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Exploring the effect of silver nanoparticles on gene expression in colon cancer cell line HCT116

  • Hussah M. Alobaid , Maha H. Daghestani , Nawal M. AL-Malahi , Sabah A. Alzahrani , Lina M. Hassen and Dina M. Metwally EMAIL logo
Published/Copyright: December 10, 2022
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Green Processing and Synthesis
From the journal Green Processing and Synthesis Volume 11 Issue 1

Abstract

This study describes a new green method for silver nanoparticles (AgNPs) using Cymbopogon proximus (CP) extract and evaluates their potential anticancer properties in HCT116 cells. Ultraviolet-visible spectroscopy, transmission electron microscopy, dynamic light scattering, and Fourier transform infrared (FTIR) spectroscopy were used to successfully analyze the AgNPs. FTIR spectral analysis revealed the presence of phytochemicals that could be responsible for silver (Ag) ion reduction and AgNP capping. The 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide assay demonstrated that treating HCT116 cells with PC-AgNPs for 48 h caused cytotoxic effects, as evidenced by the existence of 20% cell viability. The RT-qPCR study revealed that the expression of two oncogenes (cathepsin B [CTSB] and epithelial cell adhesion molecule [EpCAM]) was significantly reduced in treated cells. The levels of various tumor suppressor genes, including adenomatous polyposis coli (APC), Beclin1 (BECN1), nuclear translocation of β-catenin (CTNNB1), low-density lipoprotein receptor-related protein 6, LRP5, TP53, and TNF, were dramatically reduced in cells treated with CP extract, but this was not the case in cells treated with CP extract. To conclude, CP-AgNPs have demonstrated their ability to induce cytotoxic action and exert antitumorigenic modulatory effects, particularly on the expression of CTSB and EpCAM in colon cancer cells, utilizing AgNPs as an antitumor therapeutic agent for 48 h is not recommended, and reducing the treatment time could be more effective.

Keywords: silver nanoparticles; HCT116; Cymbopogon proximus

1 Introduction

Colorectal cancer (CRC) is a slow-developing cancer that begins as an abnormal tissue growth on the inner epithelial linings of large intestines [1,2]. If this growth becomes cancerous (polyp), it can form a tumor on the interior walls of the colon or rectum [1]. Subsequently, this tumor will grow into blood vessels or lymph vessels, increasing the chance of metastasis to other anatomical sites [2]. CRC is considered the third most lethal cancer worldwide [3,4], representing the fourth most happening malignancy among all ages and for men and women combined [3,4]. According to Saudi Cancer Registry in Saudi Arabia (KSA), CRC has been ranked first in incidence among Saudi males and third among Saudi females for the last several years. The rate among males was 19.3%, and among females was 9.2% [5]. Although the cases of CRC in KSA are lower when compared to the western population, it seems to be increasing during the past few years [6,7,8].

Most CRC originates because of multifactorial causes; however, the interaction between genetic and environmental factors plays the most significant role. It can be attributed to the increasingly aging population, unfavorable modern dietary habits, and increased risk factors such as smoking, alcohol consumption, high-fat diet, low physical exercise, and obesity [9]. Risks are dramatically increased for individuals who inherit the gene mutations responsible for familial adenomatous polyposis or hereditary nonpolyposis CRC [7,10].

