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BRIEF COMMUNICATION
Year : 2019  |  Volume : 15  |  Issue : 1  |  Page : 245-249

Cytotoxic activity of extracts and fractions from Paramignya trimera root and Phyllanthus amarus against pancreatic cancer cell lines


1 Department of Food Technology, Faculty of Food Technology, Nha Trang University, Nha Trang, Khanh Hoa 8458, Vietnam; School of Environmental and Life Sciences, Faculty of Science, University of Newcastle, Ourimbah, NSW 2258, Australia
2 School of Environmental and Life Sciences, Faculty of Science, University of Newcastle, Ourimbah, NSW 2258, Australia

Date of Web Publication13-Mar-2019

Correspondence Address:
Dr. Van Tang Nguyen
Department of Food Technology, Faculty of Food Technology, Nha Trang University, No. 2 Nguyen Dinh Chieu, Nha Trang, Khanh Hoa 8458, Vietnam. School of Environmental and Life Sciences, Faculty of Science, University of Newcastle, Ourimbah, NSW 2258

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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_85_18

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 > Abstract 


Objective: The aim of this study was to assess cytotoxic activity of extracts and fractions from the Paramignya trimera root (PTR) and Phyllanthus amarus (PA) against two pancreatic cancer cell lines (primary: BxPc3 and secondary: CFPAC1).
Materials and Methods: The root of PT and whole plant of PA were used in this study. The extracts and fractions from the PTR and PA were prepared using microwave-assisted extraction and high-performance liquid chromatography, respectively. The cytotoxic activity was assessed using the Dojindo Cell Counting Kit-8 assay.
Results: The findings showed impressive cytotoxic capacity of the PTR extract against both pancreatic cancer cells of BxPc3 and CFPAC1 in a range of concentrations from 50 to 200 μg/mL, which was higher than those of ostruthin (67 μM), gemcitabine (50 nM), and four its fractions (50 μg/mL), and to be comparable to a saponin-enriched extract from Quillaja bark at 200 μg/mL. In contrast, the cytotoxic capacity of the PA extract and nine its fractions against these pancreatic cancer cell lines was significantly lower (P < 0.05) than those of gemcitabine (50 nM) and Quillaja bark extract (200 μg/mL) and being comparable to phyllanthin (4.8 μM). The IC50 values of the PTR extract against BxPc3 and CFPAC1 cancer cells were 32.12 and 36.65 μg/mL, respectively, which was much lower than that of the PA extract against CFPAC1 cancer cells (128.81 μg/mL).
Conclusion: The outcomes obtained from this study reveal that the PTR extract is a lead source for the potential development of novel antipancreatic cancer drugs and/or functional foods.

Keywords: Cytotoxicity, extracts, fractions, Paramignya trimera, Phyllanthus amarus


How to cite this article:
Nguyen VT, Scarlett CJ. Cytotoxic activity of extracts and fractions from Paramignya trimera root and Phyllanthus amarus against pancreatic cancer cell lines. J Can Res Ther 2019;15:245-9

How to cite this URL:
Nguyen VT, Scarlett CJ. Cytotoxic activity of extracts and fractions from Paramignya trimera root and Phyllanthus amarus against pancreatic cancer cell lines. J Can Res Ther [serial online] 2019 [cited 2019 Aug 22];15:245-9. Available from: http://www.cancerjournal.net/text.asp?2019/15/1/245/244478




 > Introduction Top


Plants have been widely used for cancer prevention and treatment.[1] Currently, around 45% of all anticancer drugs have been isolated directly or indirectly from plant compounds. A number of plant-derived agents have been used for the clinical treatment of various cancers, such as the vinca alkaloids, taxanes, podophyllotoxin, and camptothecin analogs. Some plant-derived anticancer agents have been used for the treatment of pancreatic cancer, such as irinotecan, docetaxel, paclitaxel, triptolide, and minnelide (semi-synthetic).[2],[3] However, the drawback of these anticancer drugs is presented as they are highly toxic with low treatment effectiveness and significant reduction in the quality of life of the cancer patients.[4]

Xao tam phan is the Vietnamese name of Paramignya trimera (Oliv.) Guillaum (P. trimera), which has the synonym of Atalantia trimera Oliv., belongs to the Paramignya genus of the Citrus family (Rutaceae), and is well known as a traditional medicinal plant for cancer prevention and treatment in Thailand and Vietnam.[5],[6] Phyllanthus amarus (PA) is a herbal plant belonging to the Phyllanthus genus of family Phyllanthaceae(Euphorbiaceae), which is widely distributed in tropical and subtropical areas and has been used for the treatment of various chronic ailments, such as hepatitis B and C, diabetes, and cancer.[7],[8],[9]

