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Target-Guided Isolation of O-Tigloylcyclovirobuxeine-B from Buxus Sempervirens L

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Target-Guided Isolation of O-Tigloylcyclovirobuxeine-B from Buxus Sempervirens L molecules Article Target-Guided Isolation of O-tigloylcyclovirobuxeine-B from Buxus sempervirens L. by Centrifugal Partition Chromatography Lara U. Szabó and Thomas J. Schmidt * Institute of Pharmaceutical Biology and Phytochemistry (IPBP), University of Münster, Pharma Campus Correnstraße 48, D-48149 Münster, Germany; [email protected] * Correspondence: [email protected]; Tel.: +49-251-83-33378 Academic Editor: Derek J. McPhee Received: 7 September 2020; Accepted: 16 October 2020; Published: 19 October 2020 Abstract: The increasing drug resistance of malaria parasites challenges the treatment of this life-threatening disease. Consequently, the development of innovative and effective antimalarial drugs is inevitable. O-tigloylcyclovirobuxeine-B, a nor-cycloartane alkaloid from Buxus sempervirens L., has shown promising and selective in vitro activity in previous studies against Plasmodium falciparum (Pf ), causative agent of Malaria tropica. For further investigations, it is indispensable to develop an advanced and efficient isolation procedure of this valuable natural product. Accordingly, we used liquid–liquid chromatography including centrifugal partition chromatography (CPC) to obtain the pure alkaloid on a semi-preparative scale. Identification and characterization of the target compound was accomplished by UHPLC/+ESI-QqTOF-MS/MS, 1H NMR and 13C NMR. In conclusion, this work provides a new and efficient method to obtain O-tigloylcyclovirobuxeine-B, a valuable natural product, as a promising antiplasmodial lead structure for the development of innovative and safe medicinal agents. Keywords: Buxus sempervirens L.; nor-cycloartane alkaloids; O-tigloylcyclovirobuxeine-B; antimalarial activity; target-guided isolation; centrifugal partition chromatography 1. Introduction Buxus sempervirens L. (European Box; Buxaceae) is an indeciduous shrub, which represents a rich source for nor-triterpene alkaloids of the nor-cycloartane type. Decoctions of the leaves are well known in folk medicine for a variety of indications, including malaria [1,2]. Malaria is a poverty-related infectious disease caused by protozoans of the genus Plasmodium and transmitted by infected female Anopheles mosquitoes. Worldwide there were 228 million estimated malaria cases in 2018 [3]. The development of new effective agents against this life-threatening disease is imperative because of increasing drug resistance. Extracts of the leaves from B. sempervirens L. have shown selective in vitro activity against Plasmodium falciparum that causes the majority of malaria deaths [4–6]. In 2014, Althaus et al. obtained a small amount of O-tigloylcyclovirobuxeine-B from an alkaloid-enriched fraction of B. sempervirens leaf extract by bioactivity-guided isolation. The natural product yielded an IC50 value against Pf of 0.46 µg/mL (0.92 µM) vs. 9.4 µg/mL (18.9 µM) for cytotoxicity against L6 rat cells [5]. Consequently, O-tigloylcyclovirobuxeine-B is a promising lead compound for the development of novel and safe medicinal agents against malaria. For further investigations, including in vivo studies, it is required to establish a simple, reproducible and productive isolation procedure for this valuable compound. For this purpose, we describe a new efficient semi-preparative scale isolation of Molecules 2020, 25, 4804; doi:10.3390/molecules25204804 www.mdpi.com/journal/molecules Molecules 2020, 25, x 2 of 10 tigloylcyclovirobuxeine-BMolecules 2020, 25, 4804 using only liquid–liquid partition chromatography. The authenticity of2 ofthe 10 isolated O-tigloylcyclovirobuxeine-B was proven by 1H NMR, 13C NMR and +ESI-QqTOF-MS/MS. O-tigloylcyclovirobuxeine-B using only liquid–liquid partition chromatography. The authenticity of 2.the Results isolated andO-tigloylcyclovirobuxeine-B Discussion was proven by 1H NMR, 13C NMR and +ESI-QqTOF-MS/MS. We established an advanced and improved isolation method of O-tigloylcyclovirobuxeine-B (1) 2. Results and Discussion without using a solid stationary phase. After extraction of about 1.5 kg of dried plant material, only three Westeps established of liquid–liquid an advanced partition and (one improved acid/base isolation partitioning method step of andO-tigloylcyclovirobuxeine-B two steps of centrifugal partition(1) without chromatography using a solid stationary(CPC)) were phase. required After in extractionorder to obtain of about 35 mg 1.5 of kg target of dried compound. plant material, onlyThe three advantages steps of liquid–liquid in using this partition all-liquid (one separation acid/base scheme partitioning are diverse, step and including two steps a high of centrifugal recovery ofpartition injected chromatography