http://informahealthcare.com/mby ISSN: 1040-841X (print), 1549-7828 (electronic) Crit Rev Microbiol, Early Online: 1–11 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/1040841X.2013.879849

REVIEW ARTICLE

Metal nanoparticles: The protective nanoshield against virus infection Mahendra Rai1, Shivaji D. Deshmukh1, Avinash P. Ingle1, Indarchand R. Gupta1,2, Massimiliano Galdiero3, and Stefania Galdiero3

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Department of Biotechnology, SGB Amravati University, Amravati, Maharashtra, India, 2Department of Biotechnology, Government Institute of Science, Nipatniranjan Nagar, Caves Road, Aurangabad, Maharashtra, India and 3CIRPEB, University of Naples, Naples, Italy

Abstract

Keywords

Re-emergence of resistance in different pathogens including viruses are the major cause of human disease and death, which is posing a serious challenge to the medical, pharmaceutical and biotechnological sectors. Though many efforts have been made to develop drug and vaccines against re-emerging viruses, researchers are continuously engaged in the development of novel, cheap and broad-spectrum antiviral agents, not only to fight against viruses but also to act as a protective shield against pathogens attack. Current advancement in nanotechnology provides a novel platform for the development of potential and effective agents by modifying the materials at nanolevel with remarkable physicochemical properties, high surface area to volume ratio and increased reactivity. Among metal nanoparticles, silver nanoparticles have strong antibacterial, antifungal and antiviral potential to boost the host immunity against pathogen attack. Nevertheless, the interaction of silver nanoparticles with viruses is a largely unexplored field. The present review discusses antiviral activity of the metal nanoparticles, especially the mechanism of action of silver nanoparticles, against different viruses such HSV, HIV, HBV, MPV, RSV, etc. It is also focused on how silver nanoparticles can be used in therapeutics by considering their cytotoxic level, to avoid human and environmental risks.

Cytotoxicity, drug resistant, immunity booster, nanoparticles, nanoshield, virucidal

Introduction Viruses pose a very serious challenge for the medical, pharmaceutical and biotechnological fields being one of the main causes of human disease and death. Various life threatening diseases caused by viruses such as common colds, influenza, hepatitis, chickenpox, infectious mononucleosis, herpes keratitis, viral encephalitis, are wide-spread. Many attempts have been made to develop medicines and vaccines in order to fight against these infectious agents. The amazing ability of viruses for quick adaptation in current host and to switch to a new host is a matter of great concern and the major bottleneck in treatment (Esteban, 2010; Tauxe, 2002). Notwithstanding the tremendous improvements in antiviral therapy, recent treatments and medicines are unable to control viral diseases completely. Hence, there is an urgent need to develop novel potential antiviral agents. The development of modification for the improvement of existing antiviral compounds is also a priority area of research. Nanotechnology provides a platform to modify and develop the properties of metals by reducing them into metal nanoparticles, which have huge applications in different fields such as diagnostics, biomarkers, drug delivery systems,

Address for correspondence: Mahendra Rai, Department of Biotechnology, SGB Amravati University, Tapowan road, Amravati 444602, Maharashtra, India. E-mail: [email protected]

History Received 24 October 2013 Revised 12 December 2013 Accepted 30 December 2013 Published online 16 April 2014

antimicrobial agents and other nanomedicines for the treatment of various diseases (Singh & Nalwa, 2011). Now-a-days, there is a continuous search for an effective nanotechnological solution to treat viral infections. Since ancient times, silver has been used in the form of ‘‘Rajatbhasma’’ (an Ayurvedic medicine prepared from silver), which shows strong antimicrobial potential against the pathogenic multi-drug resistant as well as susceptible strains of bacteria (Rai et al., 2009, 2012). Before the discovery of antibiotics, silver was used as antiseptic in treatment of open wounds and burns. The highly reactive silver ions bind to the bacterial cell wall leading to bacterial death. Silver can inhibit the bacterial replication by denaturing bacterial DNA which ultimately leads to bacterial cell distortion and cell death (Castellano et al., 2007; Landsdown, 2002). Nanoparticles have specific and different physicochemical characteristics compared to their bulk material and their properties seem to be correlated to their high surface area to volume ratio which also leads to an increase of reactivity. In fact, nanoparticles due to unique and interesting properties and the small size have been shown to interact with viruses and other microbes. The metal nanoparticles of copper, magnesium, titanium, gold and zinc have been proved to be bactericidal at nano-levels (Rai et al., 2009). Among nanoparticles those made by silver possess important physicochemical and biological activities that are currently being deeply investigated as antimicrobials (Lok et al., 2006; Pal

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et al., 2007). Silver nanoparticles are effective broadspectrum bactericidal agents, fast-acting fungicides and wound healer (Tian et al., 2007). Bactericidal effect of silver nanoparticles against a broad range of microbes including antibiotic resistant bacteria has been reported by many researchers, hence it is likely that silver nanoparticles may represent a new generation of antimicrobials (Rai et al., 2009) and powerful nano-weapons against multi-drug resistant bacteria (Rai et al., 2012). Silver nanoparticles may generate a revolution in the treatment of multidrug resistant microbes and transform many aspects of antimicrobial therapy. Silver nanoparticles demonstrated strong antiviral potential against several viruses, which include the following families: retroviridae, hepadnaviridae, paramyxoviridae, herpesviridae, poxviridae, orthomyxoviridae and arenaviridae (Galdiero et al., 2011). Silver nanoparticles showed potential antiviral activities against broad range of viruses. In addition, there are lesser chances of viruses that become resistant to silver nanoparticles as compared to conventional antiviral agents. The nanoparticles have multivalent interactions with viral surface components and cell membrane receptors which block viral entry into the cells (Portney & Ozkan, 2006).

