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Year : 2017  |  Volume : 13  |  Issue : 51  |  Page : 459-462  

Quassinoids from the root of Eurycoma longifolia and their antiproliferative activity on human cancer cell lines

1 Department of Pharmacognosy, Faculty of Pharmaceutical Sciences, Nagasaki International University, Sasebo, Nagasaki 859-3298, Japan; Department of Pharmacy, School of Medicine and Pharmacy, Vietnam National University, Hanoi, Vietnam
2 Department of Pharmacognosy, Faculty of Pharmaceutical Sciences, Nagasaki International University, Sasebo, Nagasaki 859-3298, Japan
3 Department of Pharmacy, School of Medicine and Pharmacy, Vietnam National University, Hanoi, Vietnam

Date of Submission29-Jul-2016
Date of Acceptance08-Sep-2016
Date of Web Publication19-Jul-2017

Correspondence Address:
Yukihiro Shoyama
Department of Pharmacognosy, Faculty of Pharmaceutical Sciences, Nagasaki International University, 2825-7 Huis Ten Bosch, Sasebo, Nagasaki 859-3298
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/pm.pm_353_16

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Background: The roots of Eurycoma longifolia Jack have traditionally been used as an aphrodisiac tonic besides the other remedies for boils, fever, bleeding gums, and wound ulcer. Recently, the antiproliferative activity of E. longifolia has been reported and remained attractive to natural chemists. Objective: The objective of this study was to study on antiproliferative compounds from the root of E. longifolia. Materials and Methods: Column chromatography was used to separate individual compounds, spectroscopic data including nuclear magnetic resonances and mass spectrometry were analyzed to determine the chemical structure of the isolates and for biological testing, antiproliferative activity of compounds was tested on seven human cancer cell lines (KATO III, HCT-15, Colo205, HepG2, PC-3, Jurkat, HL-60) by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide method. Results: Nine quassinoids including a new C19longilactone-type quassinoid glycoside were characterized from the roots of the title plant. Among them, the major quassinoid eurycomanone exhibited selectively potential antiproliferative activities on the leukemia cell lines (HL-60 and Jurkat) and had very low toxic effects on normal skin fibroblast cell line (NB1RGB). Conclusion: The current study reveals one new quassinoid glycoside and the potential active component (eurycomanone) from E. longifolia for the leukemia treatment.
Abbreviations used: COSY: Correlation spectroscopy; HMBC: Heteronuclear multiple-bond correlation; HMQC: Heteronuclear multiple quantum correlation; NMR: Nuclear magnetic resonance; NOESY: Nuclear Overhauser enhancement spectroscopy; TLC: Thin layer chromatography.

Keywords: Antiproliferative activity, Eurycoma longifolia, leukemia cells, quassinoid, Simaroubaceae

How to cite this article:
Tung NH, Uto T, Hai NT, Li G, Shoyama Y. Quassinoids from the root of Eurycoma longifolia and their antiproliferative activity on human cancer cell lines. Phcog Mag 2017;13:459-62

How to cite this URL:
Tung NH, Uto T, Hai NT, Li G, Shoyama Y. Quassinoids from the root of Eurycoma longifolia and their antiproliferative activity on human cancer cell lines. Phcog Mag [serial online] 2017 [cited 2022 Nov 28];13:459-62. Available from: http://www.phcog.com/text.asp?2017/13/51/459/211035


  • Nine quassinoids (1-9) including one new quassinoid glycoside (9) and eight known ones were isolated from the roots of Eurycoma longifolia
  • The structure of the new quassinoid 9 was determined by extensive chemical and spectroscopic analyses
  • The major quassinoid, eurycomanone (3), exhibited selectively potential antiproliferative activities on both Jurkat and HL-60 leukemia cells and had very low toxic effects on normal skin fibroblast cell line (NB1RGB).

