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A strategy for the treatment of non-small-cell lung cancer by Ag nanoparticles
⁎Corresponding author. 120131sjk@sina.com (Jing-Kui Shu)
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Received: ,
Accepted: ,
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.
Abstract
This work describes an eco-friendly approach for the green formulation of Ag nanoparticles by Allium ampeloprasum extract, without using any toxic reducing and capping agents. The morphology, structure, and physicochemical properties were characterized by several analytical techniques such as fourier transformed infrared spectroscopy (FT-IR), field emission scanning electron microscopy (FESEM), transmission electron microscopy (TEM), energy dispersive X-ray spectroscopy (EDS), X-ray diffraction (XRD), and Ultraviolet–visible spectroscopy (UV–Vis). The nanoparticles were explored biologically in the anticancer assays. Exposure of the nanoparticles samples to non-small-cell lung cancer cells resulted in cell death, which was mostly due to necrosis but slightly due to late apoptosis. The viability of malignant cell lines reduced dose-dependently in the presence of nanoparticles. The IC50 of nanoparticles were 301, 266, 255, and 250 µg/mL against EKVX, HOP-62, A549 and NCI-H460 cancer cell lines, respectively. The green-synthesized nanoparticles induced cell death, suggesting anticancer prospects that may offer new insight into the development of an anticancer nanomedicine.
Keywords
Ag
Characterization
Plant
Non-small-cell lung cancer
1 Introduction
As the material science progressed, the surface engineered biocomposite nanomaterials have accomplished considerable attention in recent times (Behmaneshfar et al., 2020; Ghanimati et al., 2020). They have been quite useful in diverse applicative fields like disposal of heavy and toxic metals, quenching of dyes, harmful chemicals and environmental toxins, development of bio-engineering systems, optometry, sensing, catalysis and biomedical applications (Shin et al., 2016; Prokop and Davidson, 2008; Khazaei et al., 2020; Shafey, 2020). Today, the desire to use and produce materials with nanometer dimensions is enhancing every day because of the interesting potentials of these nanomaterials. Hence, there are methods to prepare and manufacture nanomaterials, including chemical regeneration, electric arc, laser ablation and microwave waves (Lassalle and Ferreira, 2007; Dehghani et al., 2020; Omidi and Barar, 2014; Orooji et al., 2021; Cao et al., 2017; Kazemi et al., 2018; Moghaddam et al., 2021; Xie and Wang, 2020; Motahharinia et al., 2021). But the nanoparticles resulting from these methods have potential risks for the environment due to dangerous chemical substances, radiation, carrying out reactions in special conditions (pressure and temperature), time-consuming and expensive materials. Therefore, the need for a low-cost method of producing toxic substances without environmental damage is increasing (Motahharinia et al., 2021; Lim et al., 2018; Miele et al., 2009; Bharamanagowda and Panchangam, 2020). One of the producing nanoparticles main methods is biological (green) production. Recently, considering this method to produce nanoparticles is increasing. For example, among the efforts that have been made for the biosynthesis of nanoparticles is the production of nanoparticles by microorganisms (Bharamanagowda and Panchangam, 2020; Jędrzak et al., 2018; Sadjadi et al., 2020). Both live and dead microorganisms are specific importance for nanoparticles production. Also, microorganisms can solve simultaneously the synthesis nanoparticles problems and their stabilization (Karimi-Maleh et al., 2021; Anbu et al., 2019; Hajiahmadi et al., 2019; Sun et al., 2017). In the silver nanoparticles synthesis by chemical method, it may cause to some toxic species presence absorbed on the nanoparticles surface, which will have side effects in medicine and applications. Synthesis by microorganisms can potentially solve this problem (Anbu et al., 2019; Hajiahmadi et al., 2019; Sun et al., 2017; Karimi-Maleh et al., 2021 Jul). Several methods have been provided for the green synthesis productivity of nanoparticles. Because metal nanoparticles using green agents have attracted much attention because of their special chemical, optical, electronic and photoelectrochemical properties. Also, the synthesis of nanoparticles in a green way is a non-toxic, clean and friendly environmental way that is related to several organisms such as fungi, batteries, plants and yeast (Sun et al., 2017; Beheshtkhoo et al., 2018). Therefore, both unicellular and multicellular organisms were used for nanomaterials extracellular and intracellular production. Recent researches have indicated that the medicinal plants used for synthesizing the silver nanoparticles increase their anticancer effects without any cytotoxic effects on normal cells (Anbu et al., 2019; Hajiahmadi et al., 2019; Sun et al., 2017). In this study, we decided to continue our further exploration with Ag nanoparticles containing plant extract in the bio-assays regarding the cancer cells.