Approximately 85% of CRC have a mutation in multiple genes. These are adenomatous polyposis coli (APC), tumor protein 53 (TP53) [11], Beclin1 (BECN1), and epithelial cell adhesion molecule (EpCAM) [12]. Studies showed that the loss of function of the APC gene interacts with the CTNNB1 (nuclear translocation of β-catenin) [13]. This interaction leads to triggering the Wingless-related integration site (Wnt signaling pathway). These findings directly link Wnt signaling and human CRC [14,15,16]. An important co-receptor of the Wnt pathway is low-density lipoprotein receptor-related protein 6 (LRP6), which forms a signalosome along with a Wnt ligand to activate the downstream signaling pathway [17]. According to the previous study, LRP6 contributes to the progression of CRC and certain other cancers [18]. In CRC, however, the mechanism underlying LRP6 is rarely investigated. Tumor formation and metastasis are influenced by BECN1. A marked increase was observed in the motility and invasion of CRC cells when BECN1 was knocked down. BECN1 negatively regulates CRC metastasis in an autophagy-independent manner through STAT3 signaling pathway activation. Potential therapeutic targets for metastatic CRC include the BECN1/Janus kinase 2 (JAK2)/signal transducer and activator of transcription 3 (STAT3) signaling pathway [19]. In normal cells, cathepsin B (CTSB) is a peptidase that functions in endo-lysosomal compartments [20]. CTSB production can be altered at multiple levels during malignant transformation, resulting in the overproduction of the enzyme, which plays a crucial role in several pathologies and oncogenic processes [21]. A malignant transformation of tumor cells can alter the regulation of CTSB at multiple levels, resulting in enhanced local release [21,22]. In theory, CTSB may be used to treat and chemoprevention of neoplasms and molecular detection [23]. A previous study demonstrated that human CRC cells treated with Ca074 showed enhanced invasiveness after being treated with the highly selective and non-permeant cathepsin B inhibitor [22]. Studies also demonstrated that CRC is associated with overexpression in a tumor-suppressive protein (EpCAM) [12].

CRC survival rates remain below 10% despite new treatments. Consequently, many research efforts are devoted to understanding metastasis, identifying biomarkers, and developing therapeutic targets for CRC [24]. Researchers and clinicians have developed various methods to prevent or inhibit cancer growth in the last three decades. The common types of cancer treatment are surgery, chemotherapy, radiotherapy, immunotherapy, hormone therapy, and photodynamic therapy. Despite the progress in our knowledge about cancer, current strategies for cancer treatment are not very effective. For instance, chemotherapy and radiotherapy damage the cancer cells and other healthy cells in the body [25]. FOLFOX is the most successful standard chemotherapy treatment for CRC [26], despite that, it has severe side effects (e.g., gastrointestinal and neurotoxicities) [26]. Thus, scientists are still trying to find a new biocompatible and more effective method for cancer treatment using nanotechnology and natural products.

Nanotechnology is an important field of modern research dealing with particle structure design, synthesis, and manipulation [27]. In recent years, silver nanoparticles (AgNPs) have drawn more attention to their significant biological role against microorganisms [28]. It was found that AgNPs exhibited both positive and negative effects on well-developed multi-organ systems, including humans and rats. However, the general consensus states that capped (bio)molecules have synergistic bioactivities and can reduce its toxicity. Yet, there is no convincing evidence to support this claim [29,30]. These particles have a considerable surface area compared to raw silver particles ranging from 1 to 100 nm in one dimension. This feature could provide promising and novel chemical property in their nanoscale size [26,29]. The AgNPs are the most commercialized and prominent group of nano-compounds due to their diverse applications in the health sector [30]. These particles can be prepared easily by different chemical, physical, and biological approaches [31]. However, the biological approach is the most emerging approach to preparation. This is because it is easier, cost-effective, eco-friendly, and less time-consuming and does not involve any toxic chemicals as other methods [31,32].

Combining AgNPs with plant extracts can result in AgNPs with better characteristics. This is due to the synergistic action of both AgNPs and the bioactive compounds found in plants. As a result, plant-mediated AgNPs are more physiologically active than standard AgNPs [33,34]. Several medicinal herbs have been used to synthesize AgNPs. Cymbopogon proximus (CP) (Gramineae) is a herbal plant, commonly known as “camel’s hay” and locally as Maharaib, Halfa-bar Sakhbar, or Athkhar [34,35,36]. CP is widely distributed in the Middle East, Africa, temperate Asia, western Asia, and tropical Asia [37]. CP plant is traditionally used as an addition to tea, diet, and medicine. The medicinal properties of CP grass are to treat intestinal spasms, stomach disorders, bowel irritation, dyspepsia, and diarrhea [35,37]. The most important active compounds of CP are terpenes and saponins, which have cancer chemopreventive effects, antimicrobial, antifungal, antiviral, antihyperglycemic, anti-inflammatory, and anti-inflammatory antiparasitic activities [38].