sample, a low solvent (CPC)) consumption were required (less in orderwaste to and obtain expense), 35 mg minimized of target compound. tailing of eluted peaks,The no advantagesirreversible inloss using of sample this all-liquid due to chemisorption, separation scheme high arereproducibility diverse, including and high a high purification recovery levelsof injected [7–9].sample, a low solvent consumption (less waste and expense), minimized tailing of eluted peaks, no irreversible loss of sample due to chemisorption, high reproducibility and high purification 2.1.levels Target-Guided [7–9]. Isolation of O-tigloylcyclovirobuxeine-B (1) 2.1.1.2.1. Target-Guided Extraction and Isolation Alkaloid-Enrichment of O-tigloylcyclovirobuxeine-B of B. sempervirens (1) L. Leaves 2.1.1.The Extraction discovery and of Alkaloid-Enrichment the target compound of asB. antipl sempervirensasmodialL. Leavesprinciple of B. sempervirens leaves followed the observation of an increased antiplasmodial activity of an alkaloid-enriched fraction in comparisonThe discovery to the crude of the dichloromethane target compound (DCM) as antiplasmodial extract [5]. The principle alkaloid-enriched of B. sempervirens fraction leaves was obtainedfollowed by the acid/base observation extraction of an increased of the crude antiplasmodial DCM extract. activity In the ofpresent an alkaloid-enriched study, we obtained fraction 4.63 ing ofcomparison the alkaloid to fraction the crude (ALOF) dichloromethane from 112 g (DCM)of crude extract DCM [ 5extract]. The (GBUS) alkaloid-enriched from 1.47 fractionkg of plant was material.obtained Compared by acid/base to extractionthe crude extract, of the crude a 19-fold DCM enrichment extract. In of the O-tigloylcyclovirobuxeine-B present study, we obtained 4.63(1) was g of observedthe alkaloid in UHPLC/+ESI-QqTOF-MS fraction (ALOF) from 112 (hencefort g of crudeh DCM termed extract “LC/MS”) (GBUS) analysis from 1.47 (Figure kg of 1). plant material. Compared to the crude extract, a 19-fold enrichment of O-tigloylcyclovirobuxeine-B (1) was observed in UHPLC /+ESI-QqTOF-MS (henceforth termed “LC/MS”) analysis (Figure1). FigureFigure 1. UHPLCUHPLC/+ESI-QqTOF-MS/+ESI-QqTOF-MS chromatograms: chromatograms: Base Base peak peak chromatogram chromatogram of m /zof200–1000 m/z 200–1000 (black) , (black),Extracted Extracted ion chromatogram ion chromatogram of m of/z m/z249 249 [M [M+ +2H] 2H]22++ (pink),(pink), Extracted Extracted ion ion chromatogram chromatogram of m/z of 497m/z [M497 + [M H]++ H](blue);+ (blue); (A) (dichloromethaneA) dichloromethane extract extract (GBUS); (GBUS); (B) ( Balkaloid) alkaloid fraction fraction (ALOF). (ALOF). The The target target compoundcompound was was enriched enriched from from GBUS GBUS to to ALOF ALOF by by factor factor 19. 19. 2.1.2. Selection of Suitable Two-Phase Solvent Systems Molecules 2020, 25, 4804 3 of 10 Molecules 2020, 25, x 3 of 10 2.1.2.InSelection order to ofseparate Suitable a Two-Phasesample successfully Solvent Systems by CPC the biphasic solvent system should satisfy some crucial requirements: For an adequate retention of the stationary phase, the settling time should be shorterIn order than to 30 separate s [7]. The a sample distribution successfully coefficient by CPC (termed the biphasic KC according solvent to system [10]) shouldof the target satisfy compound(s)some crucial requirements:between the two For phases an adequate should retention be close of to the one stationary (0.5 ≤ K phase,≤ 1.0) [8]. the A settling smaller time KC shouldvalue tendsbe shorter to give than a less 30 efficient s [7]. Thepeak distribution resolution while coeffi acient larger (termed KC value KC mayaccording result in to broader [10]) of peaks the target due compound(s) between the two phases should be close to one (0.5 K 1.0) [8]. A smaller K value to protracted elution time. Hence the target compound(s) should show≤ ≤ a close to equal distributionC betweentends to the give upper a less and effi cientlower peak phases resolution [8,9]. while a larger KC value may result in broader peaks due to protractedTo choose elution an appropriate time. Hence biphasic the target solvent compound(s) system for shouldthe separation, show a closethe required to equal distribution distribution ofbetween the alkaloids the upper was andevaluated lower phasesby thin [layer8,9]. chromatography (TLC) and LC/MS analysis (ALOF and fractionTo 2). choose In addition, an appropriate the phase biphasic systems solvent were systemassessed for with the separation,regard to a thestable required and rapid distribution (<30 s) phaseof the separation. alkaloids was evaluated by thin layer chromatography (TLC) and LC/MS analysis (ALOF and fractionWe observed 2). In addition, that the the eluent phase system systems Hexane:EtOAc/MeOH:H were assessed with regard2O (7:3/7:3) to a stable(v/v/v/ andv) can rapid provide
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