Silver as an antimicrobial agent Silver is a rare, basic and naturally occurring element with high electrical and thermal conductivity and has been used for producing utensils, monetary currency, jewelry, photography, dental alloy and explosives since ancient times (Susan et al., 2009). Silver has been known from centuries to be curative and it has been extensively used to fight against infections (Hoyme, 1993). After the discovery of antibiotics, however, silver was relegated to very few uses as an antimicrobial agent. The mode of action of silver is dependent on Ag+ ions, which interacts with respiratory enzymes, the electron transport system and DNA to stop the bacterial growth (Li et al., 2006). Due to the intrinsic antimicrobial properties of silver, various types of silver compounds are used in Ayurvedic (a system of traditional medicine native to Indian subcontinent and a form of alternative medicine) and Unani (‘‘Greek Medicine’’, a form of traditional medicine widely practiced in South Asia) medicine, e.g. silver nitrate, which has been used in treatment of venereal diseases and in eye drop formulations (Landsdown, 2002), silver sulfadiazine in treatment of burn wounds (Atiyeh et al., 2007, Castellano et al., 2007), silver zeolite in food preservation and disinfection (Matsumura et al., 2003) and also silver oxide, silver chloride, and silver cadmium powder are used in different formulations. Due to the development of nanotechnology, silver has made a strong comeback as a potential antimicrobial agent. As nanoscale materials are more reactive, silver nanoparticles are effective antimicrobial against a wide range of microbes including viruses (Gong et al., 2007). Silver nanoparticles showed broad-spectrum activity against several antibioticresistant bacteria (Rai et al., 2012), common pathogenic fungi (Gajbhiye et al., 2009) and viruses (Sun et al., 2005). Bactericidal activity of silver nanoparticles was extensively studied by researchers against different bacteria (Birla et al., 2009; De Souza et al., 2006; Duran et al., 2007; Gade et al.,

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2010; Ingle et al., 2008; Tang et al., 2011). Silver nanoparticles are more resistant to changes in temperature and humidity if compared to traditional antimicrobials and have the huge advantage in the lack of easy microbial resistance induction. In addition to the benefits over traditional antiviral agents, silver nanoparticles have been shown to exert antimicrobial effects on a wide range of bacteria and viruses, making them broad-spectrum antimicrobials.

Synthesis of metal nanoparticles In the last few years, the number of reports on synthesis of metal nanoparticles with a special attention to silver nanoparticles has increased dramatically due to the enormous possibilities of applications including those correlated to their antimicrobial properties. Several different physical, chemical and biological approaches have been used for the synthesis of silver nanoparticles. Silver nanoparticles have been synthesized through an array of methods and the development of better experimental procedure for the synthesis of nanoparticles of different size, shape and controlled polydispersity is pivotal (Mukherjee et al., 2002). Nanoparticles produced through different processes and for different purposes may vary in surface charge and agglomeration state and thus in activity. Each synthetic method has its own merits and limitations: an impressive number of methods for nanoparticles synthesis have been reported in literature. For an extensive coverage of the chemical and biological synthesis of metal nanoparticles, there are several recent reviews available (Faramarzi & Sadighi, 2013; Mittal et al., 2013; Narayanan & Sakthivel, 2010; Sweet & Singleton, 2012; Vaidyanathan et al., 2009). The most common methods involve the use of an excess of reducing agents such as sodium citrate or sodium borohydride (Creighton & Albrecht, 1979). Longenberger (1995) produced Au, Ag and Pd metal colloids from airsaturated aqueous solutions of polyethylene glycol (PEG). There are many methods of nanoparticles synthesis, but these methods can be broadly classified as wet or dry processes. Wet synthesis methods are commonly referred to as ‘‘bottom-up’’ synthesis methods because silver nanoparticles are constructed atom-by-atom through a nucleation process. Dry synthesis methods of creating nanoparticles are typically known as ‘‘top-down’’ methods because they involve breaking down bulk silver into silver nanoparticles. Initially, the reduction of various complexes with metallic ions leads to the formation of atoms, which is followed by agglomeration into oligomeric clusters. Controlled synthesis is usually based on a two-step reduction process: in the first step a strong reducing agent is used to produce small particles; in the second step these small particles are enlarged by further reduction with a weaker reducing agent. An array of other physical and chemical methods has been used to produce nanomaterials. In order to synthesize noble metal nanoparticles of particular shape and size specific methodologies have been formulated, such as ultraviolet irradiation, aerosol technologies, lithography, laser ablation, ultrasonic fields, and photochemical reduction techniques, although they remain expensive and involve the use of hazardous chemicals (Dong et al., 2013; Fei et al., 2013; Guzman et al., 2009; He et al., 2013; Tran et al., 2013). Therefore, there is a

