Hepatoprotection and Phytochemistry of the Vietnamese Herbs <i>Cleome chelidonii</i> and <i>Cleome viscosa</i> Stems

Phan, Nhat Minh; Tuoi Do, Thi Hong; Tuyen Nguyen, Le Thanh; Nguyen, Trong Tuan; Ngo, Quoc Luan; Tran, Trong Duc; Nguyen, Quan Hien; Chi Huynh, Bui Linh; Ky Nguyen, Diep Xuan; Bui, Trong Dat; Mai, Dinh Tri; Nguyen, Tan Phat

doi:https://doi.org/10.1155/2021/5578667

Journal of Chemistry

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Abstract Introduction Materials and Methods Results and Discussion Conclusions Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2021 | Article ID 5578667 | https://doi.org/10.1155/2021/5578667

Hepatoprotection and Phytochemistry of the Vietnamese Herbs Cleome chelidonii and Cleome viscosa Stems

Nhat Minh Phan,^1,2Thi Hong Tuoi Do,³Le Thanh Tuyen Nguyen,⁴Trong Tuan Nguyen,⁵Quoc Luan Ngo,⁵Trong Duc Tran,⁶Quan Hien Nguyen,⁷Bui Linh Chi Huynh,⁸Diep Xuan Ky Nguyen,²Trong Dat Bui,²Dinh Tri Mai,^1,9and Tan Phat Nguyen^1,9

Academic Editor: José Morillo

Received12 Jan 2021

Revised07 Apr 2021

Accepted10 Apr 2021

Published19 Apr 2021

Abstract

The study aims to determine the hepatoprotective effect of n-hexane, ethyl acetate, and methanol extracts of the leaves and stems of two Cleome species against carbon tetrachloride- (CCl₄-) induced liver toxicity both in vitro using human hepatoma (HepG2) cells and in vivo in rats as well as the hepatoprotective property of all isolated compounds on HepG2. After 72 h of treatment, at the concentrations of 25, 50, and 100 μg/mL, the methanol of C. chelidonii stems (CCSM) ranged from 18.6% to 20.8%, whereas the methanol of C. chelidonii stems (CVSM) increased from 12.3% to 17.2% cell viability. The results show that CCSM and CVSM significantly expressed in vitro hepaprotective activity on HepG2. Therefore, the animals were daily treated with these extracts at the doses of 15, 30, and 45 mg/kg body weight for 5 days, and CCl₄ was injected (2 ml/kg body weight, i.p.) on the 2nd and 3rd days. Levels of aspartate aminotransferase (ALT) and alanine aminotransferase (AST) in the blood were measured and compared to the silymarin control. The treatments with CCSM and CVSM (30, and 45 mg/kg) possessed significant hepatoprotection and were comparable with the activity of silymarin. Further, phytochemical studies of these ones were conducted and led to the identification of eight flavonoids: visconoside A (1), visconoside B (2), quercetin 3-O-β-D-glucopyranoside 7-O-α-L-rhamnopyranoside (3), kaempferol 3-O-β-D-glucopyranoside 7-O-α-L-rhamnopyranoside (4), cleomeside A (5), cleomeside B (6), cleomeside C (7), and quercetin-3-O-[β-D-glucopyranosyl-(1⟶2)]-α-L-rhamnopyranoside 7-O-α-L-rhamnopyranoside (8). Two major flavonoids (1 and 4) displayed significant hepatoprotective property (at the concentration of 100 μM, the prevention percentage values were 66.5% and 74.2%, respectively, compared to the quercetin control, with value of 80.3%).

1. Introduction

The genus Cleome belonging to the Cleomaceae family comprises about 170 species[1]. Five species were found in Vietnam [2]. In the traditional Vietnamese medicine, C. chelidonii is used for treatment of fever, flu, headache, cough, snake bite, and nephritis, whereas C. viscosa is used to treat diarrhea, fever, inflammation, liver diseases, bronchitis, skin diseases, and malarial fever [2]. Pharmacological investigations proved that C. chelidonii possessed antipyretic [3], antihyperglycemic [4], and anthelmintic [5] properties, while C. viscosa expressed anticonvulsant [6], antitumor [7], cytotoxic [8–12], antiangiogenic [12], antimalarial [13], larvicidal [14], antiallergic, diuretic [15], analgesic, antipyretic [16], α-glucosidase, and α-amylase inhibitory [17] activities. Additionally, both species exhibited antimicrobial [9–21], antinociceptive [3, 10, 22, 23], anti-inflammatory [3, 21, 23, 24], and antioxidant activities [5, 8, 9, 12, 14, 25–27].

