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BY 4.0 license Open Access Published by De Gruyter Open Access July 10, 2023

Green supported silver nanoparticles over modified reduced graphene oxide: Investigation of its antioxidant and anti-ovarian cancer effects

  • Wei Chen , Lili Huang and Bing Zhou EMAIL logo
From the journal Open Chemistry


A green biosynthesis of silver nanoparticles (AgNPs) decorated Mentha longifolia root extract-functionalized graphene oxide (GO) nanohybrid material has been described. Initially, the Mentha longifolia root was coated on GO’s surface. The phytochemicals of the plant acted as reducing agent for reduction of silver ions and GO to form the rGO-Mentha/Ag nanocomposite. The nanocomposite was characterized using FE-SEM, EDX, FT-IR, TEM, elemental mapping, and XRD analysis. The cells treated with rGO-Mentha/Ag nanocomposite were assessed by 3-[4,5-dimethylthiazol-2-yl]-2,5 diphenyl tetrazolium bromide assay for 48 h about the cytotoxicity and anti-human ovarian cancer properties on normal (HUVEC) and human ovarian cancer cell lines, i.e., SKOV3 and A2780. The IC50 of rGO-Mentha/Ag nanocomposite were 181.2 and 196.4 µg/mL against SKOV3 and A2780cell lines, respectively. The viability of malignant human ovarian cell line reduced dose-dependently in the presence of rGO-Mentha/Ag nanocomposite. After clinical study, rGO-Mentha/Ag nanocomposite can be introduced as a novel composite in the treatment of human ovarian cancer.

1 Introduction

In these days nano-biotechnology has come upon as a unique and fascinating endowment of advanced material science, converging the two distinct though indispensable domains of science, biotechnology, and nanoscience [1,2]. As an outcome, the modern scientific fraternity has witnessed the synthesis and development of diversely designed bio-engineered green materials. These biocompatible bio-nanomaterials have acquired remarkable importance due to their potential biological and pharmaceutical implications [3,4,5,6,7]. Owing to several unique features, the surface functionalized noble metal nanoparticles (NPs) (Ag, Au, Cu, Pd, and Pt) have been quite admired among the researchers [3,4,5,6,7,8] and amongst them, the AgNPs particularly have garnered enormous attraction based on their outstanding surface plasmon resonance and optoelectronic properties. These NPs are found to have multidisciplinary applications in wide domains like optics, food science, biosensing, optoelectronics, agriculture, animal husbandry, photocatalysis, and catalysis [9,10,11,12]. However, apart from these, AgNPs exhibit promising biomedical properties like antimicrobial (bacteria and fungi), antiviral, anti-nematodes, anti-inflammatory, antitumor, and anticancer activities [13,14]. Interestingly, AgNPs are found to be significantly effective in different human malignant cell lines like breast cancer (Hs 578Bst, Hs 319.T, MCF-7) [15,16], colon cancer (HT29, caco-2) [17,18], liver cancer (HepG2) [5], cervical cancer (SiHa, HeLa) [19], lung cancer (A549, Calu6, H358) [4,20], prostate cancer [21] etc. As an explanation, AgNPs indisputably promote the generation of reactive oxygen species (ROS) on interaction with cellular organism and consequently the elevated ROS level in turn is responsible for cytotoxicity, DNA damage, apoptosis, and necrosis of carcinogenic cells. Sometimes, the ROS enables the trapping of cancer cells and disconnects them from their growth media thus inhibiting their proliferation [22,23].

Now, AgNPs have been well reported to prepare following different physical and chemical methods. Nevertheless, despite their superiority and specific merits, some conditions like the use of toxic reagents and carcinogenic solvents, vigorous synthetic conditions like high temperature and pressure, and expensiveness of the reagents are detrimental for safe environment and green synthesis [24,25]. Hence, maintaining ecologically benign conditions following sustainable green protocols towards these syntheses are highly indispensable. In this connection, the bio-inspired methods have come into prominence by proper utilization of natural biological resources, alternatively called as the “bio-laboratory” [26,27]. Different microorganisms (virus, bacterium, algae, and fungi), bio-macromolecules (lipids, carbohydrates, proteins, and biopolymers), and plant extracts (leaf, flower, fruit, peel, seed, stem, latex, and root) are being enormously exercised as natural templates for the synthesis of biogenic NPs. Among them, the green approach based on plant extracts has engrossed considerable interest and quite popular as compared to others because it is abundant, cost-efficient, scalable, non-hazardous, and free from microbial contamination [2835].

