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The Isolation of Secondary Metabolites from Rheum Ribes L. and The Food Chemistry 342 (2021) 128378 Contents lists available at ScienceDirect Food Chemistry journal homepage: www.elsevier.com/locate/foodchem The isolation of secondary metabolites from Rheum ribes L. and the synthesis T of new semi-synthetic anthraquinones: Isolation, synthesis and biological activity ⁎ Ibrahim Halil Gecibeslera, , Faruk Dislib, Sinan Bayindirc, Mahmut Toprakc, Ali Riza Tufekcid, Ayse Sahin Yaglıoglug, Muhammed Altund, Alpaslan Kocake, Ibrahim Demirtasf, Sevki Ademd a Department of Occupational Health and Safety, Laboratory of Natural Product Research, Faculty of Health Sciences, Bingöl University, Bingöl, Turkey b Department of Physical Therapy and Rehabilitation, Faculty of Health Sciences, Bingöl University, Bingöl, Turkey c Department of Chemistry, Faculty of Science and Arts, Bingöl University, Bingöl, Turkey d Department of Chemistry, Faculty of Science and Arts, Çankiri Karatekin University, Cankiri, Turkey e Department of Biology, Faculty of Science and Arts, Bingöl University, Bingöl, Turkey f Department of Biochemistry, Faculty of Science and Arts, Igdır University, Igdır, Turkey g Department of Chemistry and Chemical Process Technology, Technical Sciences Vocational School, Amasya University, Amasya, Turkey ARTICLE INFO ABSTRACT Keywords: Rheum ribes L. (Rhubarb) is one of the most important edible medicinal plants in the Eastern Anatolia region and Rhubarb is called “Işkın” by local people. Resveratrol and 6-O-methylalaternin were isolated from the Rhubarb for the Food first time in addition to well-known secondary metabolites including emodin, aloe-emodin, β-sitosterol and Antioxidant α rutin. The new semi-synthetic anthraquinone derivatives with the N Fmoc-L-Lys and ethynyl group were syn- Anthraquinone thesized from the isolated anthraquinones emodin and aloe-emodin of Rhubarb to increase the bioactivities. Bioactivity α Aloe-emodin derivative with N Fmoc-L-Lys shows the highest inhibition values by 94.11 ± 0.12 and Human serum albumin Rheum ribes 82.38 ± 0.00% against HT-29 and HeLa cell lines, respectively, at 25 µg/mL. Further, modification of the aloe- α In silico emodin with both the ethynyl and the N Fmoc-L-Lys groups showed an antioxidant activity-enhancing effect. From molecular docking studies, the relative binding energies of the emodin and aloe-emodin derivatives to human serum albumin ranged from −7.30 and −10.62 kcal/mol. 1. Introduction Choowong, Supothina, & Pittayakhajonwut, 2012), neuroprotective and anti-inflammatory effects (Yang, Kim, Lee, & Song, 2018) and are Anthraquinones (9,10-dioxoantracenes) with a wide range of ap- active against multiple sclerosis (Szwed, 2013). plications constitute an important class of natural and synthetic com- R. ribes L. species from Polygonaceae family is very popular among pounds. Moreover, there is an increasing interest in developing new local people of Bingöl, Erzurum, Hakkari and Erzincan by names “Işkın, anthraquinone derivatives with biological activity. Anthraquinone-rich Uçgun and Işgın” is the only native Rheum species which grows wildly edible medicinal plants such as Rheum ribes, Rheum rhabarbarum, in the East and Southeast Anatolia (Öztürk, Aydoğmuş-Öztürk, Duru, & Frangula purshiana, Frangula alnus, Rubia tinctorum and Aloe vera have Topçu, 2007). Rheum species are medically important as they contain been used in folk medicine for a long time (Perassolo, Cardillo, Mugas, anthraquinone-derived compounds and R. ribes is also used as a source Montoya, Giulietti, & Talou, 2017; Çiçek, Ugolini, & Girreser, 2019; of several herbal medicines in the Middle East. Further, the plant is also Zhuang, Yu, Zhong, Liu, & Liu, 2019; Parvez, Al-Dosari, Alam, Rehman, used traditionally as laxative, expectorant, antihelmintic drug and for Alajmi, & Alqahtani, 2019). Anthraquinones show a broad spectrum of the treatment of rheumatic haemorrhoids, measles, smallpox, bile pharmacological activities, such as anti-HIV, cytotoxic and anti-plas- complications, stomach diseases, vomiting, diarrhea, hypertension, modial (Feilcke et al., 2019), antifungal and antibacterial obesity, ulcers and diabetes besides being used as a vegetable, snacks, (Mohamadzadeh, Zarei, & Vessal, 2020), antiviral (Zhang et al., 2016), appetizers and salad (Naqishbandi, Josefsen, Pedersen, & Jäger, 2009; antiplatelet and anticoagulant (Seo, Ngoc, Lee, Kim, & Jung, 2012), Abudayyak, 2019). In previous isolation studies, it has been reported antimalarial and anti-tuberculosis (Supong, Thawai, Suwanborirux, that the R. ribes has secondary metabolites including emodin, physcion, ⁎ Corresponding authors. E-mail address: [email protected] (I.H. Gecibesler). https://doi.org/10.1016/j.foodchem.2020.128378 Received 28 March 2020; Received