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Reductive Metabolism of Ellagitannins in the Young Leaves of Castanopsis Sieboldii

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Reductive Metabolism of Ellagitannins in the Young Leaves of Castanopsis Sieboldii molecules Article Reductive Metabolism of Ellagitannins in the Young Leaves of Castanopsis sieboldii Hatsumi Wakamatsu 1,2, Sumire Tanaka 3, Yosuke Matsuo 1 , Yoshinori Saito 1, Koyo Nishida 2 and Takashi Tanaka 1,* 1 Department of Natural Product Chemistry, Graduate School of Biomedical Sciences, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki 852-8521, Japan; [email protected] (H.W.); [email protected] (Y.M.); [email protected] (Y.S.) 2 Department of Pharmaceutics, Graduate School of Biomedical Sciences, Nagasaki University, 1-7-1 Sakamoto, Nagasaki 852-8501, Japan; [email protected] 3 Department of Natural Product Chemistry, School of Pharmaceutical Sciences, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki 852-8521, Japan; [email protected] * Correspondence: [email protected]; Tel.: +81-95-819-2432 Academic Editor: Teresa Escribano-Bailón Received: 2 November 2019; Accepted: 22 November 2019; Published: 24 November 2019 Abstract: The leaves of Castanopsis sieboldii (Fagaceae) contain characteristic hexahydroxydiphenoyl (HHDP) esters of 28-O-glucosyl 2α,3β,23,24-tetrahydroxyolean- and urs-12-en-28-oic acids. In this study, uncharacterized substances were detected in the young leaves, which are not observed in the mature leaves. Preliminary HPLC analyses indicated that the substances had dehydro-HHDP (DHHDP) ester groups; however, the esters were unstable and decomposed during extraction. Therefore, the compounds were isolated as their stable phenazine derivatives by extracting the young leaves with acidic aqueous EtOH containing o-phenylenediamine. The structures of the phenazine derivatives indicated that the unstable metabolites of the young leaves were 3,24-DHHDP esters of the abovementioned triterpenes. Extraction of the young leaves with 80% acetonitrile containing reducing agents, ascorbic acid or dithiothreitol afforded the corresponding HHDP esters. Furthermore, heating of the young leaves in 80% acetonitrile also yielded the same HHDP esters as the reduction products. The results suggested that the HHDP esters are reductively produced from DHHDP esters in the young leaves. In addition, the structures of five previously reported triterpene HHDP esters were revised. Keywords: Castanopsis sieboldii; ellagitannin; dehydrohexahydroxydiphenoyl; hexahydroxydiphenoyl; triterpene 1. Introduction Ellagitannins are a group of hydrolyzable tannins having hexahydroxydiphenoyl (HHDP) ester moieties and related acyl groups [1–3]. The HHDP group is a dimer of the galloyl group, and enzymatic conversion of gallotannins to ellagitannins has been reported [4–6]; however, the details of the biosynthetic mechanisms are still ambiguous. In addition, there is no chemical or biological evidence for the production mechanism of other ellagitannin acyl groups, such as dehydro-HHDP (DHHDP) and chebuloyl [1]. To clarify the biogenetical relationship between ellagitannin acyl groups, the chemical reactivity of the acyl groups and change of tannin composition during leaf growth were examined in our laboratory. Previously, it was demonstrated that the major ellagitannin in the leaves of Camellia japonica was oxidatively degraded as the leaves matured, and the chemical mechanism was proposed [7]. In this study, change of tannin composition in the leaves of Castanopsis sieboldii (syn. C. cuspidata var. sieboldii, Fagaceae) was examined. C. sieboldii is an evergreen broadleaf tree widely distributed in western Japan. Molecules 2019, 24, 4279; doi:10.3390/molecules24234279 www.mdpi.com/journal/molecules Molecules 2019, 24, x FOR PEER REVIEW 2 of 14 Molecules 2019, 24, 4279 2 of 14 tree widely distributed in western Japan. The leaves contain galloyl shikimic acids [8] and ellagitannins, and the latter are mainly composed of a series of HHDP esters of 28-O-glucosyl 2αThe,3β leaves,23,24-tetrahydroxyolean- contain galloyl shikimic and urs-12-en-28-oic acids [8] and ellagitannins, acids (28-O and-glucosyl the latter castanopsigenins are mainly composed A and B) of [9].aseries of HHDP esters of 28-O-glucosyl 2α,3β,23,24-tetrahydroxyolean- and urs-12-en-28-oic acids (28-O-glucosyl castanopsigenins A and B) [9]. 