(Morinda Citrifolia L.) Fruit Juice

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(Morinda Citrifolia L.) Fruit Juice molecules Communication Identification of Anti-Inflammatory Compounds from Hawaiian Noni (Morinda citrifolia L.) Fruit Juice 1, 2, 3 3 3 Dahae Lee y, Jae Sik Yu y, Peng Huang , Mallique Qader , Arulmani Manavalan , Xiaohua Wu 3, Jin-Chul Kim 4, Changhyun Pang 5, Shugeng Cao 3,* , Ki Sung Kang 1,* and Ki Hyun Kim 2,* 1 College of Korean Medicine, Gachon University, Seongnam 13120, Korea; [email protected] 2 School of Pharmacy, Sungkyunkwan University, Suwon 16419, Korea; [email protected] 3 Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI 96720, USA; [email protected] (P.H.); [email protected] (M.Q.); [email protected] (A.M.); [email protected] (X.W.) 4 Natural Product Informatics Research Center, KIST Gangneung Institute of Natural Products, Gangneung 25451, Korea; [email protected] 5 School of Chemical Engineering, Sungkyunkwan University, Suwon 16419, Korea; [email protected] * Correspondence: [email protected] (S.C.); [email protected] (K.S.K.); [email protected] (K.H.K.); Tel.: +1-808-981-8017 (S.C.); +82-31-750-5402 (K.S.K.); +82-31-290-7700 (K.H.K.) These authors contributed equally to this work. y Academic Editor: Lesław Juszczak Received: 23 September 2020; Accepted: 26 October 2020; Published: 27 October 2020 Abstract: Noni (Morinda citrifolia L.) fruit juice has been used in Polynesia as a traditional folk medicine and is very popular worldwide as a functional food supplement. In this study, compounds present in Hawaiian Noni fruit juice, with anti-inflammatory activity in lipopolysaccharide (LPS)-stimulated RAW 264.7 cells were identified. Five compounds were isolated using a bioassay-driven technique and phytochemical analysis of noni fruit juice: asperulosidic acid (1), rutin (2), nonioside A (3), (2E,4E,7Z)-deca-2,4,7-trienoate-2-O-β-d-glucopyranosyl-β-d-glucopyranoside (4), and tricetin (5). The structures of these five compounds were determined via NMR spectroscopy and LC/MS. In an anti-inflammatory assay, compounds 1–5 inhibited the production of nitric oxide (NO), which is a proinflammatory mediator, in LPS-stimulated macrophages. Moreover, the mechanisms underlying the anti-inflammatory effects of compounds 1–5 were investigated. Parallel to the inhibition of NO production, treatment with compounds 1–5 downregulated the expression of IKKα/β, I-κBα, and NF-κB p65 in LPS-stimulated macrophages. Furthermore, treatment with compounds 1–5 downregulated the expression of nitric oxide synthase and cyclooxygenase-2. Thus, these data demonstrated that compounds 1–5 present in noni fruit juice, exhibited potential anti-inflammatory activity; these active compounds may contribute preventively and therapeutically against inflammatory diseases. Keywords: noni; Morinda citrifolia; anti-inflammation; NO production; RAW 264.7 cells 1. Introduction Noni is the Hawaiian name given to Morinda citrifolia Linn. (Family: Rubiaceae), also known as beach mulberry or cheese fruit [1]. It is a small tropical evergreen tree or shrub that is native to Southeast Asia and is distributed in Australia and the South Pacific, including Hawaii [1,2]. The phytotherapeutic applications of noni fruit juice have been mentioned in folklore, and the juice has been successfully used as per traditional systems of medicine to treat a broad range of leading diseases Molecules 2020, 25, 4968; doi:10.3390/molecules25214968 www.mdpi.com/journal/molecules Molecules 2020, 25, 4968 2 of 12 Molecules 2020, 25, x FOR PEER REVIEW 2 of 12 likediseases diabetes, like diabete cancer,s, hypertension, cancer, hypertension, cardiovascular cardiovascular diseases, arthritis,diseases, pathogenic arthritis, pathogenic and worm and infections, worm poorinfections, indigestion, poor indigestion, and HIV–AIDS and HIV and– drugAIDS addiction and drug [3 addiction–5]. [3–5]. The products derived from noninoni are very popular globally,globally, particularlyparticularly the fruit juice,juice, which is used as a functionalfunctional food supplement [[3]3].. Noni juice was introduced intointo markets in the USA in thethe 1990s1990s andand intointo EuropeanEuropean communities since 2003 [[3]3].. By now, the products are very famous in New Zealand, Australia,Australia, andand somesome Asian Asian countries countries [ 6[6]].. The The worldwide worldwide market marke fort for noni-derived noni-derived products products is peakingis peaking each each year; year in; in 2006, 2006 it, reachedit reached USD USD two two billion billion [6]. [6]. Nuclear factorfactor kappa kappa B (NF-B (NFκB)-κB) is a transcriptionis a transcription factor thatfactor mainly that regulatesmainly regulates the cellular the responses cellular toresponses inflammation, to inflammation, cancer, and cancer, nervous and system nervous functioning system [7functioning]. The activation [7]. Th ofe NF-activationκB contributes of NF-κB to thecontributes development to the ofdevelopment various disorders, of various including disorders, rheumatoid including arthritis, rheumatoid atherosclerosis, arthritis, atherosclerosis, inflammatory bowelinflammatory diseases, bowel multiple diseases, sclerosis, multiple and tumors sclerosis, [8]. and The tumors inhibition [8] of. The NF- iκnhibitionB could stopof NF the-κB proliferation could stop ofthe tumor proliferation cells, which of tumor could cells become, which more could sensitive become tomore antitumor sensitive agents to antitumor [9]. Thus, agents the [9] inhibition. Thus, the of NF-inhibitionκB signaling of NF- hasκB potentialsignaling therapeutichas potential applications therapeutic in applications cancer and inflammatoryin cancer and diseasesinflammatory [8]. It wasdiseases reported [8]. I thatt was patients reported with that stage patients III/IV with invasive stage adenocarcinoma III/IV invasive adenocarcinoma who consumed homemadewho consum nonied fruithomemade juice regained noni fruit their juice body regained weight their after body 4 weight weeks [after10]. 4 This weeks encouraged [10]. This en researcherscouraged researchers to conduct in-depthto conduct studies in-depth on nonistudies fruit on juice. noni Asfruit an juice. initiative As an in initiative 2001, clinical in 2001, studies clinical have studies been carried have been out. However,carried out. after However, 5 years, after they 5 wereyears, unable they were to publish unable any to publish data supporting any data thesupporting relevance the [11 relevance]. In our previous[11]. In our studies previous on noni studies juice, on we noni identified juice, we alkyl identified catechols alkyl (4-methyl catechols catechol, (4-methyl 4-ethyl catechol, catechol, 4-eth andyl 4-vinylcatechol, catechol) and 4-vinyl [12] and catechol scopoletin) [12] [ 13and], among scopoletin which [13] 4-methyl, among catechol, which 4-ethyl4-methyl catechol, catechol, and 4-vinyl4-ethyl catecholcatechol, areand potent 4-vinyl molecules catechol thatare providepotent molecules protection that against provide diseases, protection like cancer against associated diseases, with like oxidativecancer associated stress, by with stimulating oxidative nuclear stress, factor by stimulating erythroid 2-related nuclear factorfactor 2erythroid (Nrf2) transcription 2-related factor factors. 2 In(Nrf2) continuation, transcription the factors. present In study continuation, was undertaken the present to isolatestudy was and undertaken identify inflammatory to isolate and inhibitors identify presentinflammatory in noni inhibitors fruit juice usingpresent a bioassay-guided in noni fruit juice technique. usingFive a bioassay compounds-guided (1–5 )technique (Figure1). wereFive isolatedcompounds using (1 column–5) (Figure chromatography 1) were isolated and HPLC,using column and their chromatography structures were and determined HPLC, and via NMRtheir spectroscopicstructures were and determined LC/MS analyses. via NMR Herespectroscopic we report and the LC/MS isolation analys andes. structure Here we characterizationreport the isolation of theseand structure isolates found characterization in noni fruit of juice, these as wellisolates as their found anti-inflammatory in noni fruit juice effects, as and well basic as underlyingtheir anti- mechanisminflammatory of effects action. and basic underlying mechanism of action. Figure 1. Chemical structures of compounds 1–5. Figure 1. Chemical structures of compounds 1–5. Molecules 2020, 25, 4968 3 of 12 MoleculesMolecules 2020 2020, ,25 25, ,x x FOR FOR PEER PEER REVIEW REVIEW 33 ofof 1212 2. Results and Discussion 2. Results Results and and Discussion 2.1.2.1. Isolation IsolationIsolation and and Identification IdentificationIdentification ofof BioactiveBioactive CompoundsCompounds fromfrom NoniNoni FruitFruit JuiceJuice OurOur preliminarypreliminary study study [13] [[13]13] showed showed that that different didifferentfferent noninoni juices,juicesjuices,, includingincluding purchasedpurchased crudecrude noninoni juice, ripe noni juice, and noni juice fermented with Lactobacillus plantarum (ATCC8014) at 22 °C (room juice, ripe ripe noni noni juice, juice, and and noni noni juice juice fermented fermented with with LactobacillusLactobacillus plant plantarumarum (ATCC8014)(ATCC8014) at 22 °C at (room 22 ◦C (roomtemperature)temperature) temperature) at at 24 24 h h [13] at[13] 24 demonstrated demonstrated h [13] demonstrated NF NF--κBκB inhibitio inhibitio NF-κB inhibition.nn.. We We decided decided We to to decided use use the the topurchased purchased use the purchased n nonioni juice juice innoniin thethe juiceanti anti--inflammatory ininflammatory the anti-inflammatory assay assay
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