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BY 4.0 license Open Access Published by De Gruyter Open Access November 22, 2023

Treatment of gastric cancer by green mediated silver nanoparticles using Pistacia atlantica bark aqueous extract

  • Ling Dang , Jian Yang , Sally Negm , Attalla F. El-kott , Ali A. Shati , Heba I. Ghamry and Bikash Karmakar EMAIL logo
From the journal Open Chemistry

Abstract

We herein demonstrate a novel green mediated silver nanoparticles (AgNPs) using Pistacia atlantica bark aqueous extract for the treatment of gastric cancer under in vitro conditions. Physicochemical and structural features of the nanocomposite biomaterial were assessed by several techniques like UV-Vis spectrum, transmission electron spectroscopy, field emission scanning electron microscopy, energy-dispersive X-ray spectroscopy, and inductively coupled plasma-optical emission spectroscopy. The Ag NPs showed high antioxidant activities against 2,2-diphenyl-1-picrylhydrazyl (DPPH). The IC50 of Ag NPs and Butylated hydroxytoluene against DPPH were 132 and 77 µg/mL, respectively. In the oncological part of this research, the status of normal and gastric cancer AGS and KATO III cell lines was determined. The IC50 of AgNPs was 193 and 250 µg/mL against AGS and KATO III. It seems that the prepared NP have stopped the growth of gastric cancer cells and the recent cancer cells have been removed with high concentration of NPs.

1 Introduction

Pistacia atlantica is a plant used in prescriptions related to cancer treatment. This plant is also known as Bane. This plant belongs to the pistachio family or Anacardiaceae [1,2]. Native people eat the fruits of the Pistacia atlantica tree as snacks. In this way, they are roasted and mixed with other nutritious seeds. Pistacia atlantica gum is also used to prepare a kind of natural gum [3,4]. The nature of the Pistacia atlantica plant and its gum is hot and dry, and doctors have mentioned the therapeutic effects of several parts, such as its fruit, leaves, and gum, to cure a wide range of diseases. So far, the Pistacia atlantica plant has been subjected to many studies, a large part of which has been carried out by scientists and students. For example, the antioxidant effects of fruit and peels have been investigated in various in vitro studies, and the antioxidant properties of plant extracts have been compared with the standard compounds studied [5,6,7]. In addition, leaf essential oil and gum have shown significant antibacterial and antifungal effects in different strains [8,9,10,11,12]. A search of reliable sources of traditional medicine shows that Pistacia atlantica is used in the treatment of cancer. Pistacia atlantica gum is used to treat diseases related to the digestive system and is prescribed to cleanse the brain and nervous system of excess moisture. One of the uses of Pistacia atlantica that is widely seen in Iranian medical sources is its use in ointments and poultices that are used to heal swellings, wounds, and injuries that are difficult to treat due to various reasons [13,14,15,16,17,18,19,20,21,22]. Pistacia atlantica has a special place in the indigenous medicine of different tribes. It is used in the traditional medicine of Algeria, as a compound to strengthen the digestive system and anti-diarrhea [23], in Greece, to freshen the mouth [24], in Turkey, to treat wounds [25], and in Jordan and Morocco, as a medicine against respiratory tract infections and painkillers [26,27]. There are ointments related to diseases of cancer, pigs, taalil nails, leprosy, salah, and squirus, one of the components of which is gum Pistacia atlantica. Shangarf ointment or Zenjfer is one of the topical medicinal forms for the treatment of cancer and pigs, which is mentioned frequently and with little change in the authentic books of traditional medicine. Syringe ointment is also one of the most frequently used ointment, and one of its components is Pistacia atlantica. In addition, sages have prescribed other prescriptions for the treatment of cancer or related diseases, which contain Pistacia atlantica. The point that exists in the Pistacia atlantica used in traditional medicine texts is that sages use the gum of this plant, and apparently, the rest of the plant’s components have not been widely used to treat cancer. Among the other things that can be taken into consideration are the many topical medicinal forms prepared from Pistacia atlantica gum and other ingredients for the cure of cancer and other malignancies. The conducted research works show the very high ability of the effective ingredients of the Pistacia atlantica to affect cancer cells. The amount of Pistacia atlantica constituents are analyzed and determined using methods such as GC and HPLC. According to these research works, the major components of the oil obtained from Pistacia atlantica gum are monotrin compounds such as alpha pinene, limonene, and alpha-pineol [28,29,30]. Pistacia atlantica resin also contains various triterpenoid compounds such as morolic acid, masticadienonic acid, and olanolic acid [27,28,29]. Also, gallic acid, catechin, flavonoids, and anthocyanins have also been identified in Pistacia atlantica [29,30]. The effects of polyphenol compounds in cancer prevention have been confirmed in several animal and cell research works [27,28,29,30].