This has moved us to report herein the green synthesis of AgNPs adorned reduced graphene oxide (rGO) templated over Mentha longifolia root extract affording the high surface area carbonaceous and biodegradable nanocomposite rGO-Mentha/Ag (Scheme 1). Mentha is a genus of perennial plant (Lamiaceae sp.) and enriched with a range of diverse organic phytochemicals [20,36,37]. The oxygenated organofunctions facilitated the in situ green reduction of GO and Ag+ ions. rGO was used as green support to immobilize the AgNPs and stabilize them. The functionalized phytomolecules also helped to restrict the AgNPs from aggregation [17].

Scheme 1 
               Schematic preparation of rGO-Mentha/Ag mediated by Mentha longifolia root extract.
Scheme 1

Schematic preparation of rGO-Mentha/Ag mediated by Mentha longifolia root extract.

The as-synthesized rGO-Mentha/Ag bio-nanocomposite was thereafter employed in controlling the proliferation of human ovarian cancer cells, through in vitro studies. The cytotoxicity and anti-cancer effects were investigated against the two standard cell lines SKOV3 and A2780, respectively, via 3-[4,5-dimethylthiazol-2-yl]-2,5 diphenyl tetrazolium bromide (MTT) method. Ovarian cancer is one of the leading prevalent gynecological carcinomas causing high rate of mortality as it remains undetected or undiagnosed until spread from ovary to pelvis and stomach of human body. Another reason is that its metastasis is caused without any apparent specific symptoms. Conventionally surgery and chemotherapy are followed in its treatment, although the ovarian cancer cells are often found resistant to chemotherapeutics and surgery is associated with several recurrent health hazards [38,39,40]. The contemporary bio-nanotechnology has come up as emerging solution towards the detection and treatment of ovarian cancer. In our study, the rGO-Mentha/Ag bio-nanocomposite exhibited significant results while treated against the SKOV3 and A2780 ovarian cancer cell lines. The anti-cancer effects of AgNPs and Mentha phytochemicals are anticipated to play synergistic roles in the protocol. The material is additionally found non-reactive to normal HUVEC cells and attacks specifically the ovarian cancer cells. In addition to anti-ovarian investigations, the antioxidant potential of the material was also studied by 1,1-diphenyl-2-picrylhydrazil hydrate (DPPH) radical scavenging assay and observed to carry good antioxidant potential.

2 Experimental methods

2.1 Preparation of Mentha root extract

Dried Mentha roots (1.0 g) were washed well in distilled (DI) water and boiled in 20 mL of DI water for 40 min. It was then filtered through Whatman No. 1 paper to remove the organic residues and the filtrate was used in the next step.

2.2 Synthesis of rGO-Mentha nanocomposite

The well reported modified Hummers method was followed to synthesize graphene oxide (GO) [17]. 0.01 g GO powder was suspended in 50 mL of DI water by sonication and the preserved root extract was added to it and sonicated again for 30 min. Then, the reaction medium was refluxed for 12 h which caused the reduction of GO to rGO, as indicated by a change in color. The rGO-Mentha nanocomposite was collected by centrifuge and washed repeatedly with H2O.

2.3 Synthesis of rGO-Mentha/Ag nanocomposite

The rGO-Mentha nanocomposite was again dispersed in DI water by sonication and subsequently an aqueous solution of AgNO3 (0.02 g/L) was added dropwise. The mixture was stirred at room temperature for 0.5 h in order to immobilize the Ag ions over rGO-Mentha support and then refluxed for 2 h for carrying out the reduction from Ag+ to AgNP. Finally, the rGO-Mentha/Ag was isolated by centrifuge. The Ag content in the final material was found to be 0.081 mmol/g, measured by Inductively coupled plasma optical emission spectroscopy analysis.