2 Experimental
2.1 Preparation of aqueous extract
After preparing the plant leaves, they were dried away from sunlight. After grinding the plant, extraction was done from the plants. In this way, 15 g of the plant powder obtained was poured into an Erlenmeyer flask and soaked in 200 ml of distilled water for 3 days. After straining the obtained solution with a strainer, the evaporation of the solvent was done in wide plates on a bain-marie at a temperature of 40–50 °C. Then, a solution with a concentration of 10 mg/ml of DMEM medium was prepared for the remaining solid material. This extract was used for experiments.
2.2 Synthesis of Ag NPs
To synthesize the AgNPs, 50 ml of plant extract with a concentration of 0.02 g/mL was poured into a flask containing AgNO3 (100 ml, 0.1 M). For the next step, the reaction mixture was stirred at 40 °C for 24 h. The nanoparticles were formed during the reaction time as brown precipitates. The nanoparticles were washed with water four times and centrifuged at 12000 rpm for 12 min. Afterward, AgNPs were dried at room temperature. Finally, the formed dark brown powder was kept in a vial to evaluate chemical characterization and its biological activity. Different factors of the nanoparticles like shape, particle size, fractal dimensions, crystallinity, and surface area are characterized by FT-IR and UV–Vis spectroscopy, and SEM. In the present study, the FT-IR spectra of the synthetic nanoparticles were recorded by a Shimadzu FT-IR 8400 ranging from 400 to 4000 cm−1(KBr disc); The FE-SEM images were reported using MIRA3TESCAN-XMU.
2.3 Antioxidant assay protocol
DPPH reactive solution was prepared by dissolving 1 mg DPPH powder in 17 ml ethanol. Then several dilations of nanoparticles were prepared by dissolving nanoparticles in distilled water. Finally, the reaction solution was prepared from the combination of 500 µl of DPPH reaction solution with 500 µl of different concentrations of nanoparticles and was placed in the dark for 40 min and the resulting absorbance was measured at 517 nm using a spectrophotometer (Hamelian et al., 2019; Hamelian et al., 2020; Zangeneh, 2020; Zangeneh et al., 2019; Zangeneh et al., 2019; Zangeneh et al., 2019; Zangeneh et al., 2019; Mahdavi et al., 2019).
2.4 MTT assay protocol
In this study, the anticancer effects of Ag NPs samples against the non-small-cell lung cancer cells (EKVX, HOP-62, A549 and NCI-H460) were investigated.
