type Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ triterpenoids and nortiterpenoids), organic acids (citric, fumaric, malic, and tartaric acids), 4.0/). Antioxidants 2021, 10, 620. https://doi.org/10.3390/antiox10040620 https://www.mdpi.com/journal/antioxidants Antioxidants 20212021,, 1010,, 620x FOR PEER REVIEW 22 of of 11 phenolicacids), phenolic acids (chlorogenic, acids (chlorogenic, gentisic, gentisic, p-hydroxybenzoic, p-hydroxybenzoic, p-coumaric, p-coumaric, protocatechuic, protocate- sy- chuic,ringic, syringic and salicylic, and acids)salicylic [7 ,acids)8], flavonoids [7,8], flavonoids (quercetin, (querc isoquercitrin,etin, isoquercitrin, rutin, and rutin hypero-, and hyperoside)side) [8], vitamins [8], vitamins C and E, C phytosterols,and E, phytosterols, and bioelements and bioelem (Cr,ents Cu, (Cr, Co, Ca,Cu, Mg,Co, Ca, Fe, Zn,Mg, Mn, Fe, Zn,B, Ni,) Mn, [1 B,,7 ,Ni,)9]. [1,7,9]. The major active compounds of S. chinensischinensis (Figure(Figure1 1)) are are dibenzocyclooctadiene dibenzocyclooctadiene lignans [1] [1].. Schisandrin is the most dominant S. chinensis lignan found in thethe amountsamounts ofof 2.22.2–5.3–5.3 mg/g in in S.S. chinensis chinensis fruitfruit [2,10 [2,10]].. Figure 1. Chemical structures of main Schisandra chinensis lignans. Figure 1. Chemical structures of main Schisandra chinensis lignans. Anticancer activity of S. chinensis lignans is decreased in the presence of a hydroxyl groupAnticancer at the C7 activity position, of thusS. chinensis resulting lignans in increased is decreased hydrophilicity in the presence and decreased of a hydroxyl per- meability into the lipid bilayer [11], whereas a methylenedioxy group between C12 and group at the C7 position, thus resulting in increased hydrophilicity and decreased perme- C13 enhanced anticancer activity. A 1,2,3-trimethoxy moiety, a 6-acyloxy group, and the ability into the lipid bilayer [11], whereas a methylenedioxy group between C12 and C13 absence of a 7-hydroxy group resulted in P-glycoprotein inhibition and also increased S. enhanced anticancer activity. A 1,2,3-trimethoxy moiety, a 6-acyloxy group, and the ab- chinensis anticancer efficacy [12]. Gomisin N and deoxyschisandrin were the most effective sence of a 7-hydroxy group resulted in P-glycoprotein inhibition and also increased S. anticancer lignans of S. chinensis [11,12]. S. chinensis lignans without an ester group at C6, a chinensis anticancer efficacy [12]. Gomisin N and deoxyschisandrin were the most effective hydroxyl group at C7, or a methylene dioxy moiety, and with an R-biphenyl configuration anticancer lignans of S. chinensis [11,12]. S. chinensis lignans without an ester group at C6, possess strong antiplatelet activity, with 6,7-dehydroschisandrol A as the most active com- a hydroxyl group at C7, or a methylene dioxy moiety, and with an R-biphenyl configura- pound [13]. The exocyclic methylene group in S. chinensis lignan structure is necessary for tion possess strong antiplatelet activity, with 6,7-dehydroschisandrol A as the most active the antioxidant activity, which is enhanced even more in the presence of the benzoyloxy compound [13]. The exocyclic methylene group in S. chinensis lignan structure is necessary group [14]. for the antioxidant activity, which is enhanced even more in the presence of the benzo- yloxy3. Bioavailability group [14]. of Schisandra chinensis Fruit Extract and Its Constituents The bioavailability studies of S. chinensis products were mainly performed in animals. 3. Bioavailability of Schisandra chinensis Fruit Extract and Its Constituents A maximum concentration of schisandrin of 0.08 ± 0.07 and 0.15 ± 0.09 µg/mL was achievedThe bioavailability after oral administration studies of S. of chinensis 3 g/kg and products 10 g/kg were of S.mainly chinensis performedfruit extract in ani- in mals.rats [15 A]. maximum In a parallel concentration study, schisandrin of schisandrin (10 mg/kg, of 0.08 administered ± 0.07 and 0.15 intravenously ± 0.09 μg/mL (i.v.) was or achievedorally (p.o.)) after and oral the administration herbal extract of of 3 S.g/kg chinensis and 10(3 g/kg g/kg of andS. chinensis 10 g/kg, fruit p.o.) extract were in given rats [15]indivi-dually. In a parallel to rats study, [15 ].schisandrin The dose of(10S. mg/kg, chinensis administered(3 g/kg) was intrave equivalentnously to (i.v.) schisandrin or orally (5.2(p.o.)) mg/kg), and the whereas herbal extract the dose of S. of chinensisS. chinensis (3 g/kg(10 g/kg)and 10 was g/kg, equivalent p.o.) were to given schisandrin indivi- (17.3dually mg/kg) to rats [ 15[15]].. Thus, The dose in rats, of theS. chinensis oral bioavailability (3 g/kg) was of schisandrinequivalent wasto schisandrin approximately (5.2 15.56mg/kg),± 10.47%whereas [ 15the]. Whendose of Sprague-Dawley S. chinensis (10 g/kg) rats were was administeredequivalent to 2schisandrin mg/kg (i.v.) (17.3 or 10mg/kg) mg/kg [15] (intragastrically. Thus, in rats, the (i.g.)) oral of bioavailability schisandrol B, of or schisandrin 6 mL/kg (i.g.) wasof approximatelyS. chinensis extract 15.56 (equivalent± 10.47% [15] to. 15When mg/kg Sprague schisandrol-Dawley B), rats the were oral administered absolute bioavailability 2 mg/kg (i.v.) of schisandrol or 10 mg/kg B was(intragastrically approximately (i.g.)) 18.73% of schisandrol and 68.12%, B, or respectively 6 mL/kg (i.g.) [16 ].of SchisandrinS. chinensis extract B could (equivalent modulate tocytochrome 15 mg/kg P450schisandrol 3A activity B), the (CYP3A) oral absolutein vivo bioavailabilityin
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