This study aimed to characterize the green-synthesized AgNPs from the CP extract using ultraviolet-visible (UV-Vis) spectroscopy, transmission electron microscopy (TEM), dynamic light scattering (DLS), and Fourier transform infrared (FTIR) techniques and, then, assess its potentiality to be anticancer by studying the cytotoxic effects of CP extract and CP-AgNPs and the expression levels of oncogenes APC, BECN1, CTNNB1, LRP6, LRP5, tumor necrosis factor (TNF), tumor protein 53 (TP53), CTSB, and EpCAM on CRC cell line (HCT116).

2 Materials and methods

2.1 Plant extract preparation

Fresh grasses of CP were collected from a local market. Around 10 g of the plant was thoroughly washed with sterile double distilled water two to three times until all impurities were removed. They were then boiled for 20 min in 150 mL of distilled water and left to be cooled at room temperature overnight. Then, they were filtered and stored at 4°C until required for further analysis (Figure 1a).

Figure 1 The green synthesis of AgNPs: (a) the aqueous plant extract. (b) Mixture of AgNO3 with aqueous extraction of CP. (c) Characterization of AgNPs using the UV-Vis spectroscopy.
Figure 1

The green synthesis of AgNPs: (a) the aqueous plant extract. (b) Mixture of AgNO3 with aqueous extraction of CP. (c) Characterization of AgNPs using the UV-Vis spectroscopy.

2.2 Synthesis of AgNPs

Five milliliters of aqueous plant extract prepared above were added to 50 mL of 1 mM of aqueous silver nitrate solution (AgNO3). The reaction mixtures were stirred under a vigorous stirrer with heat for 3–5 h (at 80°C). The change in the reaction mixtures was monitored to determine the nanoparticle formation (Figure 1b).

2.3 Characterization of AgNPs

The synthesized leaf extract AgNPs were characterized using different techniques detailed subsequently.

The UV-Vis spectrophotometer (PerkinElmer LS 40, USA) was used to evaluate the formation of AgNPs at wavelengths ranging from 300 to 600 nm (Figure 1c). The morphology and average size of the synthesized AgNPs were determined by TEM (Figure 2). The TEM images of synthesized AgNPs were obtained using a JEOL JEM-2100 (JEOL Ltd., Tokyo, Japan) high-resolution TEM operated at an accelerated voltage of 200 kV. An electron beam is imaged in this method while it passes through a thin sample (less than 100 nm). A detector is then used to visualize objects smaller than a nanometer based on the transmitted beam. Before analysis, AgNPs were sonicated for 5 min, and a drop of appropriately diluted sample was placed onto a carbon-coated copper grid. The liquid fraction was allowed to evaporate at room temperature. The hydrodynamic size and zeta potential of the synthesized CP-AgNPs were measured by the DLS technique using a zetasizer device (Malvern, Worcestershire, UK; Figure 3).

Figure 2 TEM image of nanoparticles. A graph of a TEM image of AgNPs at a magnification level of 100 nm.
Figure 2

TEM image of nanoparticles. A graph of a TEM image of AgNPs at a magnification level of 100 nm.

Figure 3 DLS measurement reveals the zeta potential value of CP-AgNPs (a) and hydrodynamic size (b).
Figure 3

DLS measurement reveals the zeta potential value of CP-AgNPs (a) and hydrodynamic size (b).

Further characterization was done using FTIR (Nicolet 6700, FTIR, Thermo Scientific, Waltham, MA, USA) spectral measurements to detect the functional group responsible for reducing ions to AgNPs. This was done by mixing 300 µL of the air-dried AgNPs with 10 mg potassium bromide and then oven dried. The FTIR spectra were taken at the range of 500–4,000 cm−1 and a resolution of 4 cm−1.

