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Bioactive triterpenoids from Indonesian medicinal plant Syzygium aqueum

  • Alfinda Novi Kristanti EMAIL logo , Ei Ei Aung , Nanik Siti Aminah , Yoshiaki Takaya , Hnin Thanda Aung and Rico Ramadhan
Published/Copyright: March 10, 2022
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Open Chemistry
From the journal Open Chemistry Volume 20 Issue 1

Abstract

A large common species, Syzygium aqueum, belonging to the genus Syzygium possesses numerous bioactive phytochemical constituents. Moreover, the different parts of this species have been used as folk medicine since centuries ago. In this study, a phytochemical exploration was carried out on the plant’s stem bark. Isolation of the compounds was carried out through the extraction step with some organic solvents, followed by separation and purification using chromatography techniques until the two triterpenoids were isolated from nonpolar and semipolar extracts. Structure elucidation was done using spectroscopic methods. These compounds were identified as alphitolic acid and arjunolic acid. Subsequently, these two compounds were used in anticancer tests against human cancer cells HeLa, T47D, and A549 using colorimetric assay. The result showed that both compounds showed more inhibition of the growth of HeLa and T47D than A549 cancer cells, with the highest activity shown by arjunolic acid against HeLa cell lines.

Keywords: Syzygium aqueum ; alphitolic acid; arjunolic acid; MTT assay; XTT assay

1 Introduction

One of the probable medicament manufacturing countries, Indonesia, between the Pacific and Indian Oceans, is commonly known as a country with the second richest biodiversity of medicinal plants on the earth. Medicinal plants have therapeutic properties or provide beneficial pharmacological effects for the human body. Some examples are given here. The chemical composition of the essential oils extracted from Elaeagnus umbellata Thunb fruit demonstrated antioxidant, anticholinesterase, and antidiabetic activities that could be used as an alternative drug to treat oxidative stress-related diseases [1]. The essential oil of Teucrium stocksianum possesses a strong antinociceptive potential, which is further used as a topical analgesic [2]. The study of Woodwardia unigemmata (Makino) Nakai plant extracts, which were rich in polyphenolic compounds (total phenolic compounds and total flavonoid compounds) with efficient antioxidant activity, also showed remarkable antibacterial activity against plant and animal pathogenic bacteria [3]. The diverse Indonesian medicinal plants have been used as the sources of herbal medicines for the inhibition and treatment of human diseases for several thousand years [4].

The sixteenth largest genus of flowering plants in the Myrtaceae family, Syzygium, comprises about 1,200–1,800 species. Moreover, Syzygium species of tree and shrub types are distributed in tropical areas worldwide, especially Indonesia, Malaysia, Philippines, and Thailand. Some species of Syzygium are widely cultivated for economic importance, edible fruits, spices, flavoring agents, and pharmacological proprieties. Syzygium contains abundant diversity of bioactive phytochemical constituents such as terpenoids, steroids, chalcones, flavonoids, lignans, alkyl phloroglucinols, hydrolysable tannins, and chromone derivatives [5].

A medicinal species of Syzygium found in Indonesia, Syzygium aqueum, is a large common species in this genus found in Malaysia [6]. Fruits, leaves, and roots of this species have been used as folk medicine, especially for antibiotic properties, diabetic treatment, the treatment for a cracked tongue, relieving itches, stomach aches, dysentery, and reducing of swelling, respectively [7,8,9,10,11].

Some researchers were focused on bioactive phytochemical constituents based on the above medicinal values of this plant. Therefore, bioactive phytochemical constituents such as tannins, flavonoids, steroids, triterpenoids, and phenols from leaves and stem bark of this plant have already been reported in some research articles [12,13,14,15,16,17]. These articles also showed that some flavonoids from S. aqueum (leaves) strongly showed antidiabetic properties using α-glucosidase and α-amylase inhibition assays and showed their cytotoxicity against MCF-cell line using 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay. Moreover, some triterpenoids and steroids from S. aqueum (stem bark) were active with high cytotoxicity on HeLa, T47D, and A549 cancer cell lines using MTT and 2,3-bis-(2-methoxy-4-nitro-5-sulfophenyl)-2H-tetrazolium-5-carboxanilide (XTT) assays.

Based on the literature study, the stem bark of S. aqueum was designated for this research. Primarily, some extracts of stem bark of S. aqueum were separated to collect bioactive constituents with vacuum liquid chromatography and column chromatography. The structure of isolated compounds was identified with spectroscopic methods, including UV, Fourier transform infrared (FTIR), nuclear magnetic resonance (NMR [1D and 2D]), and HR-DART-MS. After this, their anticancer activity was determined with colorimetric assay (MTT and XTT assays). The isolated bioactive constituents were triterpenoid compounds, first isolated from S. aqueum.

2 Materials and methods

2.1 Plant materials

The stem bark of S. aqueum was collected in December 2018 from Wage, Taman, Sidoarjo, East Java, Indonesia. The plant material was identified at the Department of Biology, Faculty of Science and Technology, Universitas Airlangga, and the voucher specimen (UA-MSa050918) was deposited at the Herbarium of Universitas Airlangga, Laboratory of Biosystematic, Department of Biology, Faculty of Science and Technology, Universitas Airlangga. The collected stem bark was cleaned, chopped, and crushed into small pieces of coarse powder.

2.2 Instrumentations

A polarimeter with φ 3.5 mm diameter (cell size) × 100 mm (cell length) was used to measure the specific rotation. For structure elucidation, some of the instruments used are a UV-vis 1800 spectrometer (Shimadzu), FTIR spectra on a Tracer-100 spectrophotometer (Shimadzu), NMR spectra on Bruker Avance III HD 600, and HR-DART-MS on an Exactive Plus Orbitrap DART Mass Spectrometer. Enzyme-linked immunosorbent assay (ELISA) reader was used for the anticancer test.