Metal nanoparticles as protective Nanoshield

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growing concern to develop environment-friendly and sustainable methods. Bacteria, fungi, algae, actinomycetes, plants, etc. have been successfully used for the synthesis of nanoparticles. To optimize biological production of nanoparticles, microbial cultivation methods and extraction techniques have to be standardized; in fact, factors such as shape, size and nature of nanoparticles can be simply controlled through modification of pH, temperature and nutrient media composition. Owing to the rich biodiversity of microbes, their potential as biological systems for nanoparticles synthesis is yet to be fully explored. Fungi and bacteria were most preferably investigated for their ease and rapid rate of cultivation. Some of the bacteria used for the synthesis of silver nanoparticles include, Pseudomonas stutzeri (Klaus-Joerger et al., 2001), Enterobacter cloacae (Shahverdi et al., 2007), Bacillus licheniformis (Kalimuthu et al., 2008), Bacillus subtilis (Saifuddin et al., 2009), Bacillus sp. (Pugazhenthiran et al., 2009), Escherichia coli (Gurunathan et al., 2009), Klebsiella pneumoniae (Mokhtari et al., 2009), Brevibacterium casei (Kalishwaralal et al., 2010). Bacteria that have been used for the synthesis of other metal nanoparticles include: Rhodopseudomonas capsulata (He et al., 2007), E. coli, Desulfovibrio desulphuricans (Deplanche & Macaskie, 2008), B. casei (Kalishwaralal et al., 2010), B. licheniformis (Kalimuthu et al., 2008) for the synthesis of gold nanoparticles; Clostridium thermoaceticum (Cunningham & Lundie, 1993), K. planticola (Sharma et al., 2000), E. coli (Sweeney et al., 2004) and Rhodopseudomonas palustris (Bai et al., 2009) for cadmium and cadmium sulphide nanoparticles. Rai et al. (2009) proposed the term ‘‘Myconanotechnology’’ to point out research carried out on nanoparticles synthesized by fungi. Myconanotechnology is the integrated discipline of mycology and nanotechnology. So far many fungal species have been exploited for the synthesis of silver nanoparticles including endophytic fungus Colletotrichum sp. (Shankar et al., 2003), Phoma sp. (Chen et al., 2003) soil fungi like Aspergillus fumigatus and A. niger (Bhainsa & D’Souza,

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2006; Gade et al., 2008), Phaenerochaete chrysosporium (Vigneshwaran et al., 2006), Fusarium oxysporum (Duran et al., 2005), F. semitectum (Basavaraja et al., 2008), F. acuminatum (Ingle et al., 2008), F. solani (Ingle et al., 2009), P. glomerata (Birla et al., 2009), Penicillium fellutanum (Kathiresan et al., 2009), Alternaria alternata (Gajbhiye et al., 2009), Trichoderma viride (Fayaz et al., 2010), A. terreus (Li et al., 2011), Trichophyton rubrum, T. mentagrophytes and Microsporum canis (Moazeni et al., 2012), F. oxysporum var. lycopersici (Riddin et al., 2006), F. culmorum (Bawaskar et al., 2010), Pestalotia sp. (Raheman et al., 2011). Apart from silver, several other metal nanoparticles have been synthesized by fungi like platinum nanoparticles by F. oxysporum var. lycopersici, (Riddin et al., 2006), zirconia nanoparticles by F. oxysporum (Bansal et al., 2007), cadmium sulphide nanoparticles by F. oxysporum (Sanghi & Verma, 2009) and lead nanoparticles by Aspergillus sp. (Pavani et al., 2012).

Metal nanoparticles as antiviral agent Metal nanoparticles are very effective antiviral agents and act either inside the host by inhibiting viral replication or outside by blocking the entry of viral particles (Table 1). Fujimori et al. (2011) investigated the antiviral activity of copper iodide (CuI) nanoparticles of 160 nm size against swine influenza virus, pandemic H1N1. By performing titration by plaque assay they found that the virus titer was decreased due to incubation with CuI nanoparticles in a dose-dependent manner (Fujimori et al., 2011). The study of inhibition of feline calicivirus (FCV), a non-enveloped virus, by CuI nanoparticles was performed using Crandell–Rees feline kidney (CRFK) cells (Shionoiri et al., 2012). Results showed a seven times lower infectivity of FCV following a treatment of 1 mg/ml CuI nanoparticles. The antiviral potential of CuI nanoparticles was mainly attributed to Cu+ ions which lead to generation of reactive oxygen species (ROS) followed by capsid protein oxidation. Thus, they suggest that CuI nanoparticles continuous supply of Cu+ ions may be

Table 1. Antiviral metal nanoparticles. Nanoparticle characteristics

Size (nm)

Virus

Mechanism of action

Ref.