2.4 Cell culture preparation

A human colorectal carcinoma cell line (HCT116) was commercially bought from American Type Culture Collection. The cells were routinely cultured in Dulbecco’s modified Eagle’s medium, 10% heat-inactivated fetal bovine serum, 100 U·mL−1 penicillin, 0.1 mg·mL−1 streptomycin, and 1% glutamine. The cells were seeded in 96-well plate at a 2 × 105 cell·well−1 density in 100 µL of optimized medium and incubated at 37°C and 5% CO2. The total number of cells used in the different experiments was determined by the trypan blue exclusion test (0.4%) using a cell counter.

2.5 Cytotoxicity assay

The cytotoxicity of synthesized AgNPs against HCT116 cells was measured by the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay (kit from UFC Biotechnology). After culturing the cells, they were allowed to settle for 24 h before being treated with an individual concentration of CP extract and synthesized CP-AgNPs (3.125, 6.25, 12.5, 25, 50, and 100 µL). Treated cells were allowed to grow further for 48 h. At the end of the incubation period and concentration point, 100 µL of 0.22 μm filter-sterilized MTT (Sigma Aldrich, UK) was added at 37°C at a final concentration of 5 mg·mL−1. The 96-well plate was kept in the dark for 2 h before the medium containing MTT was removed. One hundred microliters of dimethyl sulfoxide (Ajax Finechem Pty Ltd, Australia) were added to dissolve formazan crystals. The 96-well plate was also shaken for 15 min in the dark to help dissolve the formazan crystals. Each treatment’s optical density (OD) was measured at an absorbance of 490 nm using a 96-well plate reader (Molecular Devices – SPECTRA max – PLUS384). Each experiment was performed in four replicates. Values of OD were normalized according to the control (untreated cells). Therefore, cell viability values of untreated cells should be 100%, while values of treated cells are below or above 100%.

2.6 Total RNA extraction and cDNA synthesis

A high-capacity cDNA reverse transcription kit (Applied Biosystems, Thermo Fisher Scientific, USA) was used to perform reverse transcription in the Veriti 96 Well Thermal Cycler. Cultured cells at a density of 2 × 105 cells·well−1 in six-well plates were treated with different concentrations of CP extract as crude and CP-AgNPs for 48 h. Then, the total RNA was extracted following the RNeasy Plus Mini kit (Qiagen). The purity and quantity of total RNA were measured using NanoDrop Spectrophotometer (Thermo Scientific), and its integrity was examined using the gel agarose electrophoresis, as detailed here [39].

2.7 Real-time polymerase chain reaction (RT-PCR)

For the genetic evaluation of the effect of CP-AgNPs, the expression levels of APC, CTNNB1, BECN1, CTNNB1, LRP6, TNF, CTSB EpCAM, and TP53 were determined using RT-PCR. It was performed by QuantiTect SYBR Green PCR Kit (Qiagen, Cat # 204143, USA) and the Applied Biosystems ViiA7 (Life Technologies), and the instruction manual of Real-Time-Gene was followed. β-Catenin gene is mutant in HCT116 [40].

2.8 Statistical analysis

The Statistical Package for the Social Sciences (SPSS) software (version 20.0) was used for data obtained from particle size analysis and cell availability assay. ANOVA and t-test were used to analyze the differences between the groups, and p < 0.05 was considered significant. For each parameter, mean ± SD for at least three independent experiments was calculated.