2.3 General procedure

For extraction, fractionation, isolation, and purification of a sample, organic solvents such as n-hexane (n-Hex), ethyl acetate (EtOAc), dichloromethane (DCM), and methanol (MeOH) were used. In analytical thin-layer chromatography (TLC), a precoated silica gel 60 F254 (Merck) was used and an anisaldehyde-sulfuric acid reagent was sprayed on a TLC plate for visualization. Silica gel 60 (700–200 mesh ASTM) was applied for column chromatography. Then, vacuum liquid chromatography (VLC) was performed using Kieselgel 60 (F254, Merck). The melting point of pure compounds was measured on a Fisher-Johns melting point apparatus (Stuart SMP30). Spectroscopic methods, including UV-vis, IR, NMR, and MS, were used to determine the structure of isolated compounds. An anticancer test was carried out using MTT and XTT reagents (colorimetric assay), and the absorbance for an anticancer test was recorded on an ELISA reader.

2.4 Extraction and isolation

At room temperature, 2 kg of coarse powder of stem bark was extracted with a polar solvent (MetOH, 40 L) for 3 × 24 h. This crude extract (450 g) was then mentioned to partition with a nonpolar solvent (n-hexane). It was separated into a nonpolar fraction and a methanol fraction. Then, 400 mL of aqueous was added to methanol fractions before partitioning with a semipolar solvent, EtOAc. After this, this mixture was separated into a semipolar fraction and an aqueous methanol residue. First, the nonpolar fraction was chromatographed with gradient polarity solvents, n-Hex:EtOAc. Separation procedure was carried out for three times using column chromatography to obtain a pure compound. Compound 1 (30 mg) was acquired from a fraction eluted with n-Hex:EtOAc = 7:3. The semipolar fraction was separated by VLC using gradient solvent mixtures of n-Hex:DCM and DCM:EtOAc. Separation procedure using column chromatography was carried out twice to obtain a pure compound, Compound 2 (50 mg), that was eluted with DCM:EtOAc = 6:4.

2.5 Anticancer activity

2.5.1 Cell culture

Three cancer cell lines, HeLa (cervical cancer), T47D (breast cancer), and A459 (lung cancer), were obtained from American Type Culture Collection. Cells were cultured at 37°C in a CO2 incubator for 24 h and 100% humidity in medium supplemented with 10% FBS, 1% l-glutamine, and 1% penicillin/streptomycin. The cell culture process was carried out in the Cancer Chemoprevention Research Center, Faculty of Pharmacy at Universitas Gadjah Mada, Indonesia and in Physic Laboratory, Faculty of Science of University Putra Malaysia (UPM), Malaysia.

2.5.2 MTT assay

An anticancer test of pure compounds was performed using MTT assay. Cells were cultured in 96 well plates at 213 × 104 cell/well density and were incubated at 37°C in a CO2 incubator for 24 h. The cells were then treated with 100 µL of the prepared sample with different concentration series (1.5625–100 µg/mL) at 37°C in a CO2 incubator for 24 h. As much as 100 µL of the MTT reagent (50 mg in 10 mL of PBS) was filled in each well after incubation, and it was incubated again at 37°C in a CO2 incubator for 2–4 h until purple formazan crystals are formed. After the crystal formation, cells were observed with a microscope, and 100 µL of 10% SDS stopper in 0.1 N HCl was added, and it was kept in a dark place overnight (room temperature). Next, the plate’s absorbance value was read at a wavelength of 560 nm by using an ELISA reader [18,19].

2.5.3 XTT assay

The anticancer test was carried out using XTT assay. Cells were seeded (104–105 cells/well) into 96 well plates and were incubated at 37°C in a CO2 incubator for 24 h. As much as 100 µL of the prepared sample with various concentrations (1.5625–100 µg/mL) was inserted to treat cancer cells. The plate was incubated at 37°C in a CO2 incubator for 24 h. And then, PMS solution (10 mM PMS solution and PBS (3 mg PMS + 1 mL PBS)) was prepared and 10 µL of this solution was added in 4 mL of XTT (4 mg of XTT dissolved in 4 mL of 37°C cells culture medium). After incubation, 25 µL of the XTT reagent (XTT/PMS solution) was filled in each well. After this, it was incubated for 2–4 h in a CO2 incubator at 37°C until the changing of the orange formazan. The next step was to read the absorbance value at a wavelength of 450 nm using an ELISA reader [19,20]. Each experiment was carried out in triplicate, and the number of viable cells was calculated using the following formula:

% Cell viability = Absorbance of treatment − Absorbance of media Absorbance of negative control − Absorbance of media × 100 % .

3 Results and discussion

3.1 Isolation of compounds and structure elucidation

Nonpolar and semipolar fractions of S. aqueum (stem bark) gave one bioactive compound each, Compound 1 and Compound 2. Structures of these compounds were identified and elucidated using spectroscopic methods.