   Introduction Top

Eurycoma longifolia Jack (Simaroubaceae) is a flowering shrub plant native to Indonesia (commonly known as Pasak Bumi), Malaysia (called as Tongkat Ali), and to a lesser extent, Thailand, Vietnam (with local name “Cay Ba Binh”), and Laos. Its roots have traditionally been used as an aphrodisiac tonic besides the other remedies for boils, fever, bleeding gums, and wound ulcer.[1] Previous phytochemical studies on the root of E. longifolia have led to the isolation of nearly seventy quassinoids related to triterpene, considered as principal active constituents and responsible for typical bitter taste, together with several phenolic,[2],[3] typical triterpenes such as melianone,[4] squalene-type triterpene,[5] and canthin-6-one alkaloid like picrasidine L,[6] some of which have potential pharmacological and therapeutic properties.[2],[3]

In our ongoing research regarding anticancer phytotherapy, we previously reported the potent antiproliferative activity of alkannin derivatives from Alkanna tinctoria,[7],[8] crocin from saffron (Crocus sativus),[9],[10] triterpenes from Eriobotrya japonica,[11] and coumarins from Mammea siamensis.[12] As part of the ongoing study, our current phytochemical investigation on antiproliferative constituents from the root of the title plant resulted in the isolation of nine quassinoids including a novel one. This paper herein deals with the structural elucidation of the new quassinoid and the antiproliferative activity of isolated quassinoids using seven human cancer cells.

   Materials And Methods Top

General procedures

Optical rotations were obtained using a P-1020 digital polarimeter (JASCO, Easton, USA). NMR spectra were recorded on a JEOL ECX 400 NMR spectrometer (JEOL, Tokyo, Japan). High-resolution electrospray ionization (HR-ESI) time-of-flight mass spectrometry (MS) experiments utilized a JEOL AccuTOF LC 1100 mass spectrometer (JEOL, Tokyo, Japan). High-performance liquid chromatography (HPLC) analysis of sugar was run on an Agilent 1100 Series HPLC system (Agilent, Santa Clara, CA, USA) equipped with a YMC-Pack NH2 column (250 mm × 4.6 mm i.d., NH12S05-2546WT, YMC Co. Ltd., Kyoto, Japan) and an optical rotation detector JASCO OR-2090 (JASCO, Easton, USA). Column chromatography was performed on silica gel 60 (230–400 mesh, Nacalai Tesque Inc., Kyoto, Japan) and YMC ODS-A gel (50 μm, YMC Co. Ltd., Kyoto, Japan). Thin-layer chromatography (TLC) was performed on Kieselgel 60 F254 and TLC silica gel 60 RP-18 F254S(Merck, Darmstadt, Germany) plates. Spots were visualized by spraying with 1% Ce(SO4)2-10% aqueous H2 SO4 solution, followed by heating.

Plant material

The roots of E. longifolia (powder form) were purchased from Malaysian medicinal market in 2012 and authenticated by one of the authors (YS). A voucher specimen (EL-2012) has been deposited in the Department of Pharmacognosy, Nagasaki International University.

Extraction and isolation

The root powder (500 g) of E. longifolia was extracted with 95% EtOH (2.0 L × 4 times) at 40°C under sonication. The combined extracts were concentrated to give yellow syrup (14.2 g), which was then suspended in water (250 ml) following partitioning with EtOAc (250 ml × 3 times) and water-saturated n-BuOH (250 ml × 3 times) to give EtOAc soluble extract (4.1 g) and n-BuOH soluble extract (4.5 g). The EtOAc extract (4.1 g) was subjected to a silica gel column eluted with CHCl3-MeOH (15:1, v/v) to give nine fractions (fr.1.1–fr.1.9). Fr.1.7 (610 mg) was further chromatographed over a reversed-phase (RP) column eluted with MeOH-H2O (1:2, v/v) to yield 1 (12 mg) and 2 (23 mg). Likewise, fr.1.9 (1050 mg) was applied to a RP column eluted with MeOH-H2O (1:2, v/v) to obtain 3 (28 mg) and 4 (36 mg). BuOH extract (4.5 g) was subjected to a RP column eluted with MeOH-H2O (2:5, v/v) to afford four fractions (fr.2.1–fr.2.4). Then, fr.2.2 (300 mg) was further chromatographed over a silica gel column eluted with CHCl3-MeOH (6:1, v/v) to yield 6 (14 mg), 7 (9 mg), 9 (13 mg), and additional 3 (65 mg). Fr.2.3 (600 mg) was loaded onto a RP column eluted with MeOH-H2O (2:5, v/v) to give 5 (18 mg) and a subfraction (170 mg), which was subsequently applied to a silica gel column eluted with CHCl3-MeOH (5:1, v/v) to yield 8 (9 mg) and additional 4 (58 mg).