3 Results

3.1 Characterization of AgNPs with CP

The formation of synthesized CP-AgNPs is presented in Figure 1. The colorless solution of AgNO3 turned dark brown after being mixed with the yellow aqueous extract of CP within 24 h. An examination of the UV-Vis spectrum reveals a significant peak value at 432.5 nm (shown in Figure 1b). The shape and size of AgNPs were determined by the TEM and shown to be predominated by spherical-shaped morphologies (Figure 2). They ranged from 6 to 44 nm with an average size of 21.2 nm. The small relative size of CP-AgNPs indicates their nanocrystalline nature. This, in turn, supports their high catalytic and accumulation properties in the tumor area [41]. The formation of monodispersed particles was confirmed by measuring the hydrodynamic size of CP-AgNPs via zetasizer. As shown in Figure 3a, the zeta potential value was −0.684 mV, and its size was 139.9 diameter value of nanometer with 0.250 PDI (Figure 3b). The functional biomolecules in the CP extract were identified using FTIR spectral measurements in a wavelength range of 4,000–400 cm−1. These biomolecules are responsible for the reduction of the bio-reduced AgNPs. As shown in Figure 4, the pattern of peaks of both CP and CP-AgNPs reveals the binding of the silver ion with carboxylic and amide groups of CP, and the multiple peaks represent its complicated nature.

Figure 4 The spectra of AgNPs were recorded in the wavelength range of 4,000–400 cm−1 via FTIR.
Figure 4

The spectra of AgNPs were recorded in the wavelength range of 4,000–400 cm−1 via FTIR.

3.2 MTT assay

This test was conducted to assess the percentage of viable cancer cells treated with different concentrations of PC as either AgNPs or crude for 24 h of the control sample (100%) (Figure 5). The present study obtained the minimum inhibitory concentration (IC50) of AgNPs on the experimental cells at 25 µL. Exposure to increasing concentration of AgNPs exhibits significant dose-dependent anticancer activity in CRC cells. As shown in Figure 5, both crude and AgNPs significantly reduced the number of cancer cells, but the effect of AgNPs was more significant than the effect of the crude (compare Figure 5a and b).

Figure 5 Impact of various concentrations of CP-AgNPs (a) and plant extract (crude) (b) on the cell viability in HCT116 cells.
Figure 5

Impact of various concentrations of CP-AgNPs (a) and plant extract (crude) (b) on the cell viability in HCT116 cells.

3.3 RT-PCR

The expression levels of the indicated genes were measured in HCT116 cells using quantitative RT-PCR. The cells were treated with 6.25 μL of CP aqueous extract and 25 μL of synthesized CP-AgNPs for 48 h. Results showed that the expression level of APC, BECN1, CTNNB1, TNF, and TP53 was abrogated entirely in cells treated with NPS (p ≤ 0.05), whereas cells treated with the crude significantly increased the levels of both APC and CTNNB1 compared to the control (p ≤ 0.05) (Figure 6a–e). In the same way, treating cells with NPs inhibited remarkably the expression level of both LRP6 and LRP5 (Figure 6f and g). However, the inhibition was significant in the former (p ≤ 0.05) and non-significant in the latter, despite the reduction being around ∼30% (p > 0.05). The CTSB and EPCAM genes are shown in Figure 6h and i that treating cells with 6.25 μL-CP aqueous extract or 25 μL-synthesized CP-AgNPs has induced a downregulation effect (p < 0.05) by suppressing the expression level of both genes.

Figure 6 The expression levels of (a) APC, (b) BECN1, (c) CTNNB1, (d) TNF, (e) TP53, (f) LRP6, (g) LRP5, (h) CTSB, and (i) EPCAM.
Figure 6

The expression levels of (a) APC, (b) BECN1, (c) CTNNB1, (d) TNF, (e) TP53, (f) LRP6, (g) LRP5, (h) CTSB, and (i) EPCAM.

