PMC:7376974 / 9885-24301 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7376974","sourcedb":"PMC","sourceid":"7376974","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7376974","text":"Silver Nanoparticles\nMany studies have shown that naked AgNPs have a good effect on the control and prevention of a variety of viral diseases (Table 1). However, the antiviral mechanism of nanosilver is still unclear. The antiviral action is associated with the following mechanisms: Nanosilver can prevent the virus from entering the host cells and inhibit the virus from binding to the cell receptor, thereby stopping the virus from infecting the targeted cells. AgNPs may be able to bind the viral surface protein and inhibit the interaction between the virus and the cell membrane receptors (Figure 2, left). However, it has been also reported that AgNPs can inactivate the virus through denaturation of surface proteins containing cysteine and methionine residues present on the viral capsid, in a similar way reported for bacteria. For example, AgNPs smaller than 10 nm were shown to interact with the sulfur-bearing residues of gp120 glycoprotein knobs distributed on the lipid membrane of HIV-1 virus, preventing the virus from binding to CD4 receptor site on the host cells, thus inhibiting the viral infection.11 By means of a viral adsorption assay, it was shown that the AgNP mechanism of anti-HIV action is based on the inhibition of the initial stages of the HIV-1 cycle. To demonstrate that the antiviral effect of AgNPs is due to the particle structure rather than to silver ions present in solution, the antiviral activity of silver sulfadiazine (AgSD) and silver nitrate (known antibacterial silver salts) was evaluated. Both salts showed a much lower therapeutic index than AgNPs in vitro, indicating that silver ions themselves are less efficient.12 These results point out that the antiviral efficacy is not only related to the dose of Ag+ ions present in solution but is also regulated by different other parameters (e.g., size, charge, and surface functionalization) associated with the nanosize dimension. For instance, in the case of Herpesviridae and Paramyxoviridae viruses (both enveloped viruses with embedded viral-encoded glycoproteins), AgNPs can effectively reduce their infectivity, by blocking the interaction between the viral particles and the host cells with an antiviral activity strictly dependent on the size and ζ potential of the AgNPs. As a general observation, it was reported that smaller nanoparticles have better antiviral effect. This effect was associated with the increase of the surface area, where smaller-sized AgNPs could bind more efficiently to the viral particles exerting a higher antiviral activity.13 Another study reported the impairment of Peste des petits ruminants virus (PPRV) replication after incubating infectious viral particles with AgNPs, which did not exhibit any virucidal effect even up to 900 μg/mL. This result suggested that the anti-PPRV activity of the AgNPs is due to the inhibitory effect on viral replication in the target cells. AgNPs do not prevent the binding of PPRV to host cells, but inhibit the entry of viruses into these cells. AgNPs can also interact with the surface and core of PPRV, but this interaction cannot kill the virus directly.12 The same results were then confirmed on other viruses. AgNPs with a diameter of 25 nm inhibited Vaccinia virus replication by preventing viral entry into host cells. However, AgNPs cannot prevent the virus from adsorbing onto the cells, and this virus is still infectious, indicating that AgNPs lack a direct virus-killing effect.13\nFigure 2 Potential antiviral mechanism of AgNPs. (1) AgNPs interact with viral envelope and/or viral surface proteins; (2) AgNPs interact with cell membranes and block viral penetration; (3) AgNPs block cellular pathways of viral entry; (4) AgNPs interact with viral genome; (5) AgNPs interact with viral factors necessary for viral replication; and (6) AgNPs interact with cellular factors necessary for productive viral replication. Reproduced with permission from ref (14). Copyright 2016 Taylor and Francis.\nTable 1 Antiviral AgNPs and Their Possible Mechanisms of Action\nvirus shape size (nm) active concentration mechanism of action ref\nHIV-1 spherical 1–10 25 μg/mL interaction with gp120 (11)\nHIV-1 IIIB – 30–50 440 μg/mL interaction with gp120 (19)\nHSV-1, HSV-2, and HPIV-3 – 20–50 not available possible interaction directly with the viral envelope or its protein (20)\nAdenovirus type 3 spherical 5–18 25 μg/mL direct destruction of virus particles and DNA structure (15)\nH1N1 influenza A virus spherical 5–20 12.5 μg/mL inhibition of respiratory enzymes and electron transport components and interference with DNA function (21)\nHBV spherical 10–50 5 μM interaction with double-stranded DNA and/or binding with viral particles (16)\nPPRV spherical 5–30 11.1 μg/mL interaction with virus surface and core (12)\nVaccinia virus spherical 25 not available preventing viral entry into host cells (13)\nMonkey pox virus (MPV) – 10–80 12.5 μg/mL blocking virus-host cell binding and penetration (22)\nTacaribe virus (TCRV) – 5–10 25 μg/mL inactivation of virus particles before entry (23)\nPoliovirus spherical 4–9 3.1 ppm preventing viral particles from binding to the receptors of RD cells (24)\nTGEV spherical \u003c20 12.5 μg/mL direct interaction with TGEV surface protein, such as TGEV S glycoprotein (18)\nlinear 60000–80000\nlinear 20000–30000 Alternatively, nanosilver can be combined with viral nucleic acids to change the capsid structure, affect the replication of viral genetic material, and make the virus inactive. For example, TEM analyses have shown that NPs can cause a change of the structure of the Ad3 virus from a hexahedral shape to an irregular shape, destroying its fibers and capsid proteins, leading to inhibition of the virus