Compound 8 (Δ4,5-14-hydroxyglaucarubol): colorless solid; +68° (C 0.45, MeOH); HR-ESI-MS m/z: 413.1819 [M + H]+ (calcd for C20H29O9, 413.1812);1 H-NMR (CD3 OD, 400 MHz) and 13 C-NMR (CD3 OD, 100 MHz) data [Table 1].
Table 1: 1H- and 13C-NMR data for 8 and 9 in CD3OD

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Compound 9: colorless solid; +26° (C 0.30, MeOH); HR-ESI-MS m/z: 513.2348 [M + H]+ (calcd for C25H37O11, 513.2336);1 H-NMR (CD3 OD,400 MHz) and 13 C-NMR (CD3 OD, 100 MHz) data [Table 1].

Acid hydrolysis of 9

A solution of 9 (4.0 mg) in 1.0 M HCl (5.0 ml) was heated under reflux for 4 h. After cooling, the reaction mixture was poured into ice water and neutralized with Amberlite IRA-400 (hydroxyl form), and the resin was removed by filtration. Then, the filtrate was concentrated in vacuo to dryness, followed by partition between EtOAc and H2O. The aqueous layer after filtration was subjected to HPLC analysis with the mobile phase of CH3 CN-H2O (80:20, v/v) at flow rate 0.40 ml/min. D-glucose was detected at 9.6 min with positive optical rotation and compared with the authentic sample.

Cell culture and sample treatment

All cell lines were obtained from RIKEN BioResource Center Cell Bank. HepG2 and NB1RGB were maintained in Dulbecco's modified Eagle's medium and minimum essential medium-α, respectively. The other cell lines were maintained in RPMI1640 medium. All these media were supplemented with 10% fetal bovine serum and 1% penicillin–streptomycin and were then incubated at 37°C under 5% CO2 in fully humidified conditions. For the cell treatment, dimethyl sulfoxide (DMSO) concentrations in the cell culture medium did not exceed 0.2% (v/v) and the controls were always treated with the same amount of DMSO as used in the corresponding experiments.

3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide assay

Cell viability was determined by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay.[11],[12] In brief, the cells were seeded in 96-well plates at a density of 1 × 104 cells/well for suspension cells or 0.5 × 104 cells/well for attached cells. After incubation for 24 h, the cells were treated with each compound at various concentrations for 48 h. At the end of treatment, MTT solution was added to each well, and the cells were incubated for another 4 h. The precipitated MTT-formazan was dissolved with 0.04 N HCl-isopropanol, and the amount of formazan was measured at 595 nm using a microplate reader (iMark, BioRad, Tokyo, Japan). Cell viability was expressed as a percentage of the control culture.

   Results and Discussion Top

The ethanolic extract of the root of E. longifolia was suspended in water and then partitioned with EtOAc and n-BuOH, followed by various column chromatography to afford 13,21-dihydroeurycomanone (1),[13] 14.15 β-dihydroxyklaineanone (2),[2] eurycomanone (3),[2] eurycomanol (4),[14] 2-hydroxylongilactone-4(18)-ene (5),[15] longilactone (6),[2] eurycomaoside (7),[16] Δ4,5-14-hydroxyglaucarubol (8),[17] and especially one new quassinoid (9) [Figure 1].
Figure 1: Structures of quassinoids 1–9

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Compound 8 was obtained as colorless solid and has the molecular formula C20H28O9 based on HR-MS measurement. The 1 H and 13C NMR spectroscopic data of 8 [Table 1] suggested a C20 quassinoid structure similar to 13,21-dihydroeurycomanol with a lactone carbonyl signal (δC175.8), a double bonds (δC129.6, 128.3), and seven oxygenated carbon groups (δC84.2, 79.6, 77.3, 76.5, 71.5, 68.2, 67.9).[2],[13] Further analyses and comparison of NMR data of 8 with those in literature led us to confirm the structure of 8 as Δ4,5-14-hydroxyglaucarubol,[17] which was recently reported when we were doing this research.