4 Discussion

There has been a tremendous interest in using AgNPs as a drug carrier, cancer treatment, nanotechnology, and the field of biomedicine [42]. AgNPs’ synthesis strategies have evolved in the past few decades to develop eco-friendly and cost-effective synthesis methods [42,43,44]. This study developed a nano-drug using CP and assessed its anticancer activity against CRC cells (HCT116). The changing color of AgNO3 solution within 15 min indicates the reduction of the Ag ion to AgNPs. Furthermore, we applied multiple methods to evaluate the formation of green synthesis of AgNPs. The UV-Vis spectroscopy revealed a strong absorption peak at 432.5 nm of the CP-AgNPs, the highest absorbency due to their reduced AgNO3 content, and surface plasmon resonance [45]. The TEM images validate the spherical shape of CP-AgNPs, and they have an average size of 21.2 nm. A significant aggregation of the nanoparticles was also observed. This could have been caused by the coating (capping agents) that covers the NPs. This causes the NPs to be attached, resulting in a decreased space between the NPs [46,47]. The FTIR confirmed that the proteins bind to the metal NPs strongly that they form a coating on the AgNPs. The DLS results indicate variation in dimensions of AgNPs. Therefore, the results suggest that the CP extract may serve a dual purpose by forming and stabilizing AgNPs in aqueous solutions.

CRC is a heterogeneous disease caused by genetic and epigenetic alterations in cells, transforming from an adenoma to carcinoma. Globally, it is ranked second as the most frequent type of cancer-related mortality [48]. To the best of our knowledge, no study has examined the chorionic effect of this extract on CRC in the form of NPS. The cytotoxic study suggested a proliferative effect of PC extract as crude and PC-AgNPs against cancerous cells (HCT116) (Figure 5). The observed effect of AgNPs could be linked to their capacity to activate reactive oxygen species in cells, triggering oxidative stress (OS), or related to modulation by autophagy and thereby causing cell death [49,50]. A growing number of studies highlight the significant impact of AgNPs in inducing a dose-dependent cytotoxicity effect in LoVo cells (a large intestine cell line) [41] and in HCT116 cells ( a colon cancer cell line), which were treated with AgNPs of naringenin [51] or Chaetomorpha linum for 24 h [52]. Moreover, leaves and extracted oil have been reported to have antioxidant activity, which may explain the observed activity in the cancer cell lines [35].

The analysis of molecular studies showed a significant alteration in the expression levels of oncogenes in treated cancer cells compared to the control. The results herein showed that the effect of the plant extract as crude was more efficient than NPs in enhancing these genes. Indeed, treating cells with PC-AgNPs abrogate the expression levels of APC and other genes that are associated with, such as BECN1, CTNNB1, LRP6, LRP5, TNF, and TP53.

On the other hand, PC crude significantly promotes the expression levels of APC, BECN1, CTNNB1, LRP6, LRP5, TNF, and TP53 and works as anticancer activity (Figure 6). These findings are somewhat surprising because PC extract (crude) and PC-AgNPs have proliferative effects on cell viability (Figure 5). Moreover, researchers previously investigated the effect of AgNPs on cells like CRC and found a positive result [52]. The differences between our work and their work are that they treated cells for 24 h and here for 48 h. The time length could lead to a passive accumulation of NPs. The acute treatment could have a reverse effect [50,53]. Kermanizadeh et al. demonstrated that giving rats one dose of AgNPs did not affect healthy liver functions, but severe dysfunctions can be observed after an acute dose of AgNPs [54]. Thus, how AgNPs accumulate may affect the function of these organs and cells, as these partials can produce OS and free radicals [50].

Furthermore, the harmful effects of AgNPs treatments were reported to induce neurotoxicity in the brain [55] and altered gene expression profiles [56], cross the blood–brain barrier, and even change the animal behavior [57]. The size should also be considered, which is another possible explanation for these unexpected results. It was reported that the best size should range between 10 and 100 nm, and here, the average size is 20 nm. This smaller size with the length of the treatment may contribute to a massive accumulation exhibiting toxic impact.