Recent studies sought that the P. trimera root (PTR) and leaf extracts displayed potent cytotoxic capacity on the panel of various cancer cell lines including MiaPaCa-2 (pancreas), HT29 (colon), A2780 (ovarian), H460 (lung), A431 (skin), Du145 (prostate), BE2-C (neuroblastoma), Michigan Cancer Foundation (MCF)-7 (breast), MCF-10A (normal breast), and U87, SJ-G2, and SMA (glioblastoma), while the PA extracts exhibited lower cytotoxic capacity on these cancer cells.[10],[11] However, the cytotoxic activity of the extracts and fractions from the PTR and PA against two pancreatic cancer cell lines (BxPc3 and CFPAC1), which were not included in the panel above, has yet to be reported. With this in mind, the aim of this study was to assess cytotoxic activity of extracts and fractions from the PTR and PA against two additional pancreatic cancer cell lines (primary: BxPc3 and secondary: CFPAC1) for the potential development of novel anticancer drugs and/or functional foods.


 > Materials and Methods Top


Plant materials

PTR and PA were collected and prepared as follows: the PTR was obtained in January 2014 from Hon Heo, Ninh Hoa district, Khanh Hoa Province, Vietnam, and authenticated by the National Institute of Medicinal Materials, Ministry of Health, Vietnam. The fresh sample was rinsed in deionized water to remove sand and soil, drained, and dried under the sun at 34.5°C to constant weight.[10] The whole plant of the PA was collected in January 2015 from Hon Nghe, Vinh Ngoc, Nha Trang city, Khanh Hoa Province, Vietnam, and authenticated by Quang Ngai Union of Science and Technology Association, Vietnam. The fresh sample was placed in sealed plastic bags, covered with ice to minimize oxidation, and immediately taken to the laboratories at the Nha Trang University. The fresh sample was then rinsed in deionized water to remove sand, soil, and foreign materials, drained, and dried by infrared at 30°C to constant weight in an infrared drying cabinet (SHN-L, Nha Trang University, Vietnam).[9] The dried samples were packaged in vacuum-sealed polyamide bags and stored at −20°C until required. The herbarium specimen numbers of 240214 (PTR) and 240115 (PA) were deposited at the School of Environmental and Life Sciences, University of Newcastle, Australia. The dried samples were ground to a fine powder using an electric blender (Hamilton Beach Brands, Inc., China), screened through a stainless steel mesh with particle size ≤1.4 mm (Endecotts, London, England), and kept at −20°C until used for further investigations.

Analytical chemicals

All chemicals were of analytical grade. Ostruthin, phyllanthin, gemcitabine, and saponin-enriched Quillaja bark extract were the analytical products of Sigma-Aldrich Pty Ltd. (Castle Hill, Sydney, Australia). 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide, Roswell Park Memorial Institute (RPMI), and Iscove's Modified Dulbecco's Medium (IMDM) were purchased from Gibco by Life Technologies (Grand Island, NY, USA). Dojindo Cell Counting Kit-8 (CCK-8) was obtained from Dojindo Molecular Technologies Inc., Maryland, USA).

Preparation of extracts and fractions from the Paramignya trimera root and Phyllanthus amarus

The methanol extracts and fractions from the PTR and PA were prepared based on the previously described methods using microwave-assisted extraction (MAE) and high-performance liquid chromatography.[9],[10]

For preparation of the PTR and PA extracts, 10 g of dried samples was soaked in 1000 mL of 100% methanol at room temperature (21°C ± 1°C) for 20 min, followed by MAE using a microwave oven (Sharp Carousel, Sharp Corporation, Thailand) at power of 360 W, irradiation time of 7 s/2 min, and extraction time of 40 min. The extracts were then rapidly cooled to room temperature using an ice water bath and filtered through qualitative No. 1 filter papers (Bacto Laboratories Pty Ltd., NSW, Australia). After that, the extracts were evaporated under reduced pressure (−10 mbar) at 40°C using a rotavapor (Buchi, Flawil, Switzerland) and dried to constant weight using a freeze drier (Rietschle Thomas Australia Pty Ltd, NSW, Australia) at −45°C, 0.1 atm for 48 h to achieve the powdered PTR and PA extracts. These extracts were stored at −20°C until required for further experiments.