Compound 9, a colorless solid, has the molecular formula C20H28O9 as deduced by HR-MS experiment. The NMR data of 9 suggested a quassinoid glycoside. In detail, the 1H NMR (CD3 OD) spectrum of 9 [Table 1] showed four olefinic protons (δ 6.17, 5.63, 5.31, 5.03), five oxymethine protons (δ 5.12, 4.42, 4.06, 3.96, 3.53), a secondary methyl (δ 1.27), and two tertiary methyls (δ 1.46, 1.01), which were attributable to the quassinoid aglycone, and an anomeric proton (δ 4.47) with large coupling constant (J = 8.0 Hz) typical of the β-linked sugar unit. The 13C NMR spectrum of two revealed 25 signals including a set of six signals (δ 100.7, 75.1, 78.0, 71.6, 77.8, 62.6) contributing to a β-glucopyranosyl unit and 19 remaining ones of a C19-quassinoid skeleton, which consisted of a lactone carbonyl (δ 179.4), two double bonds (δ 142.3, 133.4, 126.8, 114.7), five oxymethine carbons (δ 88.1, 82.0, 76.5, 71.7, 65.4), four methines (δ 56.9, 50.4, 42.3, 28.0), two quaternary carbons (δ 44.3, 44.2), a secondary methyl (δ 14.7), and two tertiary methyls (δ 20.9, 13.0), respectively. Further inspection of the 1H and 13C NMR data of 9 found that they were similar to those of eurycomaoside except for the signals belonging to ring A, which were consistent with Δ1,4(18)-diene frame. The acid hydrolysis of 9 liberated D-glucose as confirmed by HPLC analysis. Moreover, the proposed structure of 9 was assured by the HMQC, COSY, and HMBC spectra [Figure 2]. Likewise, the relative stereochemistry of 9 was assigned on the basis of the nuclear Overhauser effect (NOE) spectroscopy spectrum. The transconformation of A/B and B/C junctions was configured due to NOE correlations of H-5/H-1, H-5/H-9, Me-19/H-6, and Me-19/Me-20. In addition, the NOE interactions of H-7/Me-20, H-9/H-11, H-13/Me-20, H-14/Me-20, and H-12/Me-21 further certified the similar stereochemistry between 9 and eurycomaoside (7)[16] as well as longilactone (6)[2] [Figure 3]. Finally, the NOE cross peak of H-1/H-1´ indicated the sugar linkage at C-1 of the quassinoid aglycone. Consequently, the structure of compound 9, one of two quassinoid glycosides including eurycomaoside (7) in nearly 70 quassinoids, was elucidated as depicted in [Figure 1].
Figure 2: Key HMBC and COSY correlations of 8 and 99

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Figure 3: Relative configuration of 8 and 9 with key nuclear Overhauser effect correlations

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In this study, we investigated whether the isolated quassinoids had antiproliferative activities against various cancer cell lines. Accordingly, we examined the effect of quassinoids 1–9 on proliferation of seven human cancer cell lines, namely, KATO III (stomach cancer), HCT-15 (colon cancer), Colo205 (colon cancer), HepG2 (hepatoma), PC-3 (prostate cancer), HL-60 (promyelocytic leukemia), and Jurkat (acute T cell leukemia), and the human normal skin fibroblast cell line NB1RGB. Cells were treated with compounds 1–9 at concentrations of 25 μM for 48 h, and cell viability was determined by MTT assay. As shown in [Table 2], among nine tested compounds, quassinoids 2 and 3 were found relatively to have strongest antiproliferative activities against all assayed cancer cell lines. The rest of the compounds including the two new constituents were considered to be inactive against the seven cancer cell lines. Noticeably, 14,15 β-dihydroxyklaineanone (2) and the major quassinoid eurycomanone (3) exhibited potent inhibitory effects on the growth of both leukemia cell lines; when treated with 25 μM, compound 2 inhibited cell growth by 95.1% (HL-60) and 90.8% (Jurkat) while compound 3 inhibited cell growth by 96.0% (HL-60) and 80.2% (Jurkat), respectively. Moreover, both compounds had negligible toxic effect on the viability of the normal skin fibroblast cell line NB1RGB. Taken together, these results suggest that 14,15 β-dihydroxyklaineanone (2) and the major quassinoid eurycomanone (3) are potent antiproliferative compounds against leukemia cells. The results could not be readily explained in terms of the structures of quassinoid derivatives.
Table 2: Cell viability of 1-9 measured by 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide assay using human cancer and normal cell lines