Compound 1 was acquired as white powder, [ α ] D 25 -9, m.p. 279–280°C. According to the HR-DART-MS spectrum, the molecular formula was C30H48O4, m/z 471.3462 [M–H]− (calc. mass for C30H48O4–H−, m/z 471.3474). The UV spectrum in MeOH was displayed at λ max 182 nm. In the FTIR spectrum (KBr), hydroxyl group (3,423 cm−1), symmetric and asymmetric sp3 C–H stretching (2,941–1,870 cm−1), carbonyl acid group (1,699 cm−1), CH2 bending (1,456 cm−1), and CH3 bending (1,381 cm−1) were recorded. The proton signals, both δ H: 3.60 ppm (H-2β) and δ H: 2.89 ppm (H-3α), were suggested as carbinol methine protons, which coupled each other according to the Double Quantum Filtered-COSY (DFQ-COSY) experiment and relative configuration indicated trans configuration due to the 9.6 Hz coupling constant of H-3α. Nuclear Overhauser Effect Spectroscopy (NOESY) cross-peaks of H-3α and H-5α confirmed the presence of the trans-AB ring. Six methyl protons possessed some Heteronuclear Multiple Bond Correlation (HMBC) such as H-23 (δ H: 0.99 ppm) and C-24 (δ C: 15.8 ppm), H-24 (δ H: 0.78 ppm) and H-25 (δ H: 0.92 ppm) and C-5 (δ C: 55.2 ppm), H-26 (δ H: 0.97 ppm) and C-7 (δ C: 1.43 ppm), and H-27 (δ H: 1.01 ppm) and C-14 (δ C: 42.3 ppm). Two vinylic protons (H-29) were observed at δ H: 4.60 ppm and δ H: 4.71 ppm. Their positions were confirmed by HMBC between these two H-29 protons with C-19 (δ C: 47.1 ppm) and C-30 (δ C: 18.2 ppm). Based on HSQC experiments, two carbinol methine carbons (R2-CH-OH) gave correlations H-2β-C-2 (δ C: 68.4 ppm) and H-3α–C-3 (δ C: 83.0 ppm). A vinylic group was appeared at δ C: 108.7 ppm (C-29) and δ C: 150.6 ppm (C-20) in the 13C NMR spectrum. The C-20 was supposed to be a quaternary carbon of the olefinic system. And then, the C-29 was suggested as methylene carbon of the same olefinic system (═CH2), which were connected by two protons [δ H: 4.60 ppm (H-29) and δ H: 4.71 ppm (H-29)] through the HSQC spectrum. Chemical shift of the carbonyl group appeared at δ C: 178.7 ppm (C-28) in the 13C NMR spectrum. In the HMBC spectrum, C-28 showed correlations with H-18 (δ H: 1.61 ppm) and H-22 (δ H: 1.43 ppm). Furthermore, the positions of quaternary carbons were verified based on the HMBC spectrum by observing the correlations of H-23 and H-24 to C-4 (δ C: 39.1 ppm), H-27 to C-8 (δ C: 40.6 ppm), H-1 to C-10 (δ C: 38.1 ppm), H-15 to C-14 (δ C: 42.3 ppm), and H-16 to C-17 (δ C: 56.1 ppm). The remaining peaks at δ C: 27.7 ppm (C-23), 15.8 ppm (C-24), 16.5 ppm (C-25), 15.3 ppm (C-26), 13.7 ppm (C-27), and 18.2 ppm (C-30) were suggested as primary carbons through Distortionless Enhancement by Polarization Transfer (DEPT) 135 information. Moreover, six methyl carbons, ten methylene carbons, seven methine carbons, and seven quaternary carbons were confirmed with the DEPT experiment (DEPT 90 and DEPT 135). Therefore, Compound 1 was verified as alphitolic acid according to the above data. DQF-COSY (1H-1H), NOESY (1H-1H), and HMBC (1H-13C) correlations of the structure are shown in Figure 1, as well as spectral data of both 1H NMR (600 MHz, methanol-d 4) with their coupling constant and 13C NMR (150 MHz, methanol-d 4) were compared with the literature data in Table 1.

Figure 1 DQF-COSY, NOESY, and HMBC correlations of alphitolic acid from S. aqueum.
Figure 1

DQF-COSY, NOESY, and HMBC correlations of alphitolic acid from S. aqueum.

Table 1

NMR spectra of alphitolic acid by comparing to literature

Position DEPT Experiment Literature [21]
δ C (ppm) δ H (ppm) {mult, J (Hz)} δ C (ppm) δ H (ppm) {mult, J (Hz)}
1 CH2 46.9 0.82 (1H, m) 46.5 — —
2.00 (1H, m)
2 CH 68.4 3.60 (1H, m) 68.6 3.46 (1H, dd, J = 4.0, 9.5 Hz)
3 CH 83.0 2.89 (1H, d, J = 9.6 Hz) 83.2 2.74 (1H, d, J = 9.5 Hz)
4 C 39.1 — 40.6 —
5 CH 55.2 0.82 (1H, m) 55.2 —
6 CH2 18.1 1.54 (1H, m) 18.2 —
1.43 (1H, m)
7 CH2 34.1 1.43 (2H, m) 34.1 —
8 C 40.6 — 39.2 —
9 CH 50.6 1.39 (1H, m) 50.3 —
10 C 38.1 — 38.2 —
11 CH2 20.8 1.43 (2H, m) 20.9 —
12 CH2 25.4 1.73 (1H, m) 25.3 1.52 (1H, m)
1.08 (1H, m) 1.64 (1H, m)
13 CH 38.2 2.32 (1H, m) 38.1 —
14 C 42.3 — 40.6 —
15 CH2 29.4 1.30 (1H, m) 30.4 —
1.15 (1H, m)
16 CH2 32.0 0.90 (2H, m) 32.1 —
17 C 56.1 — 56.1 —
18 CH 49.1 1.61 (1H, m) 48.1 —
19 CH 47.1 3.03 (1H, m) 48.9 2.86 (1H, m)
20 C 150.6 — 150.7 —
21 CH2 30.3 1.39 (2H, m) 29.5 —
22 CH2 36.7 1.91 (1H, m) 37.0 —
1.43 (1H, m)
23 CH3 27.7 0.99 (3H, s) 28.2 0.81 (3H, s)
24 CH3 15.8 0.78 (3H, s) 16.4 0.60 (3H, s)
25 CH3 16.5 0.92 (3H, s) 17.1 0.71 (3H, s)
26 CH3 15.3 0.97 (3H, s) 15.7 0.80 (3H, s)
27 CH3 13.7 1.01 (3H, s) 14.5 0.75 (3H, s)
28 COOH 178.7 — 179.3 —
29 CH2 108.7 4.60 (1H, s) 109.4 4.42 (1H, s)
4.71 (1H, s) 4.54 (1H, s)
30 CH3 18.2 1.70 (3H, s) 19.1 1.51 (3H, s)