Today, several types of cancer treatments including surgery, palliative care, radiation therapy, and chemotherapy are available, and depending on the cancer degree and location, several methods are applied for treatment. Hence, there is a need for modern treatment methods to control cancer [31,32,33]. In the current age, the term “Nano-biotechnology” has been become quite familiar amongst researchers, which has made a pivotal connection between nanoscience and biotechnology [34,35]. Meanwhile, the science of nanotechnology has contributed greatly to the development and discovery of modern cancer treatment options. For example, we can mention the use of modified nanoparticles (NPs) for the targeted and selective delivery of drugs to carcinoma tissue [36,37,38]. The use of nanotechnology in the drugs production is one of the promising fields. Because of their excellent physical characteristics, NPs have been applied as an effective candidate for drug treatment, the most important of which is silver NPs [33,34,35,36]. Although there are different methods for NP synthesis, biocompatible methods such as synthesis using bacteria, fungi, and plants are very simple and cost-effective alternatives to chemical and physical methods [39,40,41,42]. Meanwhile, plants have received more attention. Various research works have also revealed the anticancer property of plant NPs, so that these plants have been applied for the green synthesis of silver nanoparticles (AgNPs ) [43,44,45]. If the anti-tumor and therapeutic effects of these NPs are approved, this can be a step forward in the advancement of cancer treatment methods [46,47,48,49]. Various studies have proven the AgNPs role on Caspase 3 (Casp3) gene and p53 gene in anticancer effects [50,51,52,53]. The p53 gene is in the chromosome-17 short arm at position P13.17 and has 11 exons and a length of 20 kb. p53 mutations are found in approximately half of human tumors, and the remaining tumors appear to be caused by defects in p53-related pathways. Casp3 gene is in the chromosome-4 long arm at position q344 and has 8 exons. Cas3 is one of the executive caspases that can be activated by proteolysis and activate other procaspases. Finally, programmed cell death occurs and leads to DNA fragmentation, disintegration of the cell skeleton, and nuclear proteins. Also, AgNPs cause the removal of tumor cells by activating the production path of oxygen free radicals or reactive oxygen species (ROS) [51,52,53,54,55].

The goal of this research is to introduce a method for the green synthesis of AgNPs using Pistacia atlantica bark (Figure 1), as novel procedure without using any harmful and toxic agents. The prepared AgNPs were analyzed and their cytotoxicity was determined against gastric carcinoma cells.

Figure 1 
               Image of Pistacia atlantica.
Figure 1

Image of Pistacia atlantica.

2 Experimental methods

2.1 Sources

AgNO3, NaOH, acetone, and ethanol were procured from Sigma Aldrich. Cancer cells (AGS and KATO III) and normal cell lines were purchased from the Iran Pasteur Institute.

2.2 Preparation of plant extract

Cleaned and dried Pistacia atlantica fruit (1.0 g) was added to 20 mL deionized water and heated at 80°C for 0.5 h. The pale-yellow fruit extract was collected by filtration over Whatman-1paper and used as such.

2.3 Synthesis of AgNPs

10 mL of the prepared fruit extract was added to AgNO3 (50 mL, 1 mM) aqueous solution and stirred at room temperature for 30 min. The color of the solution turning dark brown confirmed the synthesis of AgNPs (Figure 2). The prepared AgNPs were collected by centrifugation at 1792RCF (G-force) for 10 min, then washed with DI water.

Figure 2 
                  Silver nitrate solution (a), Pistacia atlantica extract (b), and color changes in the synthesis of Ag NPs (c–f).
Figure 2

Silver nitrate solution (a), Pistacia atlantica extract (b), and color changes in the synthesis of Ag NPs (c–f).