Cancer cell lines were placed in 1640-RPMI medium from GiBco manufacturer and were cultured after adding 10% bovine serum, 1% streptomycin and penicillin antibiotics and 2% glutamine. At this stage, the cell culture flasks were kept in an incubator with 5% CO2 and 95% humidity at a temperature of 37 °C, and the culture medium was replaced every three days. In this step, flasks with 80% cell density were used (flasks filled with cells up to 80% of the bottom). First, the culture medium was removed from the surface of the cells and by adding 1 ml of trypsin for 3 min and then adding the same volume of medium to neutralize the effect of trypsin, all cells were separated from the flask bottom. This cell suspension was centrifuged at 1200 rpm for 4 min. The liquid above the sediment was discarded and 1 ml of culture medium was added to the sediment. By taking 10 µl of the cell suspension and adding the same amount of trypan blue on the surface of the neobar slide, the number of living cells was counted. The number of 10,000 cells from this cell suspension was added to each well of 96-well plates and 180 µl of culture medium was added to it. In the next step, 20 µl different concentrations of nanoparticles were added to the wells. In this research, based on the conventional concentrations of nanoparticles at the 0–1000 µg/ml, they were added to cancer cells. Another group of cells were tested as a control, without adding nanoparticles and only by adding water instead of nanoparticles, and each experiment was done in four replicates. After 24, 48 and 72 h, the medium on the cells was replaced with a new medium. Then 20 µl MTT solution was added to each well and placed in a greenhouse for 4 h in the dark in a CO2 incubator. During this time, the mitochondrial succinate dehydrogenase enzyme of living cells changes the yellow MTT solution into purple formazan crystals, which are insoluble in water. In the next step, 200 µl of DMSO (Dimethylsulfoxide) was added to the empty medium and shaken for 20 min to dissolve the light-producing crystals. In the last step, the absorbance was read with a wavelength of 492 and then 630 nm in an ELISA reader. Finally, the percentage of cell viability was calculated after dividing the optical absorbance (OD) of treated cells compared to control cells and multiplying by 100 (Hamelian et al., 2018; Hamelian et al., 2019; Hamelian et al., 2020; Mohammadi et al., 2020; Ahmeda et al., 2020; Zangeneh, 2020; Jalalvand et al., 2019).
2.5 Statistical analysis
The results were evaluated as Mean ± SE using SPSS software version 12 and statistical tests of variance of completely randomized block design. Drawing graphs in Excel software was performed and the significance level of the differences was considered p < 0.01.
3 Results and discussion
Cancer is one of the leading causes of death, characterized by uncontrolled growth and abnormal cell proliferation. Cancer is caused by external factors such as chemicals and tobacco, as well as internal factors such as genetic mutations and hormones. Cancer is usually diagnosed 10 years or more after exposure to chemicals (Gao et al., 2015; Mohammed et al., 2016; Li and Gu, 2014; Yang et al., 2011). Cancer is treated with various methods such as surgery, radiation therapy and chemotherapy. One of the main causes of high cancer mortality is the inability to deliver targeted drugs to cancer cells without side effects on healthy cells. It seems that nanotechnology can be a good solution to this problem. Unique properties of nanoparticles such as particle size, high surface-to-volume ratio, their targeting ability, loading ability of water-insoluble drugs and controlled release, and responsiveness to the stimulant drug can make them a good candidate for cancer treatment (Xinli, 2012; Allen, 2002; Yona and Gordon, 2015; Liang et al., 2021; Tran et al., 2017; Hu et al., 2019). When the nanoparticles are injected into the bloodstream, they need to pass through the walls of the arteries to reach the target site and then release the drug. Unlike small molecules, nanoparticles, because of their relatively large size, cannot pass through the tight connections between the endothelial cells of healthy blood vessels (Li and Gu, 2014; Yang et al., 2011; Xinli, 2012; Allen, 2002; Yona and Gordon, 2015). Tumor blood vessels, due to their leaky walls, allow nanoparticles to pass well. Targeted drug delivery to the tumor by nanoparticles is done in both passive and active targeting. In passive targeting, tumor tissue properties are used for drug delivery. In tumor tissue, due to rapid cell growth, rapid angiogenesis occurs, but the distance between vascular endothelial cells is too large, causing macromolecules and nanoparticles to leak from blood vessels into tumor tissue (Allen, 2002; Yona and Gordon, 2015; Liang et al., 2021). On the other hand, the lymphatic system of tumor tissue is not complete and is not able to collect nanoparticles and insert them into the bloodstream; As a result, nanoparticles accumulate in the tumor tissue and release their drug (Yona and Gordon, 2015; Liang et al., 2021; Tran et al., 2017; Hu et al., 2019). For passive targeting, the nanoparticle size should usually be below 200 nm. Active targeting of the tumor is achieved by binding a ligand such as antibodies, peptides, aptamers and some small molecules such as folic acid to nanoparticles (Feng et al., 2017; Wu et al., 2011; Brigger et al., 2002; Desai et al., 1996; Zang et al., 2017; Quazi, 2021).
