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Neolignans from the Twigs of Corylopsis Coreana Uyeki

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Neolignans from the Twigs of Corylopsis Coreana Uyeki plants Article SIRT1 Activation Enhancing 8,30-Neolignans from the Twigs of Corylopsis coreana Uyeki Hyun-Woo Kim 1,2 , Jin-Bum Jeon 1, Mi Zhang 1, Hyo-Moon Cho 1 , Byeol Ryu 1, Ba-Wool Lee 1 , William H. Gerwick 2,3 and Won-Keun Oh 1,* 1 Korea Bioactive Natural Material Bank, Research Institute of Pharmaceutical Sciences, College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University, Seoul 08826, Korea; [email protected] (H.-W.K.); [email protected] (J.-B.J.); [email protected] (M.Z.); [email protected] (H.-M.C.); [email protected] (B.R.); [email protected] (B.-W.L.) 2 Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, La Jolla, CA 92093, USA; [email protected] 3 Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA 92093, USA * Correspondence: [email protected] Abstract: Three undescribed 8,30-neolignans, corynol (1), 3-methoxy-corynol (2) and 30-deoxy-corynol (3), together with two bergenin derivatives, three flavonoids, two hydrolysable tannins and six simple phenolic compounds, were isolated from the twigs of Corylopsis coreana Uyeki. The structures of the 8,30-neolignans were elucidated by analyzing their NMR, HRESIMS and ECD spectra. All the isolated compounds were evaluated for their SIRT1 stimulatory activity, and 30-deoxy-corynol (3) showed SIRT1 stimulation activity. Furthermore, a docking study of 3 was performed with three representative binding pockets of SIRT1. Citation: Kim, H.-W.; Jeon, J.-B.; Zhang, M.; Cho, H.-M.; Ryu, B.; Lee, Keywords: Corylopsis coreana; hamamelidacease; neolignan; SIRT1 B.-W.; Gerwick, W.H.; Oh, W.-K. SIRT1 Activation Enhancing 8,30-Neolignans from the Twigs of Corylopsis coreana Uyeki. Plants 2021, 1. Introduction 10, 1684. https://doi.org/10.3390/ The genus Corylopsis is one of 31 genera of the Hamamelidacea family, and it is dis- plants10081684 tributed primarily in tropical and subtropical mountainous regions. Corylopsis coreana Uyeki, also called Korean winter hazel, is an endemic species of the Korean Peninsula that Academic Editor: Maria Iorizzi is distributed in the Jiri Mountains and Gwangdeok of South Korea. It is a deciduous shrub with yellowish brown or dark brown twigs that is famous for flowering before the leaves Received: 16 July 2021 appear in the spring. Little research has been performed on C. coreana; however, several Accepted: 12 August 2021 Published: 16 August 2021 bioactivities have been reported for extracts of the plant, including antioxidative, antipro- liferative, antimicrobial and xanthine oxidase inhibitory activities [1–3]. Hydrolysable C. coreana Publisher’s Note: MDPI stays neutral tannins and flavonoids have been reported as chemical constituents of , and this with regard to jurisdictional claims in plant produces large quantities of bergenin, the C-glycoside of 4-O-methyl gallic acid [4,5]. published maps and institutional affil- Silent mating type information regulation 2 homolog 1 (SIRT1), a member of the iations. sirtuins, is a nicotinamide adenine dinucleotide (NAD)-dependent deacetylase that is involved in cellular metabolism [6]. Over the past two decades, accumulating evidence has indicated that sirtuins are not only energy status sensors but also protect cells against metabolic stresses such as regulating inflammation, aging and autophagy [7]. SIRT1 has a key role in metabolic health by deacetylating many target proteins in numerous tissues, Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. including liver, muscle, adipocyte and heart tissue [8]. Recently, SIRT1 research has focused This article is an open access article on regulating cellular senescence and delaying cellular aging by deacetylation of the p53 distributed under the terms and protein [9]. conditions of the Creative Commons Despite the biological interests in SIRT1, only a few natural product-derived SIRT1 Attribution (CC BY) license (https:// activators have been reported. Resveratrol, a well-known stilbenoid antioxidant, is a SIRT1 creativecommons.org/licenses/by/ activator that stabilizes protein–substrate interactions [10]. In addition, several natural 4.0/). products, including quercetin and fisetin (flavonoids), berberine (isoquinoline alkaloid) Plants 2021, 10, 1684. https://doi.org/10.3390/plants10081684 https://www.mdpi.com/journal/plants Plants 2021, 10, 1684 2 of 12 and curcumin (diarylheptanoid), have been shown to directly or indirectly increase SIRT activation in cells [11]. In our previous studies, we reported that flavonoids from Psoralea corylifolia possess SIRT1-promoting activities [12]. Interestingly, most of these reported natural SIRT1 activators have a diphenyl moiety in their