Gold (Au) nanoparticles coated with mercaptoethane sulfonate (MES) Gold nanoparticles coated with multiple copies of an amphiphilic sulfate-ended ligand Sialic acid (SA) functionalized gold nanoparticles Multivalent water-soluble gold glyconanoparticles (mannoGNPs) Copper iodide (CuI) nanoparticles

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Herpes simplex virus type 1 (HSV-1)

Competition for the binding of the virus to the cell

Baram-Pinto et al., 2010

2

Human immunodeficiency virus type 1 (HIV-1)

Binding to gp120

Di Gianvincenzo et al., 2010

14

Influenza virus

Papp et al., 2010

115

Human immunodeficiency virus type 1 (HIV-1)

Inhibition of virus binding to the plasma membrane Inhibition of DC-SIGN binding to gp120

160

Influenza A virus of swine origin (pandemic [H1N1] 2009)

Copper iodide (CuI) nanoparticles

100–400

Feline calicivirus (FCV)

Glass fibre coated with iron oxide (Fe2O3) nanoparticles Titanium dioxide (TiO2) nanoparticles

NR*

Rotavirus and bacteriophage MS2

4–10

Influenza virus strain (H3N2)

Generation of hydroxyl radicals and degradation of viral proteins ROS generation and subsequent capsid protein oxidation Adsorption of virus on nanoparticles Fragmentation of viral envelope

Lu et al., 2008 Fujimori et al., 2011 Shionoiri et al., 2012 Nangmenyi et al., 2011 Mazurkova et al., 2010

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responsible of viral replication inhibition (Shionoiri et al., 2012). It was found that conjugation to gold nanoparticles can convert therapeutically inactive organic molecules into highly active drugs (Bowman et al., 2008). Di Gianvincenzo et al. (2010) described that gold nanoparticles coated with amphiphilic sulfate-ended ligand bind with the HIV envelope glycoprotein gp120 to inhibit infectivity of HIV in vitro. Papp et al. (2010) tested sialic acid (SA) functionalized gold nanoparticles of both 2 nm and 14 nm against the influenza viruses and found that 14 nm gold nanoparticles can inhibit the hemagglutination at nanomolar concentrations, but there is no significant activity of 2 nm gold nanoparticles. Thus, according to these findings, the activity of gold nanoparticles depends on the particle dimension and the spatial distribution of ligand receptor molecules (Papp et al., 2010). Gold nanoparticles coated with mercaptoethane sulfonate (MES) were tested in antiviral assays using the wild-type HSV-1 McIntyre strain (Baram-Pinto et al., 2010). For the inhibition experiments, Vero cells and/or virus solutions were treated with Au-MES nanoparticles at different time points to analyze the different stages of the viral infection that may be blocked. The results obtained indicate that sulfonate-capped gold nanoparticles inhibit HSV-1 infectivity by blocking early stages of virus replication. Martinez-Avila et al. (2009) prepared a small library consisting of manno-GNPs (multivalent water-soluble gold glyco-nanoparticles) and used it for inhibition of the receptor binding activity of HIV gp120. The glycoprotein gp120 is located on the viral envelope and binds with the DC-SIGN (dendritic cell-specific intracellular adhesion molecule3-grabbing non-integrin) adhesion molecule of dendritic cells. They found that the prepared manno-GNPs mimics DC-SIGN and thus prevents the binding of gp120 to DCSIGN. Further, they also studied the uptake of gold nanoparticles inside the cell bearing HIV gp 120 oligomannosides (Martinez-Avila et al., 2009). Nangmenyi et al. (2011) developed a new nano-material system made of iron oxide (Fe2O3) nanoparticles loaded on fiberglass and studied their antiviral potential against the

model virus, MS2 phage and rotavirus (Nangmenyi et al., 2011). Antiviral activity of titanium dioxide (TiO2) nanoparticles against influenza virus was reported (Mazurkova et al., 2010). They prepared TiO2 nanoparticles of size 4–10 nm by the hydrolysis of TiCl4, and tested them against Influenza virus strain (H3N2) grown on chicken embryos suspension culture. Their electron microscopic observation showed that influenza virus was destroyed by titanium dioxide nanoparticles within 30 min of incubation. They also suggested that the virus inactivation properties of TiO2 nanoparticles might be based on the direct contact between nanoparticles and virus particles. To find out the mechanisms of the antiviral effect of the TiO2 nanoparticles, they studied the effect of nanoparticles in different condition as in dark, under ultraviolet irradiation, and during daylight illumination. They found that the antiviral activity of TiO2 nanoparticles against influenza virus was not dependent upon daylight illumination or ultraviolet illumination. They also suggested that TiO2 nanoparticles inactivate the influenza virus by virus envelope destruction (Mazurkova et al., 2010).