In vivo study on rats against CCl₄-induced liver injury indicated that hydroalcohol, methanol, ethyl acetate, and hexane extracts of C. chelidonii root revealed hepatoprotective activity [28]. Another study on rats against paracetamol- and ethanol-induced liver toxicity also confirmed that a methanol extract of C. chelidonii’s whole plant displayed hepatoprotective property [24]. In vivo study on ethanol extract of C. viscosa’s whole plant against CCl₄-induced hepatotoxicity [29], as well as methanol extract against streptozotocin- (STZ-) induced diabetic rats [30], C. viscosa leaves against thioacetamide-induced hepatotoxicity [31, 32], and C. viscosa seeds against paracetamol-induced hepatotoxicity [33, 34] also showed that C. viscosa possessed a hepatoprotective effect on rat models.

So far, there has been no report on the hepatoprotection and phytochemical constituents of the C. chelidonii and C. viscosa stems. Continuing our study on bioactive composition of traditional Vietnamese medicines [35] and the Cleome genus [36–39], this paper detailed the evaluation of the hepatoprotective effect of different extracts (n-hexane, ethyl acetate (EtOAc), and methanol (MeOH) extracts) from the stems of two Cleome species against CCl₄-induced liver intoxication in both in vitro and in vivo assays. All compounds isolated from the most active extracts were also measured for the hepatoprotective activity using in vitro assay.

2. Materials and Methods

2.1. Plant Materials

C. chelidonii and C. viscosa stems were collected in Ben Cat, Binh Duong province, Vietnam, in May 2015 and certificated by Professor Vo Van Chi. The voucher specimens (No. VH/MINH-1012 and No. VH/MINH-0515, respectively) were deposited in the Institute of Chemical Technology, Vietnam Academy of Science and Technology.

2.2. Extraction

Dried stems powders of C. chelidonii (8 kg) and C. viscosa (7 kg) were extracted with 96% EtOH for three times (3 × 30 L, total amount 90 L) at room temperature. The supernatants were filtered, and the solvents were removed under vacuum to obtain crude extracts CCS (970 g) and CVS (770 g), respectively. Those extracts were subjected to solid-phase separation and successively fractionated into n-hexane, EtOAc, and MeOH extracts, respectively, to afford six extracts: CCSH (155 g), CCSE (355 g), CCSM (420 g), CVSH (130 g), CVSE (310 g), and CVSM (330 g). Similar protocols were used for powdered leaves of C. chelidonii (5 kg) and C. viscosa (7.5 kg), resulting in six extracts: CCLH (120 g), CCLE (228 g), CCLM (170 g), CVLH (150 g), CVLE (260 g), and CVLM (400 g). All extracts were stored at 4°C for further studies.

2.3. Chemicals and Reagents

Eagle’s Minimum Essential Medium (EMEM), fetal calf serum (FCS), and trypsin-EDTA were purchased from Gibco, USA; L-glutamine, penicillin, streptomycin, phosphate buffer, 3-(4, 5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT), doxorubicin, and carbon tetrachloride (CCl₄) were from Sigma-Aldrich, USA; dimethyl sulfoxide (DMSO) and isopropanol were from Merck, Germany. All chemicals met cell culture standards.

2.4. Cell Culture

HepG2 cells (the American Type Culture Collection, Manassas, Rockville) were seeded and cultured in EMEM containing 10% FCS (v/v), 2 mM L-glutamine, 100 IU/mL penicillin, and 100 μg/mL streptomycin at 5% CO₂ at 37°C to attain confluency.

2.5. Animals

Swiss albino mice weighing 26–30 g were purchased from Pasteur Institute in Ho Chi Minh City, Vietnam Ministry of Health. The mice were housed in standard cages (48 cm × 35 cm × 22 cm) at room temperature and provided with pelleted food and water.

2.6. Evaluation of the In Vitro and In Vivo Hepatoprotective Activity

2.6.1. Cell Viability

HepG2 cells were harvested and seeded in 96-well plates at 4.0 × 10 cells/cm². Then, cells were treated with EMEM containing 2 mM CCl₄ and compounds 1–8 alone or combined at different concentrations. Cell viability was measured as mitochondrial succinate dehydrogenase activity, a marker of viable cells using MTT test. Doxorubicin was used as positive control for cytotoxicity. The assay was performed using the MTT test, as previously described [17, 18]. Doxorubicin was used as a positive control for cytotoxicity.

For the cytotoxicity, the percentage of control (%) was calculated = OD₅₇₀ sample/OD₅₇₀ control × 100% measured at the different concentrations (25, 50, and 100 μg/mL) by MTT assay.