Compound 2 was acquired as white powder, m.p. 338–340°C. The UV spectrum in MeOH appeared at λ max 220 nm. In FTIR spectra (KBr), hydroxyl group (3,371 cm−1), asymmetric and symmetric sp3 C–H stretching vibration (2,941 cm−1), carbonyl (COOH) group (1,693 cm−1), CH2 bending (1,462 cm−1) and CH3 bending (1,388–1,365 cm−1), and C–O stretching (1,049 cm−1) were observed. In the 1H NMR spectrum, four carbinol protons were shown at δ H: 3.68 ppm (H-2β), δ H: 3.35 ppm (H-3α), δ H: 3.27 ppm (H-23), and δ H: 3.50 ppm (H-23). The H-3α and H-2β were coupled through the DQF-COSY spectrum. The trans configuration was confirmed due to the 10.2 Hz coupling constant of H-3α and NOESY correlation of H-2β and H-24β. Thus, H-23 was correlated to C-3 (δ C: 76.8 ppm) according to the HMBC spectrum. The olefinic protons were shown at δ H: 5.25 ppm (H-12) and coupled to H-11 (δ H: 1.95 ppm) in the DQF-COSY spectrum. Moreover, six methyl protons were appeared at δ H: 0.70 ppm (H-24), 1.03 ppm (H-25), 0.82 ppm (H-26), 1.18 ppm (H-27), 0.91 ppm (H-29), and 0.94 ppm (H-30). These methyl protons have correlations observed on the HMBC spectrum, especially between H-24 and C-23 (δ C: 65.0 ppm), H-26 and C-8 (δ C: 39.2 ppm) and C-14 (δ C: 41.6 ppm), H-27 and C-8 (δ C: 39.2 ppm), C-14 (δ C: 41.6 ppm) and C-15 (δ C: 27.4 ppm), and H-29 and H-30 and C-20 (δ C: 30.2 ppm). On the 13C NMR spectrum, the three carbinol carbons were observed at δ C: 68.8 ppm (C-2), 76.8 ppm (C-3), and 65.0 ppm (C-23). The carbons of C-2 and C-3 were identified as methine alcohol (R2-CH-OH), and C-23 was suggested as methylene alcohol (R-CH2-OH) according to DEPT (DEPT 135 and DEPT 90) experiments. Chemical shifts at δ C: 180.7 ppm in the 13C NMR spectrum indicated the presence of the carboxylic acid functional group (C-28), which was correlated with H-18 (δ H: 2.86 ppm) on the HMBC spectrum. The double bond carbons at positions C-12 and C-13 were appeared at δ C: 121.9 ppm (methine carbon) and δ C: 144.1 ppm (quaternary carbon). The remaining quaternary carbon signals were shown at δ C: 42.7 ppm (C-4), 39.2 ppm (C-8), 41.6 ppm (C-14), 46.3 ppm (C-17), and 30.2 ppm (C-20). Carbon signals at δ C: 12.4 ppm (C-24), 16.2 ppm (C-25), 16.4 ppm (C-26), 25.1 ppm (C-27), 32.1 ppm (C-29), and 22.6 ppm (C-30) were suggested as primary carbons. The presence of eight quaternary carbons, six methine carbons, ten methylene carbons, and six methyl carbons was also confirmed by the DEPT experiment. According to the above data, the structure of Compound 2 was verified as arjunolic acid, and its molecular formula was C30H48O5. DQF-COSY (1H–1H), NOESY (1H–1H), and HMBC (1H–13C) correlations of the structure are demonstrated in Figure 2. And then, the spectral data of both 1H NMR (600 MHz, methanol-d 4) with their coupling constants and 13C NMR (150 MHz, methanol-d 4) are shown in Table 2, completed with the reported literature data.

Figure 2 DQF-COSY, NOESY, and HMBC correlations of arjunolic acid from S. aqueum.
Figure 2

DQF-COSY, NOESY, and HMBC correlations of arjunolic acid from S. aqueum.

Table 2

NMR spectra of arjunolic acid by comparing to literature

Position DEPT Experiment Literature [22]
δ C (ppm) δ H (ppm) (mult, J in Hz) δ C (ppm) δ H (ppm) (mult, J in Hz)
1 CH2 46.5 0.89 (1H, m) 47.8 —
1.95 (1H, m)
2 CH 68.8 3.68 (1H, m) 69.6 3.66 (1H, m)
3 CH 76.8 3.35 (1H, d, J = 10.2 Hz) 78.1 3.36 (1H, m)
4 C 42.7 — 43.0 —
5 CH 46.8 1.28 (1H, m) 48.3 —
6 CH2 17.7 1.39 (1H, m) 19.1 —
1.48 (1H, m)
7 CH2 32.0 1.28 (1H, m) 33.8 —
1.64 (1H, m)
8 C 39.2 — 40.7 —
9 CH 47.6 1.69 (1H, m) 48.1 —
10 C 37.7 — 38.5 —
11 CH2 23.2 1.95 (1H, m) 24.0 —
1.24 (1H, m)
12 CH 121.9 5.25 (1H, m) 123.4 5.23 (1H, m)
13 C 144.1 — 144.3 —
14 C 41.6 — 42.7 —
15 CH2 27.4 1.07 (1H, m) 29.1 —
1.78 (1H, m)
16 CH2 22.6 1.59 (1H, m) 24.4 —
2.24 (1H, m)
17 C 46.3 — 46.6 —
18 CH 41.4 2.86 (1H, dd, J = 3.9, 13.7 Hz) 43.3 —
19 CH2 45.9 1.13 2H (m) 44.1 —
20 C 30.2 — 31.6 —
21 CH2 33.5 1.39 (1H, m) 34.8 —
1.21 (1H, m)
22 CH2 32.5 1.75 (1H, m) 33.5 —
1.54 (1H, m)
23 CH2 65.0 3.50 (1H, d, J = 11.0 Hz) 66.2 3.50 (1H, s)
3.27 (1H, d, J = 11.0 Hz) 3.31 (1H, s)
24 CH3 12.4 0.70 (3H, s) 13.9 0.69 (3H, s)
25 CH3 16.2 1.03 (3H, s) 17.7 0.81 (3H, s)
26 CH3 16.4 0.82 (3H, s) 17.5 0.91 (3H, s)
27 CH3 25.1 1.18 (3H, s) 26.8 1.17 (3H, s)
28 COOH 180.7 — 181.8 —
29 CH3 32.1 0.91 (3H, s) 25.3 1.03 (3H, s)
30 CH3 22.6 0.94 (3H, s) 24.6 0.94 (3H, s)