2.4 Antioxidant analysis by DPPH method

The rGO-Mentha/Ag nanocomposite was explored for its antioxidant potential by well-known DPPH method [41]. It was determined by measuring the DPPH radical scavenging capacity by the material. Experimentally, the alcoholic (EtOH) solution of DPPH was treated with the antioxidant material taken in different concentrations. In doing so, the radical abstracts’ free electron or hydrogen from the bio-nanocomposite gets quenched. The corresponding change in absorbance is detected by UV-Vis spectrophotometer.

2.5 Cytotoxic activity

Cytotoxicity or anti-cancer activity of the rGO-Mentha/Ag bio-nanocomposite was analyzed via measuring the % cell viability against the ovarian cancer cell lines, SKOV3, and A2780, respectively, following conventional MTT assay, a colorimetric as well as spectrophotometric method. The in vitro protocol started with the culture of the two cell lines. The cell culture plate with 96 wells containing 1 × 105 cells/well was incubated inside a humidified incubator at standard conditions (37°C, 20% O2, 5% CO2 atmosphere) for 24 h. Eventually, when the cell confluence reached around 85%, the FBS solution (10%), used as the cell media, was removed and the grown-up cells were thoroughly washed twice with PBS. These processed cells were brought in contact with the rGO-Mentha/Ag nanocomposite suspension in RPMI medium at five different concentrations (0.5, 5, 50, 500, and 1,000 µg/mL) and the mixtures were incubated again as before for 72 h. Then, the MTT dye solution in PBS (10 μL, 5 mg/mL) was mixed to it and again incubated for 4 h. The active or viable cells through mitochondrial activity undergoes cell metabolism and converts the MTT into purple formazan crystals. In this stage, the cell media was substituted with 100 µL of DMSO solvent in order to solubilize the crystal. Finally, absorbance of the purple color solution was measured at 570 nm equipped with an ELISA microplate reader. The concentration of formazan complex is proportional to the cell viability.

3 Results and discussion

3.1 Characterization of rGO-Mentha/Ag nanocomposite

The rGO-Mentha/Ag was fabricated following a biogenic and stepwise post-functionalization pathway. The rGO, a high surface area and biodegradable carbonaceous material, was used as a support for the tiny AgNPs. However, at the outset, rGO was functionalized with Mentha phytochemicals affording rGO-Mentha composite. Subsequently, the Ag ions were immobilized over it which was biogenically reduced in situ to corresponding AgNPs. The electron rich oxygenated organofunctions drove the green reduction of Ag ions thus producing a hybrid bio-nanocomposite material following a toxic reagent free method. The final material was characterized using FE-SEM, EDX, TEM, FT-IR, elemental mapping, and XRD techniques.

Figure 1 represents the collective FT-IR profile of bare GO, Mentha root extract, rGO-Mentha, and the final rGO-Mentha/Ag nanocomposite in order to demonstrate the hierarchical construction. The FT-IR spectrum of GO (Figure 1a) can be identified with vibrations like 3,423 cm−1 (O–H stretching), 1,490 cm−1 (unoxidized C═C stretching), 1,629 cm−1 (C═O stretching for carbonyl and carboxylic acids), 1,385 cm−1 (carboxylic O–H stretching) and 1,082 cm−1 (alkoxy or epoxy C–O stretching). The plant extract spectrum displays a group of significant absorptions at 3,402, 2,925, 1,598, 1,421, and 1,074 cm−1, which are ascribed to the O–H stretching (menthol, neomenthol, and other polyphenols), C–H stretching (C–H bonds in aromatic and aliphatic rings like pinene, caryophyllene, etc.), C═O stretching (menthone, piperitone, etc.), C═C stretching (C═C bonds in aromatic and aliphatic rings), C–O stretching (phenols and aromatic alcohols), and C–O–C stretching (tannins) vibrations, respectively (Figure 1b). The spectrum of rGO-Mentha has been depicted in Figure 1c which is merely an overlap of the two earlier spectra, signifying the successful implantation of Mentha root phytomolecules over rGO. Finally, the spectrum of AgNPs adorned rGO-Mentha nanocomposite has been represented in Figure 1d which also looks similar to that in Figure 1c, with the difference of only just shifting of vibrational signals to a little lower region (3,405 to 3,402; 1,744 to 1,699 and 1,632 to 1,608) due to the strong coordination of AgNPs with the biomolecules and rGO support.