2.4 Characterization of biosynthesized AgNPs

The obtained biosynthesized AgNPs were analyzed by modern characterization methods, as follows: transmission electron spectroscopy (TEM) analysis was performed using a Phillips CM10 microscope. Elements presence in the related composite was assessed by energy-dispersive X-ray spectroscopy (EDX) linked to scanning electron microscopy (SEM). In the spectrophotometric analysis, a double beam UV-Vis instrument (PG, T80+) was used along with quartz cuvettes (10 mm). The spectral data of prepared nanocomposite were recorded in the range of 230–700 nm.

2.5 Measurement of anti-gastric cancer properties

Synthesized Ag NPs’ cytotoxic effects on gastric cancer AGS and KATO III cells were assessed by Methy Thiazol Tetrazolium (MTT) test.

DMEM high glucose culture medium enriched with 4 mM l-glutamine and FBS 10% were used for cell culture and the cells were transferred to an incubator. After three successful passages, the cells were cultured to the number of 104 cells in each well. After 24 h of cell culture, they were exposed to several dilations of NPs for 24, 48, 72, and 96 h. Then, the MTT test was performed to determine the cytotoxicity induced by the above NPs and the percentage of cell survival. After the desired time, a sufficient amount of MTT was added to the wells. After incubating the plates for 3 h, the culture medium was removed and DMSO was added to the wells. After 150 min, optical absorption at 570 nm was read by an ELISA reader (BioTek manufactured by Viragen). The cells’ survival percentage was computed using the below formula [54]:

Cell viability ( % ) = Sample A Control A × 100 .

2.6 Measurement of antioxidant properties

In order to check the antioxidant property, 2-2 diphenyl-1-picrylhydrazil (DPPH) test was conducted. The color change was measured using spectrophotometry. 1 mL of 1 mM DPPH was added to 1 mL of NPs in different dilutions, shaken well, and kept in the dark at 25°C for 0.5 h. Then, the absorbance of the mixture at 517 nm wavelength was measured with blank methanol and DPPH solution and free radical inhibition was calculated using the below formula [54]:

DPPH scavenging effect ( % ) = [ ( A 0 A 1 ) / A 0 ] × 100 .

In the above biological tests, IC50 was obtained from a linear graph with a regression coefficient above 0.9.

3 Results and discussion

The AgNP synthesis can be easily detected by visible observations, as shown in Figure 2, where the color of the solution changed to light brown. This result was also confirmed by UV-Vis study, where the AgNPs peak appeared at around 450 nm. Figure 3 shows the reduction sequence in the measured absorbance terms in UV-Vis, at several time intervals.

Figure 3 
               UV-Vis absorption spectra of biosynthesis of AgNPs using Pistacia atlantica extract.
Figure 3

UV-Vis absorption spectra of biosynthesis of AgNPs using Pistacia atlantica extract.

The surface size, shape, and morphology of the prepared AgNPs were analyzed using field emission scanning electron microscopy (FESEM) and TEM images (Figures 4 and 5). Subsequently, the inherent structural morphology was dispensed from TEM investigations (Figure 5) As can be seen from TEM images, the materials are well-dispersed with spherical shaped. Nanocomposite particles mean diameter are within 20–30 nm.

Figure 4 
               FESEM image of biosynthesized AgNPs.
Figure 4

FESEM image of biosynthesized AgNPs.

Figure 5 
               TEM images of formulated NPs.
Figure 5

TEM images of formulated NPs.

EDX investigation of formulated AgNPs was carried out in order to have information on its chemical composition (Figure 6). The appeared strong signal at 2.5–3.2 keV was correspond to Ag species. The O and C small peaks are detected in the lower region corresponding to the phytomolecules from Pistacia atlantica.

Figure 6 
               EDX spectrum of biosynthesized AgNPs.
Figure 6

EDX spectrum of biosynthesized AgNPs.

The findings of the MTT test on gastric cancer cell lines and HUVEC showed that cell viability depended on the concentration of NPs. So, in 48 h after the treatment and at high doses of this NP, the survival rate of cancer cells decreased drastically (Table 1, Figures 7 and 8). IC50 in 48 h for cancer cells was reported to be about 193 and 250 μg/mL on AGS and KATO III, while normal cells revealed a higher percentage of survival than cancer cells. The results indicated that these NPs could inhibit gastric cancer cells more strongly than normal cells.