3.2 Anticancer activity

Isolated compounds in this study were evaluated their anticancer activity against the human cancer cells as HeLa (cervical cancer), T47D (breast cancer), and A549 (lung cancer) cell lines using MTT and XTT assays, which are the colorimetric measurement of cell viability. In the present anticancer activity test, doxorubicin was used as the standard. The pure compound is deemed highly toxic if the half-maximal inhibitory concentration (IC50) is ≤4 µg/mL and toxic if the IC50 is ≤20 µg/mL. The compound is moderately toxic if the IC50 is 20–100 g/mL and if IC50 above 100 g/mL is recommended as nontoxic [23,24].

Based on anticancer activity data obtained, alphitolic acid was suggested as a toxic compound against HeLa and T47D cell lines, with IC50 being 16.12 µg/mL and 7.37 µg/mL, respectively. However, its activity against the A549 cell line was presented as moderate inhibition (IC50 = 84.41 µg/mL). Moreover, arjunolic acid with an IC50 of 6.74 µg/mL was considered a toxic compound against HeLa cell lines. Arjunolic acid was a moderate compound against the T47D cancer cell line with an IC50 of 27.15 µg/mL, although it was a nontoxic compound against the A549 cancer cell line. According to the data mentioned earlier, the two types of triterpenoids inhibited higher toxicity against HeLa and T47D cell lines than the A549 cell line, and their activities may improve to obtain the natural origin drug from this species. The IC50 values of the two compounds are listed in Table 3.

Table 3

Anticancer activity against HeLa, T47D, and A549 cell lines

Compound name MTT assay (IC50 ± SD µg/mL) XTT assay (IC50 ± SD µg/mL)
HeLa T47D A549
Alphitolic acid 16.12 ± 0.681 7.37 ± 0.388 84.41 ± 0.048
Arjunolic acid 6.74 ± 0.015 27.51 ± 0.036 168.22 ± 0.090
Doxorubicin 2.67 ± 0.25 0.035 ± 0.012 NT

The meaning of NT is not test, SD = standard deviation.

Many terpene compounds have interesting bioactivities, so it is necessary to carry out other activity tests such as agar-well diffusion methods to evaluate the minimum inhibitory concentrations, minimum bactericidal concentration, IC50, and zone of inhibitions that could determine the potential antimicrobial and antifungal efficacy. The significant antioxidant potential could be evaluated through 1,1-diphenyl-2-picryl-hydrazyl and 2,2'-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) assays. The inhibiting of the α-glucosidase represents an antidiabetic activity that also could be visualized through molecular docking simulations. The effective anti-inflammatory agent could be determined via the carrageenan-induced assay, while an appreciable analgesic activity could be observed through the acetic acid-induced writhing bioassay [25].

4 Conclusion

This study reports the success of isolating two bioactive triterpenoid compounds from stem bark of S. aqueum, an Indonesian medicinal plant, namely alphitolic acid and arjunolic acid. These two isolated triterpenoids were significantly toxic against cervical cancer and breast cancer, shown by small IC50 values. Based on this result, we recommended continuing exploring the potential of this plant so that it can be used as a source of secondary metabolite compounds with interesting bioactivity.

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Acknowledgments

All authors express big thanks to the Indonesian Ministry of Education and Culture for the Research Grant (Penelitian Dasar, 2021), to the Faculty of Pharmacy, Meijo University, Tempaku, Nagoya, Japan, for NMR and MS data, to the Faculty of Pharmacy, Gajah Mada University, Indonesia, and the Faculty of Science, UPM, Malaysia for an anticancer test.

  1. Funding information: This work was supported by the Indonesian Ministry of Education and Culture for the Research Grant (Penelitian Dasar, 2021).

  2. Author contributions: Alfinda Novi Kristanti: conceptualization, formal analysis, funding acquisition, investigation, resources, supervision, and writing – review and editing; Ei Ei Aung: data curation, formal analysis, investigation, project administration, validation, visualization, and writing – original draft; Nanik Siti Aminah: conceptualization, formal analysis, funding acquisition, methodology, resources, and supervision; Yoshiaki Takaya: data curation, resources, software, validation, and visualization; Hnin Thanda Aung: data curation, formal analysis, methodology, and supervision; and Rico Ramadhan: data curation, formal analysis, software, and validation.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: All data generated or analyzed during this study are included in this published article [and its supplementary information files].