Regarding cancer, efforts have been made to use smart nanomaterials (nanoparticles, nanostructures), which have a greater ability to target cancer cells, to treat such patients. That is, they kill malignant cells by irradiating them, providing a microscopic therapeutic effect within electrons (Quazi, 2021; Yan et al., 2020; Paulis et al., 2013; Shao et al., 2015; Yang et al., 2018). Nanoparticles are programmed to achieve optimal therapeutic efficacy, delivering therapeutic loads to target cells. Studies have also been performed on several nanocarriers based on lipids, polymers, and peptides for delivery to the respiratory system (Guo et al., 2015; Fontana et al., 2017; Perica et al., 2014; Bauleth-Ramos et al., 2017). Properties of nanoparticles for targeted delivery of nanoparticles to tumors is the motivation for targeted drug delivery in cancer treatment to kill cancer cells. In a way, that has the least damage to healthy cells (Bauleth-Ramos et al., 2017; Liu and Sun, 2021; Will and Purkayastha, 2006; Harada et al., 2007; Schroeder et al., 2012; Gobbo et al., 2015). One of the nanotechnology goals is to mount drugs on carriers, send them and release them into the target cell, which is called targeted drug delivery. Using nanoparticles, the drug can be intelligently delivered to the desired tissue, and improve the tissue without damaging other tissues (Bauleth-Ramos et al., 2017; Liu and Sun, 2021; Will and Purkayastha, 2006; Harada et al., 2007; Schroeder et al., 2012; Gobbo et al., 2015; Sankar et al., 2014).
In this study, we strategically synthesized the Ag nanoparticles following a post-modification approach. Structural features of the nanoparticles were determined with several physicochemical techniques like FT-IR, SEM, TEM, EDX, XRD, UV–Vis.
Fig. 1 shows the FT-IR spectrum of nanoparticles. The bands at 493, 571 and 623 cm−1 (belong to Ag-O bond) that approves the producing of silver nanoparticles. Furthermore, there is a similarity between silver nanoparticles FT-IR spectrum and green synthetic nanoparticles using plant extract. The peaks at other regions including 3372 and 2928, 1382 to 1627, and 1063 belong to the different bonds of organic compounds in plant extract such as phenolic, flavonoid, triterpenes, which were reported previously.
FT-IR spectra of nanoparticles.
The surface morphology, texture and shape of the unmodified nanoparticles were ascertained by FE-SEM analysis, being in Fig. 2. The particles are on average quasi-spherical shaped and can be separately detected. The globular dots are generated within nanometric range having particle sizes between 27 and 64 nm. From the image of nanoparticles, the material is evidently a combination of its components where the additives have been immobilized over the plant surface.
FE-SEM image of nanoparticles.
The qualitative analysis of EDX was run to screen the elemental analysis of nanoparticles. The EDX diagram of nanoparticles is shown in Fig. 3 The findings approved the appearance of silver (by the peaks at 3.02 keV for AgLα and peak at 3.19 keV for AgLβ), oxygen (by the peak around 0.5 keV for OLα), and carbon (by the peak around 0.3 keV for CLα) in nanoparticles. The presence of oxygen and carbon approved the linkage between nanoparticles and organic compounds of the plant extract.
EDX of nanoparticles.
In the recent study, Fig. 4 exhibits the UV–Vis. spectrum of nanoparticles. The band at 441 nm approves the formation of the silver nanoparticles.
UV–Vis of nanoparticles.
The FE-SEM data were further justified and more intrinsically studied by TEM analysis. Fig. 5 displays the resultant image of nanoparticles. The particles are invariably globular shaped. A thin layer of plant extract over the particle surface can be noticed. The dark colored Ag NPs are also round shaped and are almost same sized to ferrite NPs in the range of 19–62 nm.
TEM image of nanoparticles.
The analysis of the XRD diffraction pattern is known as a method to study different compounds including metallic nanoparticles. The XRD pattern of the green synthesized nanoparticles is exhibited in Fig. 6. The result has approved the crystallinity of nanoparticles with a small size. The data for 2θ values has been matched to the standard database of JCPD card 04–0783. The signals at 2θ of 37.8, 65.1, and 77.4 belonged to the planes 111, 220, and 311 respectively. The crystal size of 51.27 nm was measured for the NPS using Scherer’s equation.