For fractionation of the PTR and PA extracts, before injection, the extracts were filtered through 0.45 μm nylon membranes (Phenex syringe filters), and then, 300 μL of the extracts was injected by an autosampler (SIL-10AV, Shimadzu, Kyoto, Japan) onto a Semi-prep Phenomenex Synergy 4U Polar-RP 80A column (250 mm × 10 mm) (Phenomenex, Torrance, USA). The column was kept at 35°C by an oven thermal sphere (Phenomenex, Torrance, USA) and coupled to an auto fraction collector (FRC-10A, Shimadzu, Kyoto, Japan). Two mobile phases were used including (A) 0.2% orthophosphoric acid in distilled water and (B) 100% acetonitrile. The flow rate was at 3 mL/min. The gradient was set as follows: 0–5 min, 0% B; 5–20 min, 20% B; 20–30 min, 30% B; 30–48 min, 30% B; and 48–53 min, 0% B. Phytochemicals were detected at 340 nm (for the PTR extract) and 210 (for the PA extract) using a diode array detector (8PD-M20A, Shimadzu, Kyoto, Japan). Fractionation of major phytochemicals in the PTR and PA extracts was obtained based on their retention times as follows: F1: 36.5–37.0 min, F2: 39.9–40.5 min, F3: 41.35–41.85 min, and F4: 42.85–43.35 min (for the PTR extract), and F1: 4.72–5.40 min, F2: 6.65–7.11 min, F3: 10.10–11.20 min, F4: 18.40–19.35 min, F5: 28.40–28.85 min, F6: 29.02–29.60 min, F7: 30.00–30.50 min, F8: 31.75–32.34 min, and F9: 32.90–33.30 min (for the PA extract). Four and nine fractions from the PTR and PA extracts were separately collected from the fraction collector and evaporated under reduced pressure (−30 to 50 mbar) at 45°C–60°C using a rotavapor (Buchi, Flawil, Switzerland) and dried to constant weight using a freeze drier (Rietschle Thomas Australia Pty Ltd, NSW, Australia) at −45°C, 0.1 atm for 72 h to obtain the powdered PTR and PA factions (F1: 1.1273 g, F2: 1.4584 g, F3: 1.2113 g, and F4: 0.3812 g from the PTR extract and F1: 1.093 g, F2: 0.925 g, F3: 1.507 g, F4: 1.401 g, F5: 0.858 g, F6: 0.801 g, F7: 0.695 g, F8: 1.059 g, and F9: 0.534 g from the PA extract). These fractions were kept at −20°C until used for further analysis.

Identification of bioactive components within the extracts and fractions from the Paramignya trimera root and Phyllanthus amarus

The bioactive components within the PTR and PA extracts have been presented in the previous reports.[12],[13] In this study, the bioactive components within the PTR and PA fractions were identified according to the previously reported methods.[9],[10]

Assessment of cytotoxic activity of extracts and fractions from the Paramignya trimera root and Phyllanthus amarus

Cell culture

Human pancreatic cancer cell lines (primary: BxPc3 and secondary: CFPAC1) were cultured based on the previously described methods[14],[15] with some modifications. Briefly, the cells of BxBc3 or CFPAC1 were grown in RPMI or IMDM supplemented with 10% fetal bovine serum and 1% L-glutamine at 37°C with 5% CO2, respectively.

Cell viability

Cell viability was determined using the CCK-8 assay based on the previously reported methods[14],[15] with some modifications. Briefly, the cells were seeded into a 96-well plate at 3 × 103 cells per well and allowed to adhere for 24 h at 37°C with 5% CO2. Media was removed and the cells were then treated with various concentrations of PTR and PA extracts (200-12.5 μg/mL) and fractions (50 μg/mL) in the media, ostruthin (67 μM), phyllanthin (4.8 μM), and gemcitabine (50 nM) as positive controls, saponin-enriched Quillaja bark extract (200 μg/mL) as a comparative sample, and 0.5% dimethyl sulfoxide (DMSO) as a control. After 72 h incubation at 37°C with 5% CO2, the media was removed and 100 μL of 10% CCK-8 solution in the media was added and incubated at 37°C with 5% CO2 for 2 h. Absorbance was measured at 450 nm and cell viability was expressed as a percentage of control.

Statistical analysis

The data were analyzed by SPSS software (Version 22, Chicago, IL, USA), and the results were expressed as means ± standard deviations. Statistical comparisons were made using one-way analysis of variance and Duncan's multiple range tests. Differences were considered to be statistically significant when P < 0.05.