2.6.2. Study on Hepatic Protective Effect in Mice Acute Liver Injury Induced by CCl₄

Mice were divided into six groups with six animals in each group.

Group I (normal control) received distilled water with 0.3% sodium carboxymethylcellulose (CMC-Na) (1 mL/kg body weight, p.o.) for 5 days and olive oil (1 mL/kg body weight, i.p.) on days 2 and 3.

Group II (CCl₄-intoxicated) received 0.3% CMC-Na (1 mL/kg body weight, p.o.) for 5 days and CCl₄–olive oil (1 : 1, 2 mL/kg body weight, i.p.) on days 2 and 3.

Group III (positive group) was treated daily with the positive silymarin drug (100 mg/kg body weight, p.o.) for 5 days and CCl₄–olive oil (1 : 1, 2 mL/kg body weight, i.p.) on days 2 and 3, 30 min after silymarin administration.

Test groups (IV–VI) were administered orally with 100, 200, and 400 mg/kg TFs, respectively, for 5 days. The three test groups received CCl₄–olive oil (1 : 1, 2 mL/kg, i.p.) on days 2 and 3, 30 min after TFs administration.

The mice were killed after the 24 h treatment. Blood was collected via heart puncture and serum was separated for examination of various biochemical parameters. The liver was carefully dissected and cleaned of extraneous tissue. A portion of the liver tissue was immediately transferred into 10% formalin for histopathologic investigation. Levels of biochemical parameters ALT and AST were measured and compared with silymarin control [15].

2.7. General Experimental Procedures for Isolation and Structural Identification

Column chromatography was carried out using Merck Silica gel normal-phase (230–240 mesh) and reversed-phase C₁₈ (Merck). Analytical TLC was carried out in silica gel plates (Merck DC-Alufolien 60 F₂₅₄). Compounds were visualized by spraying with 10% H₂SO₄ in EtOH and heating for 3–5 min.

The high-resolution electrospray ionization mass spectra (HR-ESI-MS) were acquired on a Bruker MicrOTOF-QII spectrometer. The ¹H-NMR (500 MHz), ¹³C-NMR (125 MHz), DEPT, COSY, HSQC, and HMBC spectra were recorded on a Bruker AM500 FT-NMR spectrometer using tetramethylsilane (TMS) as an internal standard.

2.8. Isolation of Pure Compounds

CVSM extract (330 g) was subjected to silica gel column chromatography and eluted with gradient solvent systems of chloroform and methanol (95 : 5 ⟶ 5 : 95, v/v) to collect six fractions: M1 (20 g), M2 (32 g), M3 (90 g), M4 (80 g), M5 (47 g), and M6 (62 g). The fraction M4 (80 g) was chromatographed on silica gel and eluted with CHCl₃–MeOH (6 : 1⟶3 : 1, v/v) to give four subfractions (M4.1–M4.4). The subfraction M4.2 (18 g) was separated and further purified by RP-18 with MeOH–H₂O (4 : 1, v/v) to deliver compounds 1 (150 mg), 3 (2 g), and 4 (250 mg). The fraction M5 (5 g) was applied on a silica gel chromatographic column and eluted with CHCl₃–MeOH (2 : 1, v/v) to yield compound 2 (50 mg).

Similarly, CCSM extract (420 g) was subjected to silica gel column chromatography and eluted with CHCl₃–MeOH (95 : 5–5 : 95, v/v) to get seven fractions: M1 (15 g), M2 (25 g), M3 (20 g), M4 (18 g), M5 (15 g), M6 (11 g), and M7 (52 g). The fraction M3 (20 g) was eluted with CHCl₃–MeOH–H₂O (5 : 1:0.1, v/v/v) by silica gel column chromatography to receive compound 8 (30 mg). The fraction M4 (18 mg) was loaded on silica gel column chromatography using CHCl₃–MeOH–H₂O (4 : 1:0.1, v/v/v) and furnished compound 5 (70 mg). The fraction M5 (15 g) was separated on a silica gel column with CHCl₃–MeOH–H₂O (3 : 1:0.1, v/v/v) to obtain compound 6 (45 mg). The fraction M6 (11 g) was eluted with CHCl₃–MeOH–H₂O (2 : 1:0.1, v/v/v) on a silica gel column chromatography to yield compound 7 (18 mg).

3. Results and Discussion

3.1. Protective Activity of Extracts against CCl₄-Induced Hepatoxicity in HepG2 Cells

The in vitro cytotoxic and hepatoprotective effects of extracts were shown in Tables 1 and 2.

The ethyl acetate extract of C. chelidonii stems mostly increased cell viability. Particularly, after 24 h of treatment, it increased 25% and 26% at the concentrations of 50 and 100 μg/mL, respectively; after 48 h of treatment, at 50 μg/mL, it increased 25% and 50%, respectively; after 72 h of treatment, at 100 μg/mL, it increased 26% and 60%, respectively.