from binding to the host cells and destroying the DNA structure, preventing adenoviral infection.15 Nanosilver can also bind directly to the double-stranded DNA of hepatitis B virus to inhibit its replication.16\nIn other studies, it has been demonstrated that silver ions released from nanosilver can directly damage the viruses. Based in this property, an interesting application has been proposed. AgNPs were used as a coating on polyurethane condoms, effectively inhibiting the activity of HIV and herpes simplex virus (HSV). The hypothesized mechanism is that silver ions are transferred directly from oxidized NPs to biological targets, such as viral membrane proteins gp120 and gp41. In addition, a small amount of silver ion is also released from the coated contraceptives to improve the antiviral level.17\nAlthough the studies on naked AgNPs to reduce viral infectivity have shown their potential as broad-spectrum antiviral agents, the understanding of the specific antiviral action mechanism still needs to be elucidated in depth. Many studies have shown that the antiviral performance of naked AgNPs is related to their size, and smaller nanoparticles have better antiviral activities.16 In addition to particle size, the antiviral action of AgNP morphology has also attracted interest to fight against coronavirus. AgNPs and two types of silver nanowires were able to significantly cause an inhibitory effect on coronavirus transmissible gastroenteritis (TGEV)-induced host cell infection and TGEV replication. The mechanism is likely based on a direct interaction of AgNPs with TGEV surface proteins (e.g., TGEV glycoproteins) to inhibit the beginning of viral infection. It is possible that AgNPs and Ag nanowires alter the structure of some surface proteins of TGEV and then inhibit their recognition and adhesion to the cellular receptor pAPN.18\nAlthough the potential of AgNPs as antiviral agents has been commonly recognized, unfortunately, their wide biological applications are limited by the risks of self-aggregation and environmental pollution. Silver ions can be released from the surface of AgNPs and potentially pollute the environment, and their agglomeration into bulkier particles or fibers may change their biological characteristics, diminishing the antiviral effect. In several cases, it has been reported that naked AgNPs may affect human health.25 Therefore, research and development of AgNPs whose surface is modified or stabilized by protecting molecular layers is an urgent need to overcome these problems (Table 2). Poly(N-vinyl-2-pyrrolidone) (PVP) is the most commonly used stabilizer of AgNPs. The PVP-coated AgNPs are able to inhibit the activities of HIV-1, herpes simplex 2 virus (HSV-2), and respiratory syncytial virus (RSV).11,26,27 But compared to foamy carbon, small-sized PVP and BSA-coated AgNPs showed poor antiviral activity to the HIV-1 virus.11 For RSV, PVP-coated AgNPs have a specific binding capacity to the viral surface, evidencing a regular spatial arrangement and a clear interaction with G-protein.26 In addition, to improve the stability of AgNPs, their surface modification with antiviral drugs was proved to reduce the drug resistance caused by the drugs administered alone. Tannic acid-modified AgNPs showed good antiviral effects on HSV-2 infection in vitro and in vivo. The viral infection was inhibited only when these NPs directly interacted with HSV-2 virions. Indeed, the pretreatment of host cells with such AgNPs did inhibit the entry of HSV-2. Due to the high affinity of tannins to proteins and sugars, tannic acid can bind glycoproteins on the surface of viruses to make them inert, impairing glycoprotein function and preventing viruses from attaching and entering host cells.28\nTable 2 Surface-Modified Antiviral AgNPs and Possible Mechanisms of Action\nvirus shape size (nm) coating mechanism of action ref\nHIV-1 spherical 1–10 foamy carbon, PVP and BSA interaction with gp120 (11)\nRSV spherical – PVP, BSA, and recombinant F protein (RF 412) interaction with the G-protein on the virus surface (26)\nH1N1 influenza virus spherical 2–5 Oseltamivir inhibition of the activity of neuraminidase and hemagglutinin (34)\nAmantadine (35)\nZanamivir (36)\ninhibition of accumulation of reactive oxygen species (ROS)    \nHAV, NoV and CoxB4 spherical – polyphosphonium-oligochitosans preventing viral attachment and penetration (29)\nMPV spherical 10–80 polysaccharide blocking virus-host cell binding and penetration (22)\nTCRV spherical 10 polysaccharide inactivation of virus particles prior to entry (23)\nHSV-1 spherical 4 mercaptoethanesulfonate competition for the binding of the virus to the cell (30)\nEnterovirus 71 (EV71) spherical 2–5 PEI and antiviral siRNA inhibition of the accumulation of ROS and activation of AKT and p53 (37)\nHSV-2 spherical 13, 33, 46 tannic acid direct interaction and blocking of virus attachment, penetration and spread (28) The surface modification can also exert a synergistic antiviral effect. AgNPs decorated with polyphosphonium-oligochitosan (PQPOC) exhibited moderate to excellent antiviral activity against HAV, NoV, and CoxB4. In addition, AgNPs could interact with the virion glycoproteins and prevent viral attachment and penetration. PQPOC can also serve as an effective virus inhibitor by blocking the interaction of the targeted virus with the host through the electrostatic interaction between the cationic polymers and the negatively charged binding sites of the virus.29\nSurface-modified AgNPs can also prevent viral infection by competitive adsorption on host cells. The process of infection of cells by herpes simplex virus type 1 (HSV-1) involves the interaction between viral envelope glycoproteins and heparan sulfate (HS) on cell surface. Therefore, researchers designed AgNPs capped with mercaptoethanesulfonate (Ag-MES) to compete with the cellular HS through the sulfonate end groups