in revised form 9 October 2020; Accepted 9 October 2020 Available online 15 October 2020 0308-8146/ © 2020 Elsevier Ltd. All rights reserved. I.H. Gecibesler, et al. Food Chemistry 342 (2021) 128378 Fig. 1. Structure of secondary metabolites isolated from R. ribes (A) and semi-anthraquinones (B). chrysophanol, rhein, aloe-emodin, physcion-8-O-glucoside, aloee- 2. Materials and methods modin-8-O-glucoside, sennoside A, rhaponticin, quercetin, 5-deox- yquercetin, quercetin 3-O-rhamnoside, quercetin-3-O-galactoside, 2.1. Reagents quercetin-3-O-rutinoside, β-sitosterol-3β-glucopyranoside-6'-O-fatty acid esters, triacylglycerols, β-sitosterol, phytyl fatty acid esters, and Trifluoroacetic acid (TFA), copper (II) sulfate4 (CuSO ), potassium chlorophyllide A (Tosun & Kızılay, 2003; Ragasa et al., 2017). carbonate (K2CO3), sodium sulfate (Na2SO4), copper (I) iodide (CuI), α In the present study, the R. ribes, which has a very broad spectrum of N,N-diisopropylethylamine (DIPEA), hydrogen iodide (HI), N Fmoc-L- ε biological activity and is famous for its anthraquinones, was selected as Lys-N Boc, sterile dimethylsulfoxide (DMSO), 5-Bromo-2′-deoxyuridine a possible source of bioactive natural products and its anthraquinones (BrdU), sulfuric acid (H2SO4), sodium chloride (NaCl), human serum emodin (E) and aloe-emodin (AE) were selected as target precursors to albumin (HSA), sodium hydroxide (NaOH), ammonium hydroxide synthesize their new bioactive semi-synthetic derivatives. Further iso- (NH4OH), phosphoric acid (H3PO4), 1,1-diphenyl-2-picrylhydrazyl lation studies of R. ribes extract resulted in isolation of resveratrol and (DPPH), potassium hexacyanoferrate (III) (K3Fe(CN)6), trichloroacetic 6-O-methylalaternin, for the first time from R. ribes species, as well as acid (TCA), iron (III) chloride (FeCl3), iron (II) chloride (FeCl2), 3-(2- the isolation of four well-known secondary metabolites β-sitosterol, Pyridyl)-5,6-diphenyl-1,2,4-triazine-p,p′-disulfonic acid monosodium aloe-emodin, emodin, and rutin (Fig. 1A). Following isolation of emo- salt hydrate (ferrozine), butylated hydroxyanisole (BHA), butylated dine and aloe-emodine from R. ribes we have designed and synthesized hydroxytoluene (BHT), ethylenediaminetetraacetic acid (EDTA) and α- new anthraquinones E-1 (9), AE-1 (10), FLE (11) and FLAE (12) con- tocopherol (Vit. E) were purchased from Sigma (St. Louis, MO, USA). taining L-lysine groups (Fig. 1B). Biological activity screening studies, All other chemicals including n-hexane (n-C6H12), chloroform (CHCl3), carried out during the current work, are i) anticancer activity assays dichloromethane (CH2Cl2), n-butanol (n-BuOH), methanol (CH3OH) evaluated against human prostate cancer (PC-3), human cervix cancer and ethyl acetate (EtOAc) were supplied in analytical purity. (HeLa) and human colon cancer (HT-29) cell lines, ii) antioxidant ac- tivities (DPPH free radical scavenging activity, ferrous chelating capa- city, and ferric reducing power assays) and iii) interaction tests with 2.2. Plant material transport protein human serum albumin. The study showed that natural and semi-synthetic products obtained from R. ribes could be potentially The aerial part of R. ribes was collected from the rocky slopes of used in the development of new and promising natural products as food Bingöl Yelesen village at the altitude of 1970 m (38°52′07.8″N, additives. 40°19′26.7″ E) during flowering period. The plant materials were dried in dark place. Herbarium samples were prepared by Alpaslan Kocak and stored at Herbarium of Bingol University with the herbarium number of KOCAK-4003. 2 I.H. Gecibesler, et al. Food Chemistry 342 (2021) 128378 2.3. Extraction, isolation, synthesis and structure elucidation dissolving, each reaction flasks E-1 and AE-1 were mixed separately by adding CuI (1.01 mmol) and DIPEA (6.06 mmol), respectively. Then, α ε The aerial part of dried R. ribes (5 kg) was extracted with the N Fmoc-L-Lys-N N3 (3, 1.01 mmol) was added dropwise to the re- CH3OH:CH2Cl2 (1:1; v:v, 30 L, four consecutive times) and 523.8 g of action flask with a dropping funnel and stirred overnight at 61–62°C dry extract was obtained by evaporating the solvent using a rotary under reflux. After completion, the reaction mixture was cooled tola- evaporator. The dry extract (473.8 g) was suspended in distilled water boratory temperature and the reaction was completed by adding (4L) and extracted with CHCl3 (1200 mL × 20), EtOAc (1200 mL × 9) NH4OH solution and extracted with chloroform (3 × 25 mL). The or- and n-BuOH (1200 mL × 6) in the given order of 216.3, 113.2 and ganic phase was dried over anhydrous Na2SO4, and the solvent was 74.2 g dry extracts were obtained, respectively. CHCl3, EtOAc and n- removed in vacuo. The compounds FLE and FLAE were purified from the BuOH
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