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Received: 2021-12-23
Revised: 2022-02-09
Accepted: 2022-02-15
Published Online: 2022-03-10

© 2022 Alfinda Novi Kristanti et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/chem-2022-0138
Keywords for this article
Syzygium aqueum; alphitolic acid; arjunolic acid; MTT assay; XTT assay
Creative Commons
BY 4.0

Articles in the same Issue

  1. Regular Articles
  2. Photocatalytic degradation of Rhodamine B in aqueous phase by bimetallic metal-organic framework M/Fe-MOF (M = Co, Cu, and Mg)
  3. Assessment of using electronic portal imaging device for analysing bolus material utilised in radiation therapy
  4. A detailed investigation on highly dense CuZr bulk metallic glasses for shielding purposes
  5. Simulation of gamma-ray shielding properties for materials of medical interest
  6. Environmental impact assesment regulation applications and their analysis in Turkey
  7. Sample age effect on parameters of dynamic nuclear polarization in certain difluorobenzen isomers/MC800 asphaltene suspensions
  8. Passenger demand forecasting for railway systems
  9. Design of a Robust sliding mode controller for bioreactor cultures in overflow metabolism via an interdisciplinary approach
  10. Gamma, neutron, and heavy charged ion shielding properties of Er3+-doped and Sm3+-doped zinc borate glasses
  11. Bridging chiral de-tert-butylcalix[4]arenes: Optical resolution based on column chromatography and structural characterization
  12. Petrology and geochemistry of multiphase post-granitic dikes: A case study from the Gabal Serbal area, Southwestern Sinai, Egypt
  13. Comparison of the yield and purity of plasma exosomes extracted by ultracentrifugation, precipitation, and membrane-based approaches
  14. Bioactive triterpenoids from Indonesian medicinal plant Syzygium aqueum
  15. Investigation of the effects of machining parameters on surface integrity in micromachining
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  19. Statistical analysis on the radiological assessment and geochemical studies of granite rocks in the north of Um Taghir area, Eastern Desert, Egypt
  20. Two new polypodane-type bicyclic triterpenoids from mastic
  21. Structural, physical, and mechanical properties of the TiO2 added hydroxyapatite composites
  22. Tribological properties and characterization of borided Co–Mg alloys
  23. Studies on Anemone nemorosa L. extracts; polyphenols profile, antioxidant activity, and effects on Caco-2 cells by in vitro and in silico studies
  24. Mechanical properties, elastic moduli, transmission factors, and gamma-ray-shielding performances of Bi2O3–P2O5–B2O3–V2O5 quaternary glass system
  25. Cyclic connectivity index of bipolar fuzzy incidence graph
  26. The role of passage numbers of donor cells in the development of Arabian Oryx – Cow interspecific somatic cell nuclear transfer embryos
  27. Mechanical property evaluation of tellurite–germanate glasses and comparison of their radiation-shielding characteristics using EPICS2017 to other glass systems
  28. Molecular screening of ionic liquids for CO2 absorption and molecular dynamic simulation
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  30. Iminodisuccinic acid enhances antioxidant and mineral element accumulation in young leaves of Ziziphus jujuba
  31. Cytotoxic activity of guaiane-type sesquiterpene lactone (deoxycynaropicrin) isolated from the leaves of Centaurothamnus maximus
  32. Effects of welding parameters on the angular distortion of welded steel plates
  33. Simulation of a reactor considering the Stamicarbon, Snamprogetti, and Toyo patents for obtaining urea
  34. Effect of different ramie (Boehmeria nivea L. Gaud) cultivars on the adsorption of heavy metal ions cadmium and lead in the remediation of contaminated farmland soils
  35. Impact of a live bacterial-based direct-fed microbial (DFM) postpartum and weaning system on performance, mortality, and health of Najdi lambs
  36. Anti-tumor effect of liposomes containing extracted Murrayafoline A against liver cancer cells in 2D and 3D cultured models
  37. Physicochemical properties and some mineral concentration of milk samples from different animals and altitudes
  38. Copper(ii) complexes supported by modified azo-based ligands: Nucleic acid binding and molecular docking studies
  39. Diagnostic and therapeutic radioisotopes in nuclear medicine: Determination of gamma-ray transmission factors and safety competencies of high-dense and transparent glassy shields
  40. Calculation of NaI(Tl) detector efficiency using 226Ra, 232Th, and 40K radioisotopes: Three-phase Monte Carlo simulation study
  41. Isolation and identification of unstable components from Caesalpinia sappan by high-speed counter-current chromatography combined with preparative high-performance liquid chromatography
  42. Quantification of biomarkers and evaluation of antioxidant, anti-inflammatory, and cytotoxicity properties of Dodonaea viscosa grown in Saudi Arabia using HPTLC technique
  43. Characterization of the elastic modulus of ceramic–metal composites with physical and mechanical properties by ultrasonic technique
  44. GC-MS analysis of Vespa velutina auraria Smith and its anti-inflammatory and antioxidant activities in vitro
  45. Texturing of nanocoatings for surface acoustic wave-based sensors for volatile organic compounds
  46. Insights into the molecular basis of some chalcone analogues as potential inhibitors of Leishmania donovani: An integrated in silico and in vitro study
  47. (1R,2S,5R)-5-Methyl-2-(propan-2-yl)cyclohexyl 4-amino-3-phenylbutanoate hydrochloride: Synthesis and anticonvulsant activity
  48. On the relative extraction rates of colour compounds and caffeine during brewing, an investigation of tea over time and temperature
  49. Characterization of egg shell powder-doped ceramic–metal composites
  50. Rapeseed oil-based hippurate amide nanocomposite coating material for anticorrosive and antibacterial applications
  51. Chemically modified Teucrium polium (Lamiaceae) plant act as an effective adsorbent tool for potassium permanganate (KMnO4) in wastewater remediation
  52. Efficiency analysis of photovoltaic systems installed in different geographical locations
  53. Risk prioritization model driven by success factor in the light of multicriteria decision making
  54. Theoretical investigations on the excited-state intramolecular proton transfer in the solvated 2-hydroxy-1-naphthaldehyde carbohydrazone
  55. Mechanical and gamma-ray shielding examinations of Bi2O3–PbO–CdO–B2O3 glass system