2. Results and Discussion 2. Results and Discussion 2.1. HPLC analysis of the leaves 2.1. HPLC Analysis of the Leaves In the present study, firstly the triterpene HHDP esters in the fresh leaves were compared at differentIn thegrowth present stages study, in spring firstly the(April, triterpene 2015). HPLC HHDP analyses esters in of the the fresh leaf leavesbuds and were small compared young at leavesdifferent at the growth top of stages the twig in spring showed (April, two2015). broad HPLC peaks analyseswith similar of the UV leaf absorptions buds and small to those young of other leaves triterpeneat the top DHHDP of the twig esters showed (Figure two 1A: broad 1′o,u peaks; where with o similar: oleanane UV absorptionstype, u: ursane to those type). of otherHowever, triterpene the substancesDHHDPesters were detected (Figure1A: neither10o,u in; where the winteredo: oleanane leaves type, of theu: ursanesame twig type). (Figure However, 1C) nor the in substances summer maturewere detected leaves of neither the same in the tree wintered collected leaves in July. of the This same observation twig (Figure suggests1C) nor that in summer the tannins mature detected leaves asof the the broad same peaks tree collected in the young in July. leaves This observationare key metabolites suggests in that the the metabolism tannins detected of the triterpene as the broad HHDP peaks esters.in the On young extraction leaves are of keythe metabolitesyoung leaves in thewith metabolism solvent containing of the triterpene o-phenylenediamine, HHDP esters. On the extraction broad peaksof the were young not leaves observed with and solvent two containingpeaks wereo-phenylenediamine, detected at longer retention the broad times peaks (Figure were not 1B, observed 1o, 1u, andand 2o,u two),peaks suggesting were detectedthat the atcompounds longer retention 1′o,u have times DHHDP (Figure1 B,ester1o ,moieties1u, and 2o,u[10].), In suggesting contrast, thatno changethe compounds was observed10o,u onhave treatment DHHDP of the ester mature moieties leaves [10 with]. In o-phenylenediamine. contrast, no change This was study observed aimed on attreatment characterization of the mature of the key leaves metabolites with o-phenylenediamine. 1′o,u in the young This leaves. study aimed at characterization of the key metabolites 10o,u in the young leaves. 1'o,u 2600000 A 10o 10u 2000000 d) B 1u 1o Intensity 2o,u 1000000 10u Absorbance (Max Abs) C 11o 10o 4o 4u 13o 3o,u 12o 11u 13u 9o,u 12u 0 20 22.022 2424.0 2626.0 28.028 30.030 3232.0 34.034 36.036 38.038 40.040 4242.0 min44.0 Retention Time [min] Figure 1. HPLC profiles of 80% CH3CN extracts of the leaves of C. sieboldii before and after derivatization. Figure 1. HPLC profiles of 80% CH3CN extracts of the leaves of C. sieboldii before and after (A) young leaves/80% CH3CN 2% TFA, (B) young leaves/o-phenylenediamine in 80% CH3CN 2% TFA, derivatization. A: young leaves/80% CH3CN 2% TFA, B: young leaves/o-phenylenediamine in 80% (C) mature leaves/80% CH3CN 2% TFA. 1o: 1 with oleanan-type triterpene unit, 1u: 1 with ursane-type CH3CN 2% TFA, C: mature leaves/80% CH3CN 2% TFA. 1o: 1with oleanan-type triterpene unit, 1u: 1 triterpene unit. with ursane-type triterpene unit. 2.2. Structures of Phenazine Derivatives 2.2. Structures of Phenazine Derivatives To determine the structures of the uncharacterized metabolites 10o,u, the young fresh leaves wereTo firstly determine extracted the structures by a conventional of the uncharacterized method using aqueousmetabolites acetone; 1′o,u,however, the young the fresh metabolites leaves weredecomposed firstly extracted during by concentration a conventional of themethod extract using at 40–45aqueous◦C. acetone; The aforementioned however, the metabolites preliminary decomposedexperiments during indicated concentration that the unstable of the metabolitesextract at 40–45 could °C. be The converted aforementioned into stable preliminary derivatives experimentsby treatment indicated with o-phenylenediamine that the unstable (Figuremetabolites1B); therefore,could be theconverted young leavesinto stable were derivatives extracted with by treatment30% AcOH with in o EtOH-phenylenediamine containing o-phenylenediamine. (Figure 1B); therefore, The the extract young was leaves fractionated were extracted by Diaion with HP20SS 30% AcOHcolumn in chromatographyEtOH containing ando-phenylenediamine. the fractions containing The extract triterpene was estersfractionated were furtherby Diaion separated HP20SS by column chromatography and the fractions containing triterpene esters were further separated by Molecules 2019, 24, 4279 3 of 14 reversed-phase column chromatography to yield two phenazine derivatives 1o, 1u and an inseparable mixture of 2o,u. The HR-FAB-MS of 1o and 1u indicated that these compounds had the same molecular formula, + + C56H66N2O17 (1o: m/z 1061.4250 [M + Na] , 1u: m/z 1061.4250 [M + Na] , calcd for C56H66N2O17Na, 1061.4259). Both compounds showed UV absorptions at 377, 277, and 245 nm characteristic of phenazine moieties [11], and the 1H- and 13C-NMR spectra (Table1) showed signals arising from phenazine moieties, which were identical to those observed for the phenazine derivatives of dehydroellagitannins [12]. The 13C-NMR spectra also exhibited signals arising from triterpene and β-glucopyranose moieties, the chemical shifts of
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