Antiviral potential of silver nanoparticles against different viruses As antiviral agents act directly and rapidly on viral particles, bind with virus coat proteins and disrupt either their structure or function. Though any type of metal may exert certain antiviral potential, most research has been carried out to determine the antiviral activity of silver nanoparticles (Table 2), and showed that silver nanoparticles are, indeed, the most effective metal-based antiviral agents. Interesting study has been recently carried out where 25-nm AgNPs were able to mediate a consistent reduction in Vaccinia virus (VACV) entry at non-cytotoxic concentrations. AgNPs prevented both direct fusion and macropinocytosis-dependent entry of VACV; in fact cells where a vital component of macropinocytosis (Pak1) had been knocked down showed a reduced loss of AgNP anti-entry effects. Furthermore, Western blot analysis suggested that AgNPs bind directly to the entry fusion complex of VACV revealing a potential

Table 2. Antiviral silver nanoparticles. Nanoparticle coating

Size (nm) Virus

Mechanism of action

Poly N-vinyl-2-pyrrolidone (PVP) coating

1–10

Human immunodeficiency virus type 1 (HIV-1)

Binding to gp120

Naked

10–50

Hepatitis B virus (HBV)

Naked

5–20

Influenza virus

Mercaptoethane sulfonate 4 (MES) coating Poly N-vinyl-2-pyrrolidone (PVP), 65–72 bovine serum albumin (BSA) and recombinant F protein from RSV (RF 412) coating Naked and polysaccharide coating 10–80

Monkeypox virus (MPV)

Naked and polysaccharide coating

Tacaribe virus (TCRV)

NR*, not reported.

10

Herpes simplex virus type 1 (HSV-1) Respiratory syncytial virus (RSV)

Ref.

Elechiguerra et al., 2005; Lara et al., 2010; Sun et al., 2005 Interaction with double stranded DNA Lu et al., 2008 and/or binding with viral particles Possible interaction with hemaggluMehrbod et al., 2009; tinin Interaction with viral Particles Xiang et al., 2011 Competition for the binding of the Baram-Pinto et al., 2009 virus to the cell Interference with viral attachment Sun et al., 2008

Block of virus–host cell binding and penetration Inactivation of virus particles prior to entry

Roger et al., 2008 Speshock et al., 2010

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Figure 1. Schematic representation of the reported activity of different kinds of functionalized and naked silver nanoparticles against viruses. (HIV, human immunodeficiency virus, TCRV, Tacaribe viruses, RSV, respiratory syncytial virus, HBV, hepatitis B virus, MPV, monkeypox virus, HSV, herpes viruses, MES, mercaptoethane sulfonate, PVP, poly N-vinyl-2-pyrrolidone).

virucidal mechanism (Gaikwad et al., 2013). Silver nanoparticles interaction with viral biomolecules suggest that silver nanoparticles have a huge potential not only to face the challenge offered by viral infections but also to enhance the quality of existing antiviral therapies. Depending on the interaction and virucidal effect of silver nanoparticles against viruses such as, hepatitis B virus (Lu et al., 2008), HIV-1 (Elechiguerra et al., 2005; Lara et al., 2010; Sun et al., 2005) herpes simplex virus type 1 (Baram-Pinto et al., 2009), respiratory syncytial virus (Sun et al., 2008), tacaribe virus (Speshock et al., 2010), monkeypox virus (Rogers et al., 2008) and influenza virus (Mehrbod et al., 2009; Xiang et al., 2011), it can be predicted that silver nanoparticles act as protective antiviral shields (Figure 1). Silver nanoparticles have shown antiviral efficacy against several viruses regardless of the specific family, therefore silver nanoparticles provide the opportunity of developing broad-spectrum antiviral drugs. This is one of the major point in favor of the development of silver nanoparticles as antiviral drug, since they might be of sure benefit when facing unknown viruses or viruses for which we lack specific antivirals. Nevertheless,

each nanoparticle has different properties as a consequence of its production method and the available data from literature are quite heterogeneous and of difficult categorization, in fact, different researchers have focused their interest on a specific virus or on specifically produced or coated silver nanoparticles. In the remaining of the present section we have described the available data for each virus. Human immunodeficiency virus (HIV-1) Lara and colleague demonstrated that silver nanoparticles inhibit HIV-1 by interacting with the disulphide bond region in the CD4 binding domain of glycoprotein gp120 receptor present on the (HIV-1) viral envelope (Lara et al., 2010). They also extensively studied the action of silver nanoparticles against HIV-1 and found that the action of silver nanoparticles do not depend on the cell tropism owing to which silver nanoparticles also interact with other strains of HIV-1 having different tropism, and antiviral resistance (Lara et al., 2010). HIV-1 enters cells with the help of the envelope glycoprotein gp120, which binds to the host cell receptor.