Table 1

AgNPs and Pistacia atlantica extract IC50

AgNPs (µg/mL) Pistacia atlantica extract
IC50 against AGS 193 ± 5a 562 ± 5b
IC50 against KATO III 250 ± 4a 593 ± 7b
IC50 against HUVEC

Non-identical words (a, b) show the significant difference.

Figure 7 
               The cytotoxicity effects of Pistacia atlantica extract and AgNPs.
Figure 7

The cytotoxicity effects of Pistacia atlantica extract and AgNPs.

Figure 8 
               The anti-gastric carcinoma effects of Pistacia atlantica extract and AgNPs against AGS (a) and KATO III (b) cells.
Figure 8

The anti-gastric carcinoma effects of Pistacia atlantica extract and AgNPs against AGS (a) and KATO III (b) cells.

Antioxidants prevent the free radicals formation or interrupt the free radicals release from several mechanisms, namely (1) removal of peroxidation initiator species, (2) chelation of metal ions in such a way that they cannot produce ROS or break down lipid peroxide, (3) quenching O2- to prevent the peroxide formation, and (4) reducing the O2 concentration [55,56,57]. Chain antioxidants, depending on their physical location inside the food and chemical characteristics, are different in terms of antioxidant effect. The antioxidant chemical power and oil solubility affect the access of proxy radicals, especially in the emulsion, micelle, and membrane systems, because for the effectiveness in these systems, the biophilic property is needed [56,57,58,59]. The best antioxidants have some properties: (1) Give H to oxidation free radicals and become radicals themselves, (2) have phenolic or aromatic rings, and (3) interrupt free radical chain reactions. The radical intermediates are stabilized based on the electron resonance non-establishment in the aromatic ring and the quinone formation [57,58,59,60]. Also, several phenolics lack suitable molecular positions. Propyl gallate, butylated hydroxytoluene (BHT), butylated hydroxyanisole (synthetic antioxidants), and flavonoids (natural plants containing phenolics) work in this way. So, several tissues have developed antioxidant systems to regulate the levels of secondary decomposition products, oxidation mediators, lipid oxidation, and free radicals [59,60,61,62,63]. They are tocopherols, carotenoids, phenolic acids, and flavonoids that act as reducing agents, eliminate free radicals, and inhibit the oxidation. Medicinal plants and herbal NPs have excellent H-donating effects and can have high anticancer properties [64,65,66,67,68,69,70].

Colorimetric tests of Ag NPs that were synthesized from plant extracts were done to confirm the presence of antioxidant compounds in NPs and the NPs’ toxicity effect on different cancer and normal cell lineages. The activity of antioxidants was tested using DPPH tests and the toxicity effect was tested using the MTT method, and all the findings revealed a raise with the increase in the concentration of NPs. In this research, the maximum antioxidant activity was shown at 1,000 μg/mL and above 100%. The findings of the antioxidant test are shown in Figure 9 and Table 2.

Figure 9 
               The antioxidant potentials of Pistacia atlantica extract, BHT and AgNPs.
Figure 9

The antioxidant potentials of Pistacia atlantica extract, BHT and AgNPs.

Table 2

IC50 of Pistacia atlantica extract, BHT, and AgNPs

AgNPs (µg/mL) BHT (µg/mL) Pistacia atlantica extract (µg/mL)
IC50 against DPPH 132 ± 3 77 ± 3 426 ± 6