 > Results and Discussion Top


Bioactive components within the Paramignya trimera root and Phyllanthus amarus extracts and fractions

The PTR extract contains gallic acid, chlorogenic acid, caffeic acid, (−)-epicatechin, syringic acid, p-coumaric acid, rutin, myricetin, quercetin, (+)-catechin and kaempferol, while the PA extract contains gallic acid, caffeic acid, chlorogenic acid, (−)-epicatechin, syringic acid, p-coumaric acid, (−)-epigallocatechin gallate, rutin, luteolin, β-sitosterol, myricetin and 5,7-dimethoxycoumarin.[12],[13] In this study, two PA fractions 1 and 4 were identified to be quercetin and (−)-epicatechin, respectively, while the PTR fractions have not been determined in this study. Hence, the rest PTR and PA fractions are required to characterize in further studies.

Cytotoxic activity of extracts and fractions from the Paramignya trimera root and Phyllanthus amarus on primary pancreatic cancer cells (BxPc3)

The viability of primary pancreatic cancer cells (BxPc3) treated with various concentrations of PTR and PA extracts (200-12.5 μg/mL) and fractions (50 μg/mL), ostruthin (67 μM), gemcitabine (50 nM), and Quillaja bark extract (200 μg/mL) is shown in [Figure 1] and [Figure 2]. The viability of BxPc3 cells treated with 200-50 μg/mL of PTR extract (2.35–4.32%) was comparable to that treated with 200 μg/mL of Quillaja bark extract (2.21%), but it was significantly lower (P < 0.05) than those at concentrations of 25-12.5 μg/mL (70.01–91.12%), four its fractions at 50 μg/mL (47.16–57.48%), 50 nM of gemcitabine (15.17%), and 20 μg/mL of ostruthin (60.93%) [Figure 1]. The viability of BxPc3 cells treated with 200-12.5 μg/mL of PA extract (62.84–80.76%), 50 μg/mL of PA fractions (55.00–71.71%), and 2 μg/mL of phyllanthin (59.36%) was significantly higher (P < 0.05) than those treated with 50 nM of gemcitabine (15.17%) and 200 μg/mL of Quillaja bark extract (2.21%) [Figure 2]. The IC50 value of the PTR extract against BxPc3 cancer cells was found to be 32.12 μg/mL, while it was not determined for the PA extract.
Figure 1: Viability of BxPc3 cells treated with different concentrations of Paramignya trimera root extract and its fractions. Dimethyl sulfoxide was used as a control; gemcitabine and ostruthin were used as positive controls; Quillaja bark extract was used as a comparative sample. Different letters in the columns outline significant differences between values (P < 0.05)

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Figure 2: Viability of BxPc3 cells treated with different concentrations of Phyllanthus amarus extract and its fractions. Dimethyl sulfoxide was used as a control; gemcitabine and phyllanthin were used as positive controls; Quillaja bark extract was used as a comparative sample. Different letters in the columns outline significant differences between values (P < 0.05)

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The viability of BxPc3 cells treated by the PTR and PA extracts in this study is similar to that of MiaPaCa-2 cells treated by these extracts in previous reports,[9],[10] revealing that the PTR and PA extracts possessed potent cytotoxic potential on primary pancreatic cancer cell lines.

To compare with other extracts and compounds, the viability of BxPc3 cells treated with 200 μg/mL of PTR extract in this study (2.21%) is comparable to that treated with 200 μg/mL of PT leaf extract (2.30%); however, the viability of BxPc3 cells treated with 100-50 μg/mL of PTR extract (2.32%–4.32%) is much lower than those of the PT leaf extract (20.52%–87.79%)[11] and the extracts from two selected Eucalyptus species, i.e., Eucalyptus microcorys and Eucalyptus saligna (73.94–89.77%).[16] The viability of BxPc3 cells treated with 100-50 μg/mL of PA extract (67.86–80.76%) in this study is also lower than that of the extracts from these selected Eucalyptus species. Fan et al.[17] assessed the viability of BxPc3 cells treated by sulforaphane and quercetin and found that the number of BxPc3 cells was strongly decreased (approximately 20%) after treatment with these compounds in a dose-dependent manner (30 μM). This finding indicated that the PTR and PA extracts are potential sources against primary pancreatic cancer cell lines.

