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Year : 2017  |  Volume : 10  |  Issue : 5  |  Page : 1265-1270
Antioxidant and anti-inflammatory activity of green synthesized silver nanoparticles using Salvia officinalis extract

1 Research Center for Animal Development Applied Biology, Department of Biology, Mashhad Branch, Islamic Azad University, Mashhad, Iran
2 Department of Animal Biology, Faculty of Biological Sciences, Kharazmi University, Tehran, Iran
3 Medical Plants Research Center, Basic Health Sciences Institute, Shahrekord University of Medical Sciences, Shahrekord, Iran

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Date of Web Publication6-Nov-2017


Background and Aims: Free-radical-mediated peroxidation of membrane lipids and oxidative damage of DNA and proteins are believed to be associated with a variety of chronic pathological complications such as cancer. The aim of this study was to describe antioxidant and anti-inflammatory of silver nanoparticles (AgNPs) synthesized using medicinal plant extract of Sage (Salvia officinalis). Materials and Methods: AgNPs were synthesized using S. officinalis as reducer agents and characterized using ultraviolet-visible, Fourier transform infrared spectroscopy, particle seizer, and transmission electron microscopy. Toxicity of AgNPs on MCF-7 cells was investigated using 3-(4,5-Dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide (MTT) assay. Changes in expression of inflammation related genes include cyclooxygenase-2, IL-8, and tumor necrosis factor-alpha (TNF-α) genes were evaluated using semi-quantification reverse transcription-polymerase chain reaction (RT-PCR). The antioxidant potential of capped AgNPs was assessed using 1,1 diphenyl-2-picryl-hydrazyl (DPPH) and 2,2'-azino-bis-3-ethylbenzthiazoline-6-sulfonic acid (ABTS) radicals activity assay. Results: AgNPs successfully synthesis with an average size of 16 nm and spherical. FTIR spectrum from plant extract and AgNPs indicated the extract covered nanoparticles. AgNPs decreased cells viability with inhibitory concentration (IC50) of 25 μg/ml and 20 μg/ml after 24 and 48 h, respectively. To ascertain the anti-inflammatory genes expression, MCF-7 cells were treated with 20 μg/ml AgNPs (concentration below of IC50 value according to MTT assay). Semi-quantification RT-PCR results showed that AgNPs increased IL-8 and TNF-α genes expression 28.76% and 42%, respectively, but suppressed cyclooxygenase-2 gene expression with 20.5% comparing to control groups. Antioxidant assay of green synthesized AgNPs coated by S. officinalis extract showed free radical scavenging effect with IC50 of 830 and 800 μg/ml for DPPH and ABTS radicals, respectively. Conclusion: The coated AgNPs with S. officinalis have promising potential as a source for the development of chemotherapeutic agents in future.

Keywords: Anti-inflammatory, Antioxidant, Salvia officinalis, Silver nanoparticles

How to cite this article:
Baharara J, Ramezani T, Mousavi M, Asadi-Samani M. Antioxidant and anti-inflammatory activity of green synthesized silver nanoparticles using Salvia officinalis extract. Ann Trop Med Public Health 2017;10:1265-70

How to cite this URL:
Baharara J, Ramezani T, Mousavi M, Asadi-Samani M. Antioxidant and anti-inflammatory activity of green synthesized silver nanoparticles using Salvia officinalis extract. Ann Trop Med Public Health [serial online] 2017 [cited 2020 Jul 14];10:1265-70. Available from:

   Introduction Top

Free radicals derived from oxygen, nitrogen and sulfur molecules in the biological system are highly active to react with other molecules due to their unpaired electrons. These radicals are produced during cellular metabolism and functional activities and have important roles in cell signaling, apoptosis, gene expression, and ion transportation.[1] However, excessive reactive oxygen species (ROS) attack bases in nucleic acids, amino acid side chains in proteins and double bonds in unsaturated fatty acids, and causes oxidative stress, which can damage DNA, RNA, proteins and lipids, resulting in an amplified risk for cardiovascular disease, cancer, autism, and other diseases.[1],[2] Antioxidants can decrease the oxidative damage directly through reacting with free radicals or indirectly by inhibiting the activity of free radical generating enzymes or enhancing the activity/expression of intracellular antioxidant enzymes.[2] On the other hand, inflammation is an early protective homeostatic immune response to tissue trauma, it is considered in the production of pro-inflammatory cytokines and the activation of cells in the immune system.[3] The initial features of inflammation, include increased vascular permeability, the release of prostaglandins and chemotactic substances such as complement factors, interleukin (IL)-1, tumor necrosis factor-alpha (TNF-α), and transforming growth factor beta.[4],[5] Over production of reactive oxygen and nitrogen species, an aberrant inflammatory cytokine such as IL-1, IL-6, and IL-8 expression, increased cyclooxygenase (COX)-2 and nuclear factor kappa B expression, play a pivotal role in mediating the interaction between cancers cells and the microenvironment.[6]

With the advent of nanoscience, pure silver can now be made into nanometer-sized particles. Researchers have already demonstrated that besides antibacterial action, silver nanoparticles appear to have anti-inflammatory properties in a burn wound model in mice and anti-inflammatory of silver nanoparticles (AgNPs) were effective on reducing inflammation in peritoneal adhesions without substantial toxic effects.[3] In this regard, the sage (Salvia officinalis) belongs to the genus Salvia of the Labiaceae family which is reported to have multiple pharmacological effects, including antibacterial, antiviral, anti-inflammatory, fungistatic, anti-mutagenic, anti-cancer, and antioxidant effects.[7],[8] The leaves of S. officinalis possess some therapeutic effects mainly due to the presence of flavonoids; phenolic compounds such as carnosic, rosmarinic, caffeic, and salvianolic acids; and other phenolic structure-based compounds.[9],[10],[11] Since there is no report on the recognition of antioxidant and anti-inflammatory potential of eco-friendly synthesis AgNPs coated with S. officinalis, this study investigates antioxidant and anti-inflammatory effects of green synthesis of AgNPs coated with S. officinalis.

   Materials and Methods Top


Silver nitrate, Roswell Park Memorial Institute medium (RPMI-1640), fetal bovine serum (FBS), penicillin-streptomycin and 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide, yellow tetrazole (3-(4,5-Dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide [MTT]) were all purchased from Sigma–Aldrich (USA). MCF-7 cells were obtained from Pasteur Institute of Iran. All solutions were prepared using double distilled water. High Pure RNA Isolation kit (Roche, Germany), RevertAid First Strand cDNA Synthesis Kit (Thermo Scientific), and reverse transcription-polymerase chain reaction (RT-PCR) kit (Parstous, Iran) were used in this study. Saliva officinalis were obtained from a local source (Mashhad-Iran).

Green synthesis of silver nanoparticles capping with Saliva officinalis extract

We previously synthesis AgNPs using S. officinalis leave extract. In brief, leave of S. officinalis were collected from Iran (Khorasan, Masshad, May 2013). The leaves were powdered and used for extraction. For the fabrication of AgNPs, a solution of 10 mL of AgNO3 solution (5 mM) with of S. officinalis extract was mixed and was warmed to 40°C until the color of the solution changing to brown (the process carried out in 40°C and pH = 7). The synthesis Ag-NPs were characterized by ultraviolet (UV)-visible, Fourier transform infrared (FTIR) spectroscopy, particle sizer and transmission electron microscopy imaging.[12]

Cell culture

MCF-7 cells were cultured in RPMI-1640 medium supplemented with 10% FBS, 100 units penicillin-streptomycin and maintained at 37°C with 5% CO2 in a humidified atmosphere.