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Elechiguerra et al. (2005) studied three types of silver nanoparticles with different surface behavior as foamy carbon silver nanoparticles, PVP (Poly N-vinyl-2pyrrolidone) coated silver nanoparticles, and BSA (bovine serum albumin) coated silver nanoparticles. Interactions of silver nanoparticles with HIV-1 were observed using High Angle Annular Dark Field (HAADF) scanning transmission electron microscope. They observed that silver nanoparticles of 1–10 nm interact with the sulfur-bearing residues of the gp120 glycoprotein. Further, they also found that PVP-coated and BSA conjugated nanoparticles showed slightly lower inhibition efficacy due to their coated surface. In contrast, foamy carbon silver nanoparticles have a greater inhibitory potential (Elechiguerra et al., 2005). A luciferase-based assay also proved that PVP coated silver nanoparticles were an effective virucidal agent. Silver nanoparticles inhibited the initial stages of the HIV-1 replication by preventing the gp120-CD4 interaction and attachment (Lara et al., 2010). Sun et al. (2008) studied the antiviral potential of silver nanoparticles by HEPES buffer and found that silver nanoparticles have dose-dependent cyto-protective as well as anti-HIV-1 activity. They further reported superiority of silver nanoparticles over gold nanoparticles for their antiviral and cyto-protective activities against HIV-1 infection by using Hut/CCR5 cells (Sun et al., 2008). An interesting application of silver nanoparticles has been described by Fayaz et al. (2012). They used nanoparticles as a coating for polyuretan condoms. Such nanosilver coated condoms exerted a highly inhibitory activity against HIV-1, HSV-1, HSV-2 and several bacteria and fungi and can be considered a real broadspectrum antimicrobial agent against sexual-transmitted diseases causing pathogens. Their further study showed that AgNPs produced by fungi are able to inhibit HSV-1 and 2 infectivity in a dose-dependent manner, showing the wide possibility of using a green-chemistry approach to produce antiviral compounds (Fayaz et al., 2012). Hepatitis B virus (HBV) Lu et al. (2008) reported that silver nanoparticles inhibit HBV replication by binding to HBV DNA and also inhibit the synthesis of HBV RNA and formation of extracellular virions. Further, they studied the activity of polydispersed silver nanoparticles against the HBV and found that the nanoparticles having diameter 10 nm and 50 nm showed antiviral activity without cellular toxicity, however, nanoparticles of 800 nm in diameter were found to have increased cellular toxicity. Antiviral effects of silver nanoparticles on HBV using a human hepatoma cell line were studied and silver nanoparticles of 10 and 50 nm showed high binding affinity for HBV DNA and extracellular virions. Moreover, it was reported that silver nanoparticles also inhibit HBV RNA and extra cellular virions production in vitro (Lu et al., 2008). Influenza virus Mehrbod et al. (2009) studied the antiviral effects of nanosilver against influenza virus. They treated MDCK (Madin-Darbey Canin Kidney) cell cultures with nanosilver and observed the effects during and after virus infection. Among the effect of different concentration of nanosilver

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studied, it was reported that nanosilver at concentration up to 1 mg/ml was non-toxic to MDCK cells. Inhibitory effects of nanosilver on the virus and its cytotoxicity were assessed by haemagglutination (HA) assay and concluded that nanosilver can destruct virus membrane glycoproteins (Mehrbod et al., 2009). Further experiments to investigate the activity of silver nanoparticles against influenza virus were performed. They synthesized silver nanoparticles with sizes varying from 5 to 20 nm and tested them with a number of viral infectivity inhibition assays. Results from these studies suggested that silver nanoparticles provide a strong protection against influenza virus infections without the risk of cell toxicity (Xiang et al., 2011). Herpes simplex virus type-1 Baram-Pinto et al. (2009) described the antiviral potential of metal nanoparticles against HSV-1. Silver nanoparticles were developed in such a way that they should mimic heparan sulfate (HS) in order to compete and inhibit the binding of the virus with host cell. The novel designed silver nanoparticles coated with MES were tested against HSV-1 McIntyre strain. In antiviral assays, virus was treated with MES-coated silver nanoparticles at different time intervals to analyze the block at different stages of the viral infection. They found that silver nanoparticles coated with sulfonate have the strong ability to inhibit HSV-1 infections by preventing the binding to host cells and ultimately block the entry of virus into the cells (Baram-Pinto et al., 2009). Respiratory syncytial virus Three types of conjugated silver nanoparticles were prepared using three types of coatings: poly N-vinyl-2-pyrrolidone (PVP), bovine serum albumin (BSA) and recombinant F protein from RSV (RF 412). All these conjugated silver nanoparticles were used against the RSV infection in Hep-2 cell culture (Sun et al., 2008). While studying the interaction between conjugated silver nanoparticles and RSV, it was observed that BSA and RF 412 conjugated silver nanoparticles interact with RSV without any specific association and attachment. But silver nanoparticles conjugated to PVP showed binding ability to the viral surface with a regular spatial arrangement and effective interaction with G proteins present on the envelope of the RSV virion. Additionally, they studied the cytotoxicity of each compound by using the Trypan Blue assay and found that all the above conjugates showed a reduction of cell viability lower than 20% at a concentration of 100 mg/ml (Sun et al., 2008). Poxviruses Rogers et al. (2008) tested the antiviral activity of different types of silver nanoparticles against Monkeypox Virus (MPV) by plaque reduction assay. In their study they used plasma gas-synthesized silver nanoparticles of 25, 55 and 80 nm and the polysaccharide coated silver nanoparticles of 10, 25 and 80 nm. They found that the polysaccharide coated silver nanoparticles of the size of 25 nm and naked silver nanoparticles of the size of 55 nm demonstrated significant dose-dependent inhibitory action on MPV plaque formation.

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They concluded that silver nanoparticles may prevent the early steps of virus penetration by blocking virus host cell attachments or they can disrupt intracellular virus replication (Rogers et al., 2008).