Cytotoxic activity of extracts and fractions from the Paramignya trimera root and Phyllanthus amarus on secondary pancreatic cancer cells (CFPAC1)

[Figure 3] and [Figure 4] show viability of secondary pancreatic cancer cells (CFPAC1) treated with various concentrations of PTR and PA extracts (200-12.5 μg/mL) and fractions 50 (μg/mL), ostruthin (67 μM), gemcitabine (50 nM), and Quillaja bark extract (200 μg/mL). The viability of CFPAC1 cells treated with 200-50 μg/mL of PTR extract (7.86%–12.53%) was significantly lower (P < 0.05) than those treated with concentration of 25-12.5 μg/mL of PTR extract (83.76%–85.98%), four its fractions at 50 μg/mL (68.61%–73.83%), and 20 μg/mL of ostruthin (81.40%), but it was not significantly different from 50 nM of gemcitabine (15.96%) and 200 μg/mL of Quillaja bark extract (7.90%) [Figure 3]. [Figure 4] indicates that the viability of CFPAC1 cells treated with 200 μg/mL of PA extract (32.47%) was significantly lower than those treated by 100-12.5 μg/mL of PA extract (56.90%–78.22%), nine its fractions at 50 μg/mL (78.60%–104.10%), and 2 μg/mL of phyllanthin (71.08%); however, it was significantly higher than those of 50 nM of gemcitabine (15.96%) and 200 μg/mL of Quillaja bark extract (7.90%). The IC50 values of the PTR and PA extracts against CFPAC1 cancer cells were 36.65 and 128.81 μg/mL, respectively.
Figure 3: Viability of CFPAC1 cells treated with different concentrations of Paramignya trimera root extract and its fractions. Dimethyl sulfoxide was used as a control; gemcitabine and ostruthin were used as positive controls; Quillaja bark extract was used as a comparative sample. Different letters in the columns outline significant differences between values (P < 0.05)

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Figure 4: Viability of CFPAC1 cells treated with different concentrations of Phyllanthus amarus extract and its fractions. Dimethyl sulfoxide was used as a control; gemcitabine and phyllanthin were used as positive controls; Quillaja bark extract was used as a comparative sample. Different letters in the columns outline significant differences between values (P < 0.05)

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Similar to the primary pancreatic cancer cells (BxPc3), the viability of CFPAC1 cells treated by 200 μg/mL of PTR extract in this study (7.86%) was similar to that of the PT leaf extract (7.92%).[11] In particular, the viability of CFPAC1 cells treated with 100-50 μg/mL of PTR extract (7.89%–12.53%) was much lower than those treated by the PT leaf extract (16.36%–58.70%)[11] and the extracts from two selected Eucalyptus species, i.e., E. microcorys and E. saligna (85.34%–93.55%).[16] In addition, the viability of CFPAC1 cells treated with 100-50 μg/mL of PA extract (56.90%–69.11%) in this study was also lower than that of the extracts from these selected Eucalyptus species.

Impressive cytotoxic capacity of the PTR extract against pancreatic cancer cells (BxPc3 and CFPAC1) is due to its high contents of phytochemicals in terms of saponins, phenolics, flavonoids, and proanthocyanidins (7731.05 mg escin equivalents, 238.13 mg gallic acid equivalents, 81.49 mg rutin equivalents, and 58.08 mg catechin equivalents/g dried extract, respectively).[10] On the other hand, limited cytotoxic capacity of the PTR and PA fractions against these pancreatic cancer cells may be because of the loss of their activity by oxidation or decomposition during fractionation under environmental conditions such as oxygen-rich air, ultraviolet light, and high temperature. For this limitation, further studies are needed to preserve the biological activity and characterize the chemical properties of the PTR and PA fractions.

To compare with other extracts and compounds, Shi et al.[18] evaluated the effect of metformin (MET) on the growth of CFPAC1 cells and found that the survival of CFPAC1 cells was significantly decreased with an increase of MET concentration from 1 to 60 mmol/L (from 83 to 7%, respectively). Akimoto et al.[19] examined the effect of ginger extract on the viability of BxPc3 and CFPAC1 cells and indicated that a greater reduction of BxPc3 and CFPAC1 cells was observed when the ginger extract concentration increased from 100 to 200 μg/mL (from 55% to 7% and from 15% to 5%, respectively). This outcome showed us that the PTR and PA extracts are promising sources against secondary pancreatic cancer cell lines.


 > Conclusion Top


The results obtained from this study allow us to conclude that the PTR extract displayed potent cytotoxic activity against both primary and secondary pancreatic cancer cells, and it is, therefore, a promising source for further development of novel anticancer drugs and/or functional foods. However, extensive investigations are needed to characterize the factions, evaluate the efficacy of the PTR extract in cancer-bearing animals, and understand the mechanism of its action both in vitro and in vivo for further application in the nutraceutical, medicinal, and pharmaceutical industries.

Acknowledgments

The authors would like to thank the support from the Faculty of Science, the University of Newcastle, Australia and the Vietnamese Government. The National Foundation for Science and Technology Development (NAFOSTED) is also gratefully acknowledged.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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