Cell viability assay

The effect of coated AgNPs with S. officinalis on the cell survival was evaluated by MTT assay. 5 × 105 cells/well was cultured into 96-well plates. After overnight incubation, the cells were treated with different concentrations of AgNPs (5, 10, 15, 20, and 25 μg/ml) and its effects on cell viability were measured 24 and 48 h after treatment by MTT assay. For MTT assay 10 μL of MTT solution was added to each well and the plate was incubated for 2 h in darkness, then 100 μL dimethyl sulfoxide was added, and the absorbance of each well was measured at 570 nm with a microplate spectrophotometer (Biotek, USA). The cell viability was calculated using the equation as follows:

Cell viability (%) = (Atreated/Acontrol) × 100

Free radical scavenging activity by 1,1 diphenyl-2-picryl-hydrazyl assay

The 1,1 diphenyl-2-picryl-hydrazyl (DPPH) stock solution was prepared by dissolving 10 mg of DPPH (2, 2-diphenyl1-picrylhydrazyl) radical solution in 10 ml methanol. The working solution was obtained by diluting the stock solution of the DPPH radical with methanol to produce an absorbance at 515 nm against the reference sample (methanol).

In brief, 100 μl AgNPs at different concentrations (100–1000 μg/ml) was mixed with 100 μl DPPH and the mixture was left at room temperature for 30 min in darkness. Finally, the mixture absorbance (a sample) was read at 517 nm wavelength by a spectrophotometer against methanol as a blank. A negative control was taken after adding 100 μl DPPH solutions to 100 μl of the deionized water (nanoparticles solvent). The percentage of DPPH scavenging of the sample was calculated according to the equation:

% scavenging capacity = [1–(Asample/Acontrol)] ×100

Where A represents absorbance and butylated hydroxyanisole (BHA) was used as a standard.

Finally, IC50 values, which represented the extract concentration providing 50% inhibition of DPPH radicals, were calculated from the plot of inhibition percentage against extract concentration.

Antioxidant activity by 2,2'-azino-bis-3-ethylbenzthiazoline-6-sulphonic acid assay

The stock solutions contained 7.4 mM 2,2'-azino-bis-3-ethylbenzthiazoline-6-sulfonic acid (ABTS) solution and 2.6 mM potassium persulfate solution. The working solution was then prepared by mixing the two stock solutions in equal quantities and allowing them to react for 12 h at room temperature in darkness. The solution was then diluted by mixing ABTS solution with methanol to obtain an absorbance of 1.1 ± 0.02 at 734 nm by the spectrophotometer. Fresh ABTS solution was prepared for each assay. Then, 100 ml of sample was mixed with 100 ml of ABTS solution, and the absorbance at 734 nm was measured after 10 min incubation at room temperature. The scavenging of ABTS radical was calculated as:

% ABTS-scavenging activity= [1– (Asample/Acontrol)] ×100

Where A represents absorbance and BHA was used as a standard.

Reverse transcription-polymerase chain reaction of IL-8, tumor necrosis factor-alpha and cyclooxygenase-2

To assess the anti-inflammatory effect of AgNPs, the changes in the expression of IL-8, TNF-α and COX-2 mRNA were examined by the RT-PCR methods. RNA of treated MCF-7 cell was isolated by the High Pure RNA Isolation kit according to the manufacturer's protocol and stored at −80°C. cDNA was synthetized using RevertAid First Strand cDNA Synthesis kit according to the manufacturer's instruction. The produced cDNA (5 μg) was added to 10 μl Taq premix, 2 μl forward primer, 2 μl reverse primer [sequence of primer represented in [Table 1] and distilled water. Ultimately, RT-PCR was performed with one cycle at 94°C/5 min, 30 cycles at 94°C/30 s for denaturation, 56°C/30 s for annealing, 68°C/45 s for extension and one cycle at 72°C/5 min according to the manufacturer's protocol.
Table 1: The sequences of primers and annealing temperatures

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The PCR products were run in 2% gel electrophoresis, and the gels were observed using gel documentation (UV TEC Cambridge, UK). The experiments were repeated in triplicate, then the percentage of relative band densities of cDNA from the treated cells were compared with the untreated cells by ImageJ software.

Statistical analysis

Statistical evaluation of the data was performed using one-way analysis of variance. Tukey's post hoc test was used for multiple comparisons in SPSS software 16.0 (SPSS Inc., Chicago, Illinois). P < 0.05 was considered to be the level of significance.