  56. Machine learning-based forecasting of potability of drinking water through adaptive boosting model
  57. The potential effect of the Rumex vesicarius water seeds extract treatment on mice before and during pregnancy on the serum enzymes and the histology of kidney and liver
  58. Impact of benzimidazole functional groups on the n-doping properties of benzimidazole derivatives
  59. Extraction of red pigment from Chinese jujube peel and the antioxidant activity of the pigment extracts
  60. Flexural strength and thermal properties of carbon black nanoparticle reinforced epoxy composites obtained from waste tires
  61. A focusing study on radioprotective and antioxidant effects of Annona muricata leaf extract in the circulation and liver tissue: Clinical and experimental studies
  62. Clinical comprehensive and experimental assessment of the radioprotective effect of Annona muricata leaf extract to prevent cellular damage in the ileum tissue
  63. Effect of WC content on ultrasonic properties, thermal and electrical conductivity of WC–Co–Ni–Cr composites
  64. Influence of various class cleaning agents for prosthesis on Co–Cr alloy surface
  65. The synthesis of nanocellulose-based nanocomposites for the effective removal of hexavalent chromium ions from aqueous solution
  66. Study on the influence of physical interlayers on the remaining oil production under different development modes
  67. Optimized linear regression control of DC motor under various disturbances
  68. Influence of different sample preparation strategies on hypothesis-driven shotgun proteomic analysis of human saliva
  69. Determination of flow distance of the fluid metal due to fluidity in ductile iron casting by artificial neural networks approach
  70. Investigation of mechanical activation effect on high-volume natural pozzolanic cements
  71. In vitro: Anti-coccidia activity of Calotropis procera leaf extract on Eimeria papillata oocysts sporulation and sporozoite
  72. Determination of oil composition of cowpea (Vigna unguiculata L.) seeds under influence of organic fertilizer forms
  73. Activated partial thromboplastin time maybe associated with the prognosis of papillary thyroid carcinoma
  74. Treatment of rat brain ischemia model by NSCs-polymer scaffold transplantation
  75. Lead and cadmium removal with native yeast from coastal wetlands
  76. Characterization of electroless Ni-coated Fe–Co composite using powder metallurgy
  77. Ferrate synthesis using NaOCl and its application for dye removal
  78. Antioxidant, antidiabetic, and anticholinesterase potential of Chenopodium murale L. extracts using in vitro and in vivo approaches
  79. Study on essential oil, antioxidant activity, anti-human prostate cancer effects, and induction of apoptosis by Equisetum arvense
  80. Experimental study on turning machine with permanent magnetic cutting tool
  81. Numerical simulation and mathematical modeling of the casting process for pearlitic spheroidal graphite cast iron
  82. Design, synthesis, and cytotoxicity evaluation of novel thiophene, pyrimidine, pyridazine, and pyridine: Griseofulvin heterocyclic extension derivatives
  83. Isolation and identification of promising antibiotic-producing bacteria
  84. Ultrasonic-induced reversible blood–brain barrier opening: Safety evaluation into the cellular level
  85. Evaluation of phytochemical and antioxidant potential of various extracts from traditionally used medicinal plants of Pakistan
  86. Effect of calcium lactate in standard diet on selected markers of oxidative stress and inflammation in ovariectomized rats
  87. Identification of crucial salivary proteins/genes and pathways involved in pathogenesis of temporomandibular disorders
  88. Zirconium-modified attapulgite was used for removing of Cr(vi) in aqueous solution
  89. The stress distribution of different types of restorative materials in primary molar
  90. Reducing surface heat loss in steam boilers
  91. Deformation behavior and formability of friction stir processed DP600 steel
  92. Synthesis and characterization of bismuth oxide/commercial activated carbon composite for battery anode
  93. Phytochemical analysis of Ziziphus jujube leaf at different foliar ages based on widely targeted metabolomics
  94. Effects of in ovo injection of black cumin (Nigella sativa) extract on hatching performance of broiler eggs
  95. Separation and evaluation of potential antioxidant, analgesic, and anti-inflammatory activities of limonene-rich essential oils from Citrus sinensis (L.)
  96. Bioactivity of a polyhydroxy gorgostane steroid from Xenia umbellata
  97. BiCAM-based automated scoring system for digital logic circuit diagrams
  98. Analysis of standard systems with solar monitoring systems
  99. Structural and spectroscopic properties of voriconazole and fluconazole – Experimental and theoretical studies
  100. New plant resistance inducers based on polyamines
  101. Experimental investigation of single-lap bolted and bolted/bonded (hybrid) joints of polymeric plates
  102. Investigation of inlet air pressure and evaporative cooling of four different cogeneration cycles
  103. Review Articles
  104. Comprehensive review on synthesis, physicochemical properties, and application of activated carbon from the Arecaceae plants for enhanced wastewater treatment
  105. Research progress on speciation analysis of arsenic in traditional Chinese medicine
  106. Recent modified air-assisted liquid–liquid microextraction applications for medicines and organic compounds in various samples: A review
  107. An insight on Vietnamese bio-waste materials as activated carbon precursors for multiple applications in environmental protection
  108. Antimicrobial activities of the extracts and secondary metabolites from Clausena genus – A review
  109. Bioremediation of organic/heavy metal contaminants by mixed cultures of microorganisms: A review
  110. Sonodynamic therapy for breast cancer: A literature review
  111. Recent progress of amino acid transporters as a novel antitumor target
  112. Aconitum coreanum Rapaics: Botany, traditional uses, phytochemistry, pharmacology, and toxicology
  113. Corrigendum
  114. Corrigendum to “Petrology and geochemistry of multiphase post-granitic dikes: A case study from the Gabal Serbal area, Southwestern Sinai, Egypt”
  115. Corrigendum to “Design of a Robust sliding mode controller for bioreactor cultures in overflow metabolism via an interdisciplinary approach”