On the contrary, both CTSB and EpCAM genes are overexpressed in colon cancer. CTSB functions primarily as an endopeptidase in endolysosomes [22]. When tumors expand, CTSB can be overexpressed and exported outside the cells, as the regulation of the protein is altered at multiple levels [22]. According to this, CTSB might play a role in alterations contributing to cancer progression. EpCAM is a tumor antigen and serves as a prognostic indicator. Besides that, it is also a therapeutic target and a molecule anchoring in circulating and disseminated tumor cells. It is considered a multi-functional transmembrane protein that regulates the adhesion, proliferation, and migration of carcinoma cells [58]. Results herein demonstrated that both CP crude and CP-AgNPs had a modulatory effect on the levels of these genes in CRC cells (Figure 6). It is suggested that the PC-AgNPs have anticarcinogenic modulatory effects. Noteworthy, considering the importance of the Wnt/APC/CTNNB1 pathway in initiating human tumorigenesis, our data emphasize the association between the overexpression of CTSB and the mutation of APC. This is in line with previous work that clarified that CTBS could deregulate the mutation of APC, leading to the insufficient breakdown of CTNNB1 and increased nuclear signaling [59].

5 Conclusion

The present study has efficiently synthesized AgNPs using CP. The doses were 6.25 and 25 μL of PC crude and AgNPs, respectively. HCT116 cells were treated for 48 h and exhibited a cytotoxic effect on the growth of CRC. However, the PC-AgNPs have had a negative impact on oncogenes levels. In contrast, the CP crude significantly enhanced the mutant genes (tumor suppressor). It does not mean that utilizing AgNPs is an ultimately harmful tool. It could be related to the long period of treating cells, and it is advisable to repeat the work by treating cells for 24 h before concluding. In addition, PC-AgNPs have deactivated both CTSB and EpCAM. Overall, we can conclude that this study highlights the great potential of AgNPs to be used as a nontoxic anticancer drug delivery system, considering the length of treatment which could minimize the negative impact on cells.

To sum up, this technique is a double-edged sword, mainly applied to highly heterogeneous cells. Cancer cells are unique in their behavior. Same cells with the same tumor could have different genetic changes and could act differently to the exact therapy. Still, further investigations are needed to optimize the best size and treatment period for each type of cancer.

  1. Funding information: This research project was supported by Researchers Supporting Project number (RSP-2022/R495), King Saud University, Riyadh, Saudi Arabia.

  2. Author contributions: Hussah Alobaid: writing – original draft, writing – review and editing, formal analysis; Maha Daghestani: designed the experiment and funding resources; Nawal Almelahi: carried out the gene expression; Sabah A. Alzahrani and Lina M. Hassen: formal analysis of gene expression; Dina M. Metwally: writing – review and editing.

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

  4. Data availability statement: All data generated or analyzed during this study are included in this published article.

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Received: 2022-06-18
Revised: 2022-10-17
Accepted: 2022-11-08
Published Online: 2022-12-10

© 2022 the author(s), 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/gps-2022-0094
Keywords for this article
silver nanoparticles; HCT116; Cymbopogon proximus
Creative Commons
BY 4.0

Articles in the same Issue

  1. Research Articles
  2. Kinetic study on the reaction between Incoloy 825 alloy and low-fluoride slag for electroslag remelting
  3. Black pepper (Piper nigrum) fruit-based gold nanoparticles (BP-AuNPs): Synthesis, characterization, biological activities, and catalytic applications – A green approach
  4. Protective role of foliar application of green-synthesized silver nanoparticles against wheat stripe rust disease caused by Puccinia striiformis
  5. Effects of nitrogen and phosphorus on Microcystis aeruginosa growth and microcystin production
  6. Efficient degradation of methyl orange and methylene blue in aqueous solution using a novel Fenton-like catalyst of CuCo-ZIFs
  7. Synthesis of biological base oils by a green process
  8. Efficient pilot-scale synthesis of the key cefonicid intermediate at room temperature
  9. Synthesis and characterization of noble metal/metal oxide nanoparticles and their potential antidiabetic effect on biochemical parameters and wound healing
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  15. MW-assisted hydrolysis of phosphinates in the presence of PTSA as the catalyst, and as a MW absorber
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  55. Effectiveness of different accelerated green synthesis methods in zinc oxide nanoparticles using red pepper extract: Synthesis and characterization
  56. Blueprinting morpho-anatomical episodes via green silver nanoparticles foliation
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