   Results Top

Green synthesis of AgNPs capping with Saliva officinalis extract

We have previously reported synthesized, characterized, and recognized green AgNPs capping with S. officinalis extract. UV-visible spectrum of this nanoparticles showed a sharp peak at 440 nm. FTIR results indicated appropriate coating of plant extract on nanoparticles and the average was recorded as 16.5 ± 1.2 nm which was remarkable [Figure 1].
Figure 1: (a) Ultraviolet-visible absorbance for anti-inflammatory of silver nanoparticles represent sharp peak at 440 nm, (b) transmission electron microscopy images of silver nanoparticles, (c) shows particle size distribution of synthesized silver nanoparticles, (d) Fourier transform infrared spectra of Saliva officinalis extract before (black) and after the synthesis of silver nanoparticles (red)

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Effect of AgNPs on MCF-7 cell viability

The MTT assay indicated that the AgNPs bio-synthesized with S. officinalis exerted cytotoxic and inhibitory effect on the cell viability of the MCF-7 cells in a dose-dependent manner. The concentration of AgNPs at up to 15 μg/ml, did not have any toxic effect on human breast cancer cells in comparison with the control. The IC50 value was 25 μg/ml after 24 h and 20 μg/ml after 48 h. [Figure 2] illustrates MTT assay results from treatment of MCF-7 cell at various concentrations of AgNPs in 24 h and 48 h [Figure 2].
Figure 2: 3-(4,5-Dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide assay results from treatment of MCF-7 cell at various concentration of silver nanoparticles synthesized with Saliva officinalis in 24 h and 48 h, *P < 0.05, **P < 0.001

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DPPH radical scavenging activity assay

Results from DPPH assay showed antioxidant activity of AgNPs increased in a dose-dependent manner. The IC50 was calculated approximately 830 μg/ml [Figure 3].
Figure 3: 1,1 diphenyl-2-picryl-hydrazyl radical scavenging activity of silver nanoparticles synthesized with Saliva officinalis

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ABTS antioxidant activity

IC50 represents the effective concentration of the sample that has 50% ABTS scavenging capacity which was 800 μg/ml for capped AgNPs with S. officinalis. Through linear regression, curve of inhibitory concentration percentage was achieved. The lower value of IC50 indicates a higher antioxidant activity. AgNPs (IC50 = 780 μg/mL) shows ABTS radical scavenging activity which is comparable to the reference standards BHA [Figure 4].
Figure 4: 2,2'-azino-bis-3-ethylbenzthiazoline-6-sulphonic acid radical scavenging activity of silver nanoparticles synthesized with Saliva officinalis

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As displayed in [Table 2], capped AgNPs of S. officinalis extracts were found to be a potent free radical scavenger when compared to either S. officinalis extract or AgNO3 as solution.
Table 2: The comparison of 1,1 diphenyl-2-picryl-hydrazyl and 2, 2'-azino-bis-3-ethylbenzthiazoline-6-sulphonic acid scavenging activities capped silver nanoparticles of Salvia officinalis extracts with Salvia officinalis extract or silver nitrate as solution

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Gene expression by reverse transcription-polymerase chain reaction

In this regard, the eco-friendly bio-synthesized AgNPs coated with S. officinalis extract significantly suppressed IL-8 and TNF-α gene expression with 28.76% and 42%, respectively (P < 0.001), whereas COX-2 gene expression was reduced by 20.5% (P < 0.05) [Figure 5].
Figure 5: Inflammation related genes expression *P < 0.05, **P < 0.001