Figure 1 
                  FT-IR spectrum of (a) GO, (b) Mentha root extract, (c) rGO-Mentha, and (d) rGO-Mentha/Ag.
Figure 1

FT-IR spectrum of (a) GO, (b) Mentha root extract, (c) rGO-Mentha, and (d) rGO-Mentha/Ag.

The structural features and physical characteristics of the rGO-Mentha/Ag nanocomposite including its shape and texture were investigated by FE-SEM study. Figure 2 shows the FESEM images of GO and rGO-Mentha/Ag for comparison and detection of functionalization. It represents the layered and flaky microstructure, characteristic of GO. It appears like peeling scales from its surface. However, the Mentha modification or AgNPs immobilization could not be detected from the image. The key ingredients of the material were further determined by EDX study, equipped with an SEM instrument. As Figure 3 displays, the bio-nanomaterial is composed of Ag, C, and O elements. The C and O are evidently coming from the rGO and Mentha phytochemical associations. A major and sharp signal of Au is detected, corroborated to the golden grid in sample preparation.

Figure 2 
                  FE-SEM images of (a) GO and (b) rGO-Mentha/Ag.
Figure 2

FE-SEM images of (a) GO and (b) rGO-Mentha/Ag.

Figure 3 
                  EDX spectrum of rGO-Mentha/Ag.
Figure 3

EDX spectrum of rGO-Mentha/Ag.

Further inherent structural details were investigated through TEM studies, which are displayed in Figure 4. It clearly shows the thin and wrinkled sheet like microstructure of typical GO or rGO material, acting as a support. The round shaped black dots spread over the surface represent the AgNPs which are dispersed quite homogeneously keeping apart from each other, thus nullifying the tendency of self-aggregation. They are within the dimension of 10–15 nm. Nevertheless, the Mentha biomolecular modifications cannot be detected.

Figure 4 
                  TEM images of rGO-Mentha/Ag.
Figure 4

TEM images of rGO-Mentha/Ag.

The crystalline nature, types of diffraction pattern, phase structure, and purity of the rGO-Mentha/Ag were explored by XRD study and are shown in Figure 5. Evidently, the pattern reveals that the material is of very good crystallinity and pure as displayed without noise. The single-lined diagram indicates the material is a united entity. A broad and moderately crystalline signal appearing at 2θ = 24.5° (002) was accredited to the rGO support (Figure 5b) as compared with GO (Figure 5a). Another four sharp diffraction peaks were observed at 2θ = 37.5°, 47.2°, 66.4°, and 76.8° which were assigned to (1 1 1), (2 0 0), (2 2 0), and (3 1 1) planes of fcc Ag crystalline pattern, respectively (JCPDS No. 04-0783).

Figure 5 
                  XRD patterns of (a) GO and (b) rGO-Mentha/Ag.
Figure 5

XRD patterns of (a) GO and (b) rGO-Mentha/Ag.

3.2 Study of antioxidant potential of rGO-Mentha/Ag nanocomposite

There have been several reports in support of AgNPs and its nanocomposite derivatives, to function as very good antioxidant material, being studied in vitro. In view of high demand of the AgNPs antioxidant materials in health management sectors towards oxidative stress, they have profound applications. With this view, we herein demonstrated the antioxidant capacity of rGO-Mentha/Ag bio-nanomaterial following the well-known DPPH assay. The proposed antioxidant sample was prepared in six different concentrations (31.25, 62.5, 125, 250, 500, and 1,000 µg/mL) and introduced to the purple ethanolic DPPH solvent (150 µL, 0.04 mg/mL). The mixture was incubated at 37°C for 30 min in dark when the color gradually faded due to quenching of the free radical. The resulting solutions were exposed to UV-Vis spectrophotometer for absorbance measurements at 517 nm and the % inhibition was calculated following the equation.

Inhibition ( % ) = 1 Abs sample Abs blank Abs control Abs blank × 100 ,

where Abssample is the absorbance of the reaction mixture, Absblank is the absorbance of the blank for each sample dilution in DPPH solvent, and Abscontrol is the absorbance of DPPH solution in the sample solvent.