Several research works have been done on the Pistacia atlantica fruit, known as Bane, in such a way that the fruit extract has been tested on different types of cancer cells. Based on the studies conducted on the methanolic extract of the pericarp of Pistacia atlantica fruit on the breast cancer cell line (T47D), it was found that this extract can induce apoptosis and prevent cell proliferation, and its effect is comparable to that of doxorubicin [71]. In another study by the same group of researchers, to clarify the mechanism of the anti-cancer effect of the skin of Beneh fruit, the effect of the extract on the cell cycle of breast cancer cells (T47D) and the proteins involved in it were analyzed by cytometry and Western blot methods. According to the findings of this research, the anti-cancer activity of Beneh fruit is applied by stopping the cell cycle and greatly decreasing the expression of the genes related to cdk4 and cyclin D1 proteins, which are the mediator proteins in DNA replication and mitosis division [72]. In another study, the effect of the fruit extract of the tuber on the colon cancer cell line (HT29) was compared with that of doxorubicin. In this study, the extract (0.7 mg/mL) had the same activities as that of doxorubicin with a concentration of 500 nM. The mechanism of action is the inhibitory effect on gene expression of cyclin A and cyclin B1 proteins [73]. The ethanolic extract of fruit peel of Beneh has been tested on the prostate cancer cell line (PC3) and normal L929 cells. The findings of this research showed that this extract can prevent the PC3 cells proliferation. This inhibitory effect depends on the duration of the test period and the dose of the extract. It was also found that the extract of the skin of Beneh fruit induces apoptosis in PC3 cells and its cytotoxic effects on PC3 cells are more than normal L929 cells [74]. In addition to this, research has been conducted to assess the effect of the fruit extract on the SK-N-MC (neuroblastoma cell line). In this research, dry fruits were powdered and extracted by methanol and water with a ratio of 70–30 using the percolation method. Examining the compounds of the extract with the HPLC method has shown that terpenoids are the key compounds in the said extract. The mentioned extract has confirmed effects on inhibiting the human neuroblastoma cell line. Since continuous cell division is one of the indicators of cancer cells and microtubule proteins play a key role in these cell divisions, the effect of the extract on the polymerization of microtubules has been tested. Based on the results of this study, it has been found that Beneh fruit extract causes structural changes in tubulin proteins and inhibits the polymerization of microtubules. Based on these results, Beneh fruit has been introduced as a source for the preparation of herbal anti-cancer drugs [75]. Ethanol extract of Pistacia atlantica leaves has been investigated on gastric cancer cells (AGS), uterine cancer cells (HeLa), and skin fibroblast cells (HDFS). The values of IC50 or inhibition of 50% of the growth of cancer cells were determined to be 382 g/m for AGS cells, 332 µg/m for HL cells, and 896 µg/m for HDF cells. According to the mentioned results, Pistacia atlantica leaf extract can inhibit the gastric and uterine cancer cells proliferation [76]. The bark and leaves of the Pistacia atlantica grown in Jordan have also been the subject of research on the anti-cancer effects of this plant. The essential oil obtained from leaves and gall have been tested on colon cancer (HCT116and2-Caco) and breast cancer (T47Dand MCF7) cell lines. In addition, their effects have been investigated in combination with doxorubicin. Both leaf and gall essential oils have been investigated in terms of chemical compounds, monoterpenes with low molecular weight were the dominant compounds of both essential oils, but sesquiterpenes were present in a higher percentage in the leaf essential oil. The comparison of these two essential oils has shown stronger cytotoxic effects of leaf essential oil than gall essential oil in the tested cell lines. In addition, the effects of the drug doxorubicin increase with leaf essential oil, while this effect is not seen in the case of gall essence [77]. A group of researchers conducted a study on Pistacia atlantica resin and investigated its cytotoxic and genotoxic effects on normal and cancer cells. In this study, Pistacia atlantica resin was dissolved in a phosphate-saline buffer containing 5% of DMSO and tested on NIH 33 KB and HUVEC cells. According to the findings of this research, Pistacia atlantica resin has cytotoxic and genotoxic effects on both normal cells and cancer cells. The researchers of this study have suggested that since Pistacia atlantica gum is a natural gum and is also commonly used to treat diseases, in vivo studies should be done to investigate its cytotoxic and genotoxic effects [78].

4 Conclusion

In conclusion, we introduced a method for the green synthesis of AgNPs using Pistacia atlantica bark, as novel procedure without using any harmful and toxic agents. The IC50 of BHT and AgNPs were 77 and 132 µg/mL, respectively. The silver NPs were checked in anticancer potentials against gastric cancer AGS and KATO III cells. The viability of cancer cells reduced in the presence of Ag NPs.

Acknowledgements

The authors extend their appreciation to the Deanship of Scientific Research at King Khalid University for funding this work through large groups under grant number RGP2/227/44.

  1. Funding information: The work was financially supported by Deanship of Scientific Research at King Khalid University (number RGP2/227/44).

  2. Author contributions: All authors equally contributed in conceptualization, data curation, formal analysis, acquisition, investigation, methodology, project administration, resources, software, supervision, validation, visualization, writing – original draft, and writing – review and editing.

  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: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2023-10-31
Accepted: 2023-11-02
Published Online: 2023-11-22

© 2023 the author(s), published by De Gruyter

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

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