  116. Corrigendum to “Statistical analysis on the radiological assessment and geochemical studies of granite rocks in the north of Um Taghir area, Eastern Desert, Egypt”
  117. Corrigendum to “Aroma components of tobacco powder from different producing areas based on gas chromatography ion mobility spectrometry”
  118. Corrigendum to “Mechanical properties, elastic moduli, transmission factors, and gamma-ray-shielding performances of Bi2O3–P2O5–B2O3–V2O5 quaternary glass system”
  119. Erratum
  120. Erratum to “Copper(ii) complexes supported by modified azo-based ligands: Nucleic acid binding and molecular docking studies”
  121. Special Issue on Applied Biochemistry and Biotechnology (ABB 2021)
  122. Study of solidification and stabilization of heavy metals by passivators in heavy metal-contaminated soil
  123. Human health risk assessment and distribution of VOCs in a chemical site, Weinan, China
  124. Preparation and characterization of Sparassis latifolia β-glucan microcapsules
  125. Special Issue on the Conference of Energy, Fuels, Environment 2020
  126. Improving the thermal performance of existing buildings in light of the requirements of the EU directive 2010/31/EU in Poland
  127. Special Issue on Ethnobotanical, Phytochemical and Biological Investigation of Medicinal Plants
  128. Study of plant resources with ethnomedicinal relevance from district Bagh, Azad Jammu and Kashmir, Pakistan
  129. Studies on the chemical composition of plants used in traditional medicine in Congo
  130. Special Issue on Applied Chemistry in Agriculture and Food Science
  131. Strip spraying technology for precise herbicide application in carrot fields
  132. Special Issue on Pharmacology and Metabolomics of Ethnobotanical and Herbal Medicine
  133. Phytochemical profiling, antibacterial and antioxidant properties of Crocus sativus flower: A comparison between tepals and stigmas
  134. Antioxidant and antimicrobial properties of polyphenolics from Withania adpressa (Coss.) Batt. against selected drug-resistant bacterial strains
  135. Integrating network pharmacology and molecular docking to explore the potential mechanism of Xinguan No. 3 in the treatment of COVID-19
  136. Chemical composition and in vitro and in vivo biological assortment of fixed oil extracted from Ficus benghalensis L.
  137. A review of the pharmacological activities and protective effects of Inonotus obliquus triterpenoids in kidney diseases
  138. Ethnopharmacological study of medicinal plants in Kastamonu province (Türkiye)
  139. Protective effects of asperuloside against cyclophosphamide-induced urotoxicity and hematotoxicity in rats
  140. Special Issue on Essential Oil, Extraction, Phytochemistry, Advances, and Application
  141. Identification of volatile compounds and antioxidant, antibacterial, and antifungal properties against drug-resistant microbes of essential oils from the leaves of Mentha rotundifolia var. apodysa Briq. (Lamiaceae)
  142. Phenolic contents, anticancer, antioxidant, and antimicrobial capacities of MeOH extract from the aerial parts of Trema orientalis plant
  143. Chemical composition and antimicrobial activity of essential oils from Mentha pulegium and Rosmarinus officinalis against multidrug-resistant microbes and their acute toxicity study
  144. Special Issue on Marine Environmental Sciences and Significance of the Multidisciplinary Approaches
  145. An insightful overview of the distribution pattern of polycyclic aromatic hydrocarbon in the marine sediments of the Red Sea
  146. Antifungal–antiproliferative norcycloartane-type triterpenes from the Red Sea green alga Tydemania expeditionis
  147. Solvent effect, dipole moment, and DFT studies of multi donor–acceptor type pyridine derivative
  148. An extensive assessment on the distribution pattern of organic contaminants in the aerosols samples in the Middle East
  149. Special Issue on 4th IC3PE
  150. Energetics of carboxylic acid–pyridine heterosynthon revisited: A computational study of intermolecular hydrogen bond domination on phenylacetic acid–nicotinamide cocrystals
  151. A review: Silver–zinc oxide nanoparticles – organoclay-reinforced chitosan bionanocomposites for food packaging
  152. Green synthesis of magnetic activated carbon from peanut shells functionalized with TiO2 photocatalyst for Batik liquid waste treatment
  153. Coagulation activity of liquid extraction of Leucaena leucocephala and Sesbania grandiflora on the removal of turbidity
  154. Hydrocracking optimization of palm oil over NiMoO4/activated carbon catalyst to produce biogasoline and kerosine
  155. Special Issue on Pharmacology and metabolomics of ethnobotanical and herbal medicine
  156. Cynarin inhibits PDGF-BB-induced proliferation and activation in hepatic stellate cells through PPARγ
  157. Special Issue on The 1st Malaysia International Conference on Nanotechnology & Catalysis (MICNC2021)
  158. Surfactant evaluation for enhanced oil recovery: Phase behavior and interfacial tension
  159. Topical Issue on phytochemicals, biological and toxicological analysis of aromatic medicinal plants
  160. Phytochemical analysis of leaves and stems of Physalis alkekengi L. (Solanaceae)
  161. Phytochemical and pharmacological profiling of Trewia nudiflora Linn. leaf extract deciphers therapeutic potentials against thrombosis, arthritis, helminths, and insects
  162. Pergularia tomentosa coupled with selenium nanoparticles salvaged lead acetate-induced redox imbalance, inflammation, apoptosis, and disruption of neurotransmission in rats’ brain
  163. Protective effect of Allium atroviolaceum-synthesized SeNPs on aluminum-induced brain damage in mice
  164. Mechanism study of Cordyceps sinensis alleviates renal ischemia–reperfusion injury
  165. Plant-derived bisbenzylisoquinoline alkaloid tetrandrine prevents human podocyte injury by regulating the miR-150-5p/NPHS1 axis
  166. Network pharmacology combined with molecular docking to explore the anti-osteoporosis mechanisms of β-ecdysone derived from medicinal plants
  167. Chinese medicinal plant Polygonum cuspidatum ameliorates silicosis via suppressing the Wnt/β-catenin pathway
  168. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part I
  169. Investigation of improved optical and conductivity properties of poly(methyl methacrylate)–MXenes (PMMA–MXenes) nanocomposite thin films for optoelectronic applications
  170. Special Issue on Applied Biochemistry and Biotechnology (ABB 2022)
  171. Model predictive control for precision irrigation of a Quinoa crop
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