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   Conclusion Top

We have identified nine quassinoids including a new C19 longilactone-type quassinoid glycoside (9) and antiproliferative testing revealed 14,15 β-dihydroxyklaineanone (2) and the major quassinoid eurycomanone (3) as potent preferential antileukemia agents which may be of potential therapeutic use for the leukemia treatment in the future. Further studies on their mechanism of action and in vivo antitumor need to be explored.

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Conflicts of interest

There are no conflicts of interest.

   References Top

Bhat R, Karim AA. Tongkat ali (Eurycoma longifolia Jack): A review on its ethnobotany and pharmacological importance. Fitoterapia 2010;81:669-79.  Back to cited text no. 1
Miyake K, Tezuka Y, Awale S, Li F, Kadota S. Quassinoids from Eurycoma longifolia. J Nat Prod 2009;72:2135-40.  Back to cited text no. 2
Low BS, Das PK, Chan KL. Standardized quassinoid-rich Eurycoma longifolia extract improved spermatogenesis and fertility in male rats via the hypothalamic-pituitary-gonadal axis. J Ethnopharmacol 2013;145:706-14.  Back to cited text no. 3
Lavie D, Jain MK, Kirson I. Terpenoids. Part VI. The complete structure of melianone. J Chem Soc C 1967;1967:1347-51.  Back to cited text no. 4
Itokawa H, Kishi E, Morita H, Takeya K, Iitaka Y. Eurylene, a new squalene-type triterpene from Eurycoma longifolia. Tetrahedron Lett 1991;32:1803-4.  Back to cited text no. 5
Tran TV, Malainer C, Schwaiger S, Atanasov AG, Heiss EH, Dirsch VM, et al. NF-κB inhibitors from Eurycoma longifolia. J Nat Prod 2014;77:483-8.  Back to cited text no. 6
Huu Tung N, Du GJ, Wang CZ, Yuan CS, Shoyama Y. Naphthoquinone components from Alkanna tinctoria (L.) Tausch show significant antiproliferative effects on human colorectal cancer cells. Phytother Res 2013;27:66-70.  Back to cited text no. 7
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Aung HH, Wang CZ, Ni M, Fishbein A, Mehendale SR, Xie JT, et al. Crocin from Crocus sativus possesses significant anti-proliferation effects on human colorectal cancer cells. Exp Oncol 2007;29:175-80.  Back to cited text no. 9
Kawabata K, Tung NH, Shoyama Y, Sugie S, Mori T, Tanaka T. Dietary crocin inhibits colitis and colitis-associated colorectal carcinogenesis in male ICR mice. Evid Based Complement Alternat Med 2012;2012:820415.  Back to cited text no. 10
Uto T, Sakamoto A, Tung NH, Fujiki T, Kishihara K, Oiso S, et al. Anti-Proliferative activities and apoptosis induction by triterpenes derived from Eriobotrya japonica in human leukemia cell lines. Int J Mol Sci 2013;14:4106-20.  Back to cited text no. 11
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Chan KL, Lee SP, Sam TW, Tan SC, Noguchi H, Sankawa U. 13',18-dihydroeurycomanol, a quassinoid from Eurycoma longifolia. Phytochemistry 1991;30:3138-41.  Back to cited text no. 13
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Meng D, Li X, Han L, Zhang L, An W, Li X. Four new quassinoids from the roots of Eurycoma longifolia Jack. Fitoterapia 2014;92:105-10.  Back to cited text no. 17


  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2]

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