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Tacaribe virus Speshock et al. (2010) studied the antiviral potential of two types of silver nanoparticles (uncoated and polysaccharide coated) against TCRV. Vero cells infected with viruses pretreated with silver nanoparticles (uncoated silver nanoparticles) showed remarkable, i.e. 50% reduction in progeny of TCRV. While, the viruses treated with polysaccharide coated silver nanoparticles were found to have little infectivity reduction. Possible mechanism for a decrease in TCRV infectivity may involve binding of silver nanoparticles with viral membrane glycoproteins, which function as receptor for host cell binding, and therefore, preventing the internalization of the viral particles prior to the cell exposure (Speshock et al., 2010). It also prevents the viral uncoating in the endosome and decreases viral replication by interfering with the TCRV RNA-dependent RNA polymerase.

Toxicity of nanoparticles Silver nanoparticles are being increasingly used due to their inherent antimicrobial activity and various beneficial properties for the betterment of mankind (Ip et al., 2006). Conversely, their increased use raised several issues related to the health and environmental impacts. Cellular toxicity It has been observed that at low concentrations silver nanoparticles possess excellent antimicrobial activity whereas at higher concentration they induce toxic effects to higher organisms, including mammalian cell lines (Han et al., 2012). Therefore, with the increase in research in the field of nanotechnology there is an increasing risk of exposure to nanoparticles (Clancy et al., 2008). The toxicity of silver nanoparticles is evaluated by performing different biochemical assays in vitro and in vivo. Toxicity assessments usually include the analyses of the effects such as measuring changes in cellular morphology, generation of ROS, metabolic activity during the exposure and expression of various stress markers. Currently, there are a number of reports available which depicts the various effects and mechanisms of silver nanoparticles toxic action. They all suggest that beyond certain limit silver nanoparticles induce toxic effects both in vivo and in vitro. It is also well established that human get exposed to nanoparticles through penetration in the skin (Tinkle et al., 2003), via inhalation (Geiser et al., 2005) and via ingestion (Bockmann et al., 2000). In this respect, Kaur & Tikoo (2012) measured cellular changes in cells of skin or lung epithelium and murine macrophages following a silver nanoparticles treatment. The amount of silver nanoparticles used in their study ranged from 5 to 100 mg/ml and results showed a dose-dependent increase of cellular disruption and generation of ROS together with increased expression of stress markers such as pp38, TNF-a and HSP-70. An independent study on A549 cells supports similar conclusions

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(Chairuangkitti et al., 2013) and also demonstrated a time and concentration-dependent reduction in cell viability and mitochondrial membrane potential (MMP) with increase in apoptotic cells and cell cycle arrest. Induction of stress response in eukaryotic cells is one of the mechanisms resulting in the toxicity of silver nanoparticles. Singh & Ramarao (2012) reported the internalization of silver nanoparticles via scavenger receptor-mediated phagocytosis in murine macrophages. These effects were confirmed by localizing the silver nanoparticles in the intracellular milieu by confocal and electron microscopy. It is still controversial whether the toxicity of silver nanoparticles is due to themselves or to the release of Ag ions when they are suspended in the suitable solvent. Asharani et al. (2009) suggested that the surface oxidation of silver nanoparticles, after contact with cell culture medium or proteins in the cytoplasm, releases Ag+ ions that might increase toxicity. In this regard, Singh & Ramarao (2012) further supported the involvement of Ag ions in toxicity because of mitochondrial damage, and thereby apoptosis and cell death. Furthermore, they also confirmed that AgNPs dissolve 50 times faster inside the cell cytoplasm as compared to water. On the contrary, the results obtained by Grosse et al. (2012) showed that silver ions had lesser effect on the colony formation of rat brain endothelial (RBE4) cells than nanosilver particles. Grosse et al. (2012) suggested that silver nanoparticles cause membrane damage by accumulation on the cell surface thus disrupting the normal functioning of the cell. It is also a well-accepted theory that smaller sized nanoparticles cause more harm in a size and dose-dependent manner, as compared to their larger counterpart. It has also been proposed that the toxicity of silver nanoparticles depends on their surface chemistry (Sur et al., 2012). Interestingly, citrate reduced silver nanoparticles were reported to induce a time- and concentration-dependent increase in necrotic or apoptotic cells as well as increased geno-toxicity with up regulation of p53. Whereas, lactose and a 12-base long oligonucleotide modified silver nanoparticles have been found to be comparatively safer. Kim et al. (2009) studied the biocompatibility of both uncoated and polysaccharide coated silver nanoparticles with Vero cells. Vero cells were treated with polydisperse silver nanoparticles and it was observed that cell viability decreases by 25–60%. They concluded that polysaccharide coated silver nanoparticles were less cytotoxic as compared to the uncoated silver nanoparticles and these activities also found to be dose dependent (Kim et al., 2009). In vitro assessments of toxic effect of silver nanoparticles usually rely on use of cell cultures. However, such studies do not mimic exact condition as that of the in vivo condition, only giving an idea of the probable harmful effect up to a certain extent. Therefore, in vivo studies are very important to get a closer look into the exposure effects. Inhalation of silver nanoparticles in rats for longer time periods can lead to their accumulation in the lung, where they could lead to harmful effects. Ji et al. (2007) evaluated the inhalation effects of silver nanoparticles for 4 weeks. The study revealed the accumulation and transport of silver nanoparticles from lung to gastrointestinal tract and liver. Additionally the ingestion of colloidal silver was also found to cause liver and kidney damage (Kim et al., 2010). Asharani et al. (2008) assessed the