XRD profile of nanoparticles.
The treated cells with different concentrations of the present nanoparticles were assessed by MTT assay for 48 h about the cytotoxicity properties on normal (HUVEC) and EKVX, HOP-62, A549 and NCI-H460 cancer cells (Table 1; Figs. 7-9).
Nanoparticles (µg/mL)
IC50 against HUVEC
–
IC50 against EKVX
301 ± 0a
IC50 against HOP-62
266 ± 0a
IC50 against A549
255 ± 0b
IC50 against NCI-H460
250 ± 0b
The anticancer properties (Cell viability (%)) of nanoparticles (Concentrations of 0–1000 µg/mL) against EKVX and HOP-62 cell lines.
The anticancer properties (Cell viability (%)) of nanoparticles (Concentrations of 0–1000 µg/mL) against A549 and NCI-H460 cell lines.
The cytotoxicity effects of nanoparticles against normal (HUVEC) cell line.
The viability of malignant prostate cell lines reduced dose-dependently in the presence of nanoparticles. The absorbance rate was evaluated at 570 nm, which represented viability on normal cell line (HUVEC) even up to 1000 μg/mL for nanoparticles (Table 1; Fig. 9).
Nanoparticles have several compounds, each with a different structure. The extraction of these compounds depends on several factors, the most important of which are the type of solvent and the extraction method. It will be very difficult to choose a solvent for any group of nanoparticles compounds, because with these compounds, there are other substances that affect the degree of solubility of these substances (Sankar et al., 2014). When extracting nanoparticles, it should be noted that always use a method that has the best performance in the survival of antioxidant compounds. Usually nanoparticles have unique antioxidant effects (Katata-Seru et al., 2018). Recent studies have shown that when the plant extracts are placed in metal nanoparticles as stabilizing and reducing compounds, they form nanocomposites with extraordinary antioxidant effects. Antioxidants are generally referred to as substances that can delay, slow down, and even stop oxidation processes (Bauleth-Ramos et al., 2017; Liu and Sun, 2021; Will and Purkayastha, 2006; Harada et al., 2007; Schroeder et al., 2012; Gobbo et al., 2015). These compounds can optimally prevent changes in the color and taste of food because of oxidation reactions. The antidote to the mechanism of oxidants is that they prevent the spread of oxidation chain reactions by giving hydrogen atoms to free radicals. In recent years, the synthetic antioxidants use such as BHT, BHA, TBHQ as well as other chemical additives has been limited due to their potential toxicity and carcinogenicity. Today, most research in this area focuses on the use of new and safe antioxidants from plant, animal, microbial and food sources (Schroeder et al., 2012; Gobbo et al., 2015; Sankar et al., 2014; Katata-Seru et al., 2018). In the recent study, the scavenging capacity of nanoparticles and BHT at different concentrations expressed as percentage inhibition has been indicated in Table 2 and Fig. 10. In the antioxidant test, the IC50 of nanoparticles and BHT against DPPH free radicals were 191 and 74 µg/mL, respectively (Table 2).
Ag NPs (µg/mL)
BHT (µg/mL)
IC50 against DPPH
191 ± 0b
74 ± 0a
The antioxidant properties of Ag NPs and BHT against DPPH.
4 Conclusion
This work describes an eco-friendly approach for in situ immobilization of Ag nanoparticles containing Allium ampeloprasum extract, without using any toxic reducing and capping agents. The structure, morphology, and physicochemical properties were characterized. In addition, nanoparticles have good cytotoxicity effect against cancer cell lines. Our results showed that biosynthesized nanoparticles induced a concentration-dependent cytotoxicity in EKVX, HOP-62, A549 and NCI-H460 cancer cells. The green-synthesized nanoparticles induced cell death, suggesting anticancer prospects that may offer new insight into the development of an anticancer nanomedicine.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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