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   Discussion Top

Oxidants play a significant role in the pathogenesis of a number of disorders such as inflammation, rheumatoid arthritis, asthma, psoriasis, and contact dermatitis leading to oxidative stress. Oxidative stress may be defined as an imbalance between the cellular production of ROS and antioxidant defense mechanisms. It is important to develop, identify and utilize a new source of effective antioxidants of natural origin.[13],[14],[15] Hence in this study, the cytotoxic effect of AgNPs coated with S. officinalis extract was investigated then based results from MTT assay nontoxic concentration of AgNPs was used to assessment antioxidant properties of AgNPs. DPPH and ABTS radical scavenging activity assay results showed the antioxidant activity of AgNPs increased in a dose-dependent manner. The IC50 was calculated approximately 830 and 780 μg/ml for DPPH and ABTS assay, respectively. It has been already reported that the biological synthesis of AgNPs with Hydnocorpus alpina leaf have antioxidant activity can be used against deleterious effects of free radicals.[16] Kanipandian et al. also showed that green synthesized AgNPs with Cleistanthus collinus extract as a surface modifier had noticeable DPPH radical scavenging activity.[17] For the relationship between the antioxidant activity of biogenic AgNPs and coating agents, capping of the phyto-compounds, probably polyphenols from Piper, and Longum fruit extract may be responsible for free radical DPPH inhibition.[10] Seralathan et al. showed that free radical scavenging activity of biogenic AgNPs synthesized with Salicornia brachiata aqueous extract which was assessed by DPPH assay was not only due to the capping agents (chemical compounds present in the extract) but it was also enhanced due to silver nanoparticles.[16] Similar observations have been also reported with enhanced DPPH scavenging activity by selenium, platinum, AgNPs and by torolex and chitosan coated gold AgNPs.[18],[19] For the current study, these scavenging activities might increase due to the presence of S. officinalis polyphenole on the surface of AgNPs. In this study, anti-inflammatory activities of the AgNPs synthesized with S. officinalis extract were evaluated by semi-quantification RT-PCR assay on MCF-7 cell line by COX-2, TNF-α, and IL-8 genes expression. Eco-friendly bio-synthesized AgNPs coated with S. officinalis extract suppressed significantly IL-8 and TNF-α gene expression, whereas reduction of COX-2 gene expression. It was previously reported that AgNPs could effectively reduce the infiltration of inflammatory cells, inhibit the production of inflammatory cytokines, and up-regulate the expression of matrix metalloproteinase.[3] Jang et al. demonstrated that administration of AgNPs reduced inflammation by decreasing vascular endothelial growth factor, PBK and mucous glycoprotein expression in ovalbumin-induced allergy in murine model.[20] Moreover, Wong et al. reported that AgNPs possessed anti-inflammatory activity in postoperative peritoneal adhesion model.[3] Yilma et al. showed that silver-polyvinyl pyrrolidone nanoparticles exhibited anti-inflammatory activity by reducing TNF-α.[21] Moreover, exposure to AgNPs did not significantly increase the levels of ROS generation in Caco-2 and SW480 human intestinal epithelial cells. The potential mechanism of AgNPs-mediated anti-inflammatory property was due to the intracellular blocking of inflammatory pathways and down-regulating pro-inflammatory cytokines.[22]

   Conclusion Top

The aqueous extract of the aerial parts of S. officinalis is capable of producing coated AgNPs which exhibited excellent antioxidant and anti-inflammatory potential. Since S. officinalis itself represented antioxidant and anti-inflammatory potentials, it was a promising and great finding that green bio-synthesized AgNPs capped with S. officinalis exhibited significant potential, which was much more remarkable than using this medicinal plant extract alone. However, further research is needed to elucidate its mechanism.


This work was funded by the Research Center for Animal Development Applied Biology, Islamic Azad University, Mashhad Branch. The authors sincerely thank their colleagues in this center for their kind assistance and support.

Financial support and sponsorship

This work was funded by the Research Center for Animal Development Applied Biology, Islamic Azad University, Mashhad Branch. The authors sincerely thank their colleagues in this center for their kind assistance and support.

Conflicts of interest

There are no conflicts of interest.

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Correspondence Address:
Majid Asadi-Samani
Medical Plants Research Center, Basic Health Sciences Institute, Shahrekord University of Medical Sciences, Rahmatiyeh, Shahrekord
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ATMPH.ATMPH_174_17

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]

  [Table 1], [Table 2]


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