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concentration-dependent toxicity of silver nanoparticles on zebrafish (Danio rerio). Silver nanoparticles were also reported to hamper the normal development of the fish embryo. Moreover, after entry inside the body silver nanoparticles are able to cross the blood–brain barrier (BBB) (Sharma et al., 2009) as well as blood–testes barrier (Braydich-Stolle et al., 2005), thereby causing the harmful effects. From this discussion it is obvious that notwithstanding the vast research going on globally, the precise mechanism of nanosilver toxicity has not been fully elucidated. Expanding toxicological in vitro and in vivo data is very important for the design of biocompatible silver nanoparticles in order to define the boundary beyond which silver nanoparticles would be toxic and within which they would be safe for use in various biomedical and other applications. Environmental risk Assessment of the environmental risks requires analysis of environmental release, mobility, bioavailability, and toxicity of metal nanoparticles. Release of silver nanoparticles into the environment takes place from point sources, i.e. from their

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origin, during their production, and from non-point sources, such as deposition in the atmosphere, and from the products containing nanoparticles (Nowack & Bucheli, 2007). Due to the nano dimension these nanoparticles may have significant impact on biotic component and bioavailability of toxins or nutrients. The potential interaction of nanoparticles with toxic organic compounds may amplify or lighten their toxicity. Thus, organic pollutants and nanoparticles can create an inert system for living organisms, in which toxic agents are adsorbed by nanoparticles, reducing their free concentration and diminishing the toxicity (Simonet & Valcarcel, 2009). As silver nanoparticles are strong antimicrobials, ecologists feel that if metal nanoparticles are released in the environment, they will have serious impact on the natural system i.e. soil and aquatic communities. Silver in its bulk form is toxic to fish, algae, other aquatic plants and certain fungi, crustaceans (Panyala et al., 2008), zebrafish (Danio rerio) (Bowman et al., 2012) and soil forming bacteria (Albright & Wilson, 1974). Silver nanoparticles also have certain toxic effects on beneficial bacteria which include nitrogen fixing bacteria, ammonifying bacteria and chemolithotrophic bacteria. These micro-organisms play important roles in nitrogen fixation and biodegradation of organic matter. Certain bacteria also have

Figure 2. Potential antiviral mechanism of silver nanoparticles. (1) Silver nanoparticles interact with viral envelope and/or viral surface proteins; (2) Silver nanoparticles interact with cell membranes and block viral penetration; (3) Silver nanoparticles block cellular pathways of viral entry; (4) Silver nanoparticles interact with viral genome; (5) Silver nanoparticles interact with viral factors necessary for viral replication; (6) Silver nanoparticles interact with cellular factors necessary for productive viral replication.

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symbiotic relationships with leguminous plant, for providing nitrogen to these and other plants (Panyala et al., 2008). Therefore, the eventual toxicity of metal nanoparticles needs to be carefully addressed taking into consideration the potential damage to eukaryotic cells as the first target, but the global perspective of the environmental impact needs a proper attention.

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Conclusions The emergence, re-emergence and spreading of drug resistant viruses offer a challenge to develop novel and broad-active antiviral agents, which act as a protective shields and fight against pathogen attack. In fact, nanoparticles may represent the magic bullets which have specific physicochemical characteristics different from their bulk materials. It has been proved that silver nanoparticles have strong antiviral activities which have been evidenced by various studies. In addition, the virucidal potential of silver nanoparticles can be increased by understanding the exact site of interaction and mode of action leading to modification of the nanoparticles surface for a broader and more effective use. As there is a direct attachment with viral surface glycoproteins, silver nanoparticles can enter into the cell and prevent genome (DNA or RNA) replication, ultimately blocking the viral multiplication. Silver nanoparticles also help to prevent the fusion of the viral envelope with host cell blocking the viral penetration into the host cell. Possible mechanisms of action of silver nanoparticles are shown in Figure 2. Collectively, the data gathered in recent years, have shown that silver nanoparticles can be potent and broad-spectrum antiviral agents and therapeutics. Nonetheless, one should keep in mind that silver nanoparticles can be used in therapeutic with or without surface modifications considering their cytotoxic level to avoid human and environmental risks. Capping agents or stabilizers, added to naked silver nanoparticles (polyvinylpyrrolidone, citrate and PEG, etc.) have been proven biologically compatible; however, they possess their own antimicrobial properties, which would make the identification of inherent silver nanoparticles antiviral activity difficult. Further studies and more detailed description of the activity of naked nanoparticles are warranted to draw a precise outline of their effective antiviral activity. The capping agents may be further developed to increase the intrinsic activity of silver.

Acknowledgements We thank Department of Science and Technology, New Delhi, Govt of India for financial assistance under nanomission and University Grants Commission, New Delhi for support under UGC-SAP programme.

Declarations of interest Author reports no declarations of interest.

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Metal nanoparticles: The protective nanoshield against virus infection.

Re-emergence of resistance in different pathogens including viruses are the major cause of human disease and death, which is posing a serious challeng...
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