The n-hexane and methanol extracts of C. chelidonii stems, after 72 h of treatment, at 100 μg/mL, approximately increased 21.4%, while the n-hexane and methanol extracts of C. chelidonii leaves, after 72 h of treatment at 100 μg/mL, increased 26.9% and 30%, respectively. Meanwhile, the ethyl acetate and methanol extracts of C. viscosa leaves and the n-hexane extract of C. viscosa stems, after 72 h treatment, at 100 μg/mL, increased from 20% to 30% cell viability.

The results show that the methanol extracts of the stems of C. chelidonii and C. viscosa significantly revealed in vitro hepatoprotective activity. Thus, these ones were further examined for in vivo hepatoprotection against CCl₄-induced liver toxicity in mice.

3.2. Hepatic Protective Effect of Extracts against CCl4-induced Liver Injury in Mice

The in vivo hepatoprotective effects of methanolic extracts of the stems of C. chelidonii and C. viscosa (Table 3 and Figure 1) were tested against CCl₄-induced toxicity of liver in mice.

(a)

(b)

At the doses of 30 mg/kg and 45 mg/kg, the methanol extracts of the stems of C. chelidonii and C. viscosa (CCSM and CVSM) significantly decreased ALT and AST concentrations in comparison with untreated extracts and the hepatic protection of these extracts was comparable to that of silymarin.

This result warranted the CCSM and CVSM extracts to be further investigated on phytochemical components.

3.3. Phytochemical Components of the Most Hepatic Protective Effect Extracts

The most in vitro and in vivo liver protection extracts of two species stems (CCSM and CVSM) were subjected to silica gel normal-phase and reversed-phase RP-18 chromatography to give eight known flavonoids (1–8) whose structures were confirmed by HR-ESI-MS, NMR experiments, and comparisons with the published data: visconoside A (1), visconoside B (2) [20], quercetin 3-O-β-D-glucopyranoside 7-O-α-L-rhamnopyranoside (3), kaempferol 3-O-β-D-glucopyranoside 7-O-α-L-rhamnopyranoside (4) [18], cleomeside A (5), cleomeside B (6) [19], cleomeside C (7), and quercetin-3-O-[β-D-glucopyranosyl-(1⟶2)]-α-L-rhamnopyranoside 7-O-α-L-rhamnopyranoside (8) [17] (Figure 2).

The phytochemical study confirmed that flavonoids are the main components of two species, which might be representative of their hepatoprotective effect. Therefore, the hepatoprotections of flavonoids (1–8) were screened using HepG2 cell line.

3.4. Cytotoxicity and Hepatoprotective Activity of Purified Compounds

The cytotoxicity (Table 4) and hepatoprotection (Table 5) using HepG2 cell line of all separated compounds 1–8 were measured by MTT assay.

At tested concentrations, samples did not show cytotoxicity, except compounds 3, 5, 6, and 8 at 25 μM (cell viability decreased, ranging from 25.0% to 30.0%).

At the concentration of 100 μM, compounds 1 and 4 significantly showed hepatoprotective effect (with prevention percentages of 66.5% and 74.2%, respectively), whereas compounds 5 and 8 disclosed weaker activity (with prevention percentages of 32.3% and 34.3%, respectively, compared to that of 80.3% of quercetin positive control).

The hepatoprotective effects of compounds 1 and 4 were tested for the first time.

4. Conclusions

In vitro and in vivo hepatoprotections using HepG2 and in mice of C. chelidonii and C. viscosa stems and their phytochemical constituents were investigated for the first time. The phytochemical study evidenced that flavonoids are the main compounds of two species. Furthermore, the hepatoprotections of visconoside A (1) and kaempferol 3-O-β-D-glucopyranoside 7-O-α-L-rhamnopyranoside (4) were identified for the first time. However, further clinical examinations are required to determine the molecular mechanisms of hepatoprotection as well as qualitative and quantitative identification of main biological flavonoid markers (1, 4, and 6) from these species.

The present study suggests that C. chelidonii and C. viscosa plants are good sources of natural hepatoprotective agents and contribute to understanding the biological activities of Cleome species in traditional Vietnamese medicine.

Data Availability

All the data related to the study are available from the corresponding author and can be provided upon request.

Conflicts of Interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

Acknowledgments

This work was partially supported by the Vietnam Academy of Science and Technology, Project no. UDSXTN.03/19–20, and Binh Phu Pharma Ltd.

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Copyright © 2021 Nhat Minh Phan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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