structure. Lignans are a major class of polyphenol and commonly possess a diphenyl moiety as part of their structure; however, they have not been studied for their SIRT1 stimula- tory effects. The only exception is magnolol, which has been reported to increase SIRT1 expression in an experimental rat stroke model [13]. Lignans and neolignans are a large group of naturally occurring phenols that are widely distributed within plants [14], and some 5258 lignans have been reported in nature. Among them, only 83 compounds have been reported as 8,30-neolignans. Biosynthetically, 8,30-neolignans are reduced forms of 7,40-epoxy-8,30-neolignans, a process that is catalyzed by phenylcoumaran benzylic ether reductase (PCBER) [15], and also found in the metabolism of dehydrodiisoeugenol (DDIE) with demethylation and ring-opening reaction [16]. The bioactivity of 8,30-neolignans has rarely been investigated. Icariside E5, which was isolated from Capsicum annuum, protects Jurkat cells from apoptosis induced by oxidative stress mediated by serum with- drawal [17]. Piperkadsin C, which was isolated from Piper kadsura, potently inhibits NO production in LPS-activated BV-2 microglial cells. Thus, investigations of the bioactivities of 8,30-neolignan could be worthwhile and may lead to the discovery of new sources of bioactive compounds. Investigations into the natural product chemical diversity in C. coreana isolated three pre- viously undescribed 8,30-neolignans (1–3) with 13 known compounds (4–16). The structures of the undescribed compounds were identified and named corynol (1), 3-methoxy-corynol (2) and 30-deoxy-corynol (3) based on an analysis of their NMR, HRESIMS and ECD spectra. Subsequently, we evaluated the isolated compounds for their SIRT1-promoting activities. 2. Results and Discussion 2.1. General The methanolic extract of twigs of C. coreana was suspended in H2O and partitioned successively using n-hexane, CH2Cl2, EtOAc and H2O. The water residues were sub- jected to Diaion HP-20 resin column chromatography and eluted with H2O and MeOH to provide two fractions. The CHCl2, EtOAc and MeOH extracts were separated by chro- matographic methods, and three previously undescribed neolignans (1–3) were isolated along with 13 known compounds including bergenin (4)[18], 11-O-galloyl bergenin (5)[19], (−)-epicatechin (6)[20], (−)-epicatechin 3-O-gallate (7)[21], (−)-epigallocatechin gallate (8)[22], 1,2,4,6-tetra-O-galloyl-β-D-glucose (9)[23], 1,2,3,4,6-penta-O-galloyl-β-D-glucose (10)[24], ellagic acid (11)[25], benzoic acid (12)[26], 3,4,5-trihydroxybenzoic acid (13)[27], 3,5-dihydroxy-4-methoxybenzoic acid (14)[28], 1-(4-hydroxy-3,5-dimethoxyphenyl)-1- propanone (15)[29] and 3,4,5-trimethoxyphenyl-(60-O-galloyl)-O-β-D-glucopyranoside (16) (Figure1)[ 30]. The structures of the known compounds (4-16) were identified by comparison with previously reported NMR data. Plants 2021, 10, 1684 3 of 12 Figure 1. Chemical structures of 16 isolated compounds from C. coreana. 2.2. Structure Elucidation of the Previously Undescribed Compounds Compound 1 was obtained as a pale brown amorphous powder. Its molecular formula was determined to be C18H20O3 based on the high-resolution electrospray ionization mass − spectrometry (HRESIMS) ion peak at m/z 283.1332 [M-H] (calcd for C18H19O3, 283.1334). The IR spectrum showed the presence of hydroxy (3365 cm−1) and aromatic (1441 cm−1) 1 groups. In the H NMR spectrum of 1 (Figure S1), two aromatic proton signals at dH 6.95 (2H, d, J = 8.4 Hz, H-2, 6) and 6.64 (2H, d, J = 8.4 Hz, H-3, 5) showed an AA0XX0 aromatic 0 system (A ring). The meta-coupled proton signals at dH 6.47 (1H, d, J = 1.9 Hz, H-6 ) and 6.44 (1H, d, J = 1.9 Hz, H-20) indicated the presence of a meta-coupled aromatic system 0 (B ring) in 1. Three olefinic proton signals at dH 5.90 (1H, ddt, J = 16.8, 10.2, 6.7 Hz, H-8 ), dH 0 0 5.00 (1H, dd, J = 16.8, 1.1 Hz, H-9 a) and dH 4.97 (1H, dd, J = 10.2, 1.1 Hz, H-9 b) indicated the presence of an unsaturated aliphatic chain. Further analysis of the 2D NMR spectra of 1 helped to define its molecular structure (Figure2 and Figure S2). The connection of the saturated aliphatic chain between H-7 ( dH 2.88 and 2.55), H-8 (dH 3.33) and H-9 (dH 1.11) was confirmed as a propyl group by analysis of the 1H-1H COSY spectrum. The connection of an unsaturated aliphatic chain between 0 0 0 H-7 (dH 3.19), H-8 (dH 5.90) and H-9 (dH 5.00 and 4.97) was also confirmed as a propylene 0 group by COSY. The HMBC correlations of H-8 (dH 3.33) with C-1 (dC 133.7), C-2 (dC 119.0) 0 and C-4 (dC 141.9) suggested that the aromatic rings were linked via a saturated aliphatic chain at C-1 and C-30. The propylene group was located at C-10, which was confirmed by 0 0 0 the HMBC correlation of H-7 (dH 3.19) with C-6 (dC 113.7) and C-2 (dC 119.0).
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