Figure 6 displays the corresponding graphical representation of % inhibition against the corresponding antioxidant concentrations. The antioxidant capacity gradually increases with loads of rGO-Mentha/Ag nanocomposite and gives the highest capacity at 1,000 µg/mL.

Figure 6 
                  Antioxidant activity of rGO-Mentha/Ag.
Figure 6

Antioxidant activity of rGO-Mentha/Ag.

3.3 Cytotoxicity studies over rGO-Mentha/Ag nanocomposite

The next endeavor was to investigate the cytotoxicity and anti-cancer potential of rGO-Mentha/Ag against the two ovarian cancer cell lines, SKOV3 and A2780. The standard MTT colorimetric assay was followed in the protocol. After measurement of optical density (OD) in terms of absorbance the following equation was used in the determination of % toxicity and % cell viability.

Toxicity % = 1 Mean OD of sample Mean OD of control × 100 ,

Viability % = 100 Toxicity % .

As can be seen from the outcomes obtained against the two cell lines (Figures 7 and 8, respectively) the rGO-Mentha/Ag bio-nanocomposite had significant toxicity that increased gradually with material concentrations (5–2,000 µg/mL). The ability to produce high concentrations of ROS by the Ag associated nanocomposite is particularly responsible for the very good anti-cancer effects.

Figure 7 
                     In vitro toxicity analysis of rGO-Mentha/Ag nanocomposite on SKOV3 cell.
Figure 7

In vitro toxicity analysis of rGO-Mentha/Ag nanocomposite on SKOV3 cell.

Figure 8 
                     In vitro toxicity analysis of rGO-Mentha/Ag nanocomposite on A2780 cell.
Figure 8

In vitro toxicity analysis of rGO-Mentha/Ag nanocomposite on A2780 cell.

The related IC50 values were detected as 181.2 and 196.4 µg/mL against SKOV3 and A2780 cell lines, respectively. Furthermore, we investigated the adverse effects of the nanomaterial over normal healthy cells and thereby the % toxicity was studied against the HUVEC cell lines. Evidently, the cells remained almost unaffected thus implying the rGO-Mentha/Ag nanocomposite as a safe material to human body (Figure 9).

Figure 9 
                     In vitro toxicity analysis of rGO-Mentha/Ag on HUVEC cell.
Figure 9

In vitro toxicity analysis of rGO-Mentha/Ag on HUVEC cell.

4 Conclusion

To conclude, we reported a green sustainable protocol for the development of AgNPs decorated rGO, as a high surface area carbonaceous nanocomposite. The bio-inspired synthesis was executed using Mentha longifolia root extract where the inherent phytochemicals were utilized as the green reducing agent. The in situ synthesized AgNPs were dispersed over the high surface of GO and the electron rich biomolecules from Mentha helped to stabilize the NPs. The material was then characterized using various techniques. TEM images revealed the thin wrinkled paper like surface of rGO with AgNPs sized between 10 and 15 nm. XRD analysis justified it to be a fairly crystalline material having distinct diffraction signals of GO as well as fcc AgNPs. Towards the application, the bio-nanocomposite was explored as a nano-formulated chemotherapeutic drug like material against human ovarian cancer. MTT method was used to determine the cytotoxicity of the material against two cell lines, SKOV3 and A2780, which displayed quite satisfactory outcomes with increasing dose-dependent cell viability. In addition, DPPH assay was followed to determine its very good antioxidant potential.

# Wei Chen and Lili Huang contributed equally to the article.

  1. Funding information: Authors state no funding involved.

  2. Author contributions: Wei Chen, Lili Huang, and Bing Zhou: visualization, writing original draft, and formal analysis. Bing Zhou: funding acquisition, methodology, and supervision. Wei Chen and Lili Huang: writing original draft, formal analysis, and writing – review and editing. All authors reviewed the manuscript.

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

  4. Ethical approval: The research related to animal use has been complied with all the relevant national regulations and institutional policies for the care and use of animals and in accordance with The Affiliated Ganzhou Hospital of Nanchang University animal ethical committee.

  5. Data availability statement: The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.


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Received: 2023-04-26
Revised: 2023-05-28
Accepted: 2023-05-29
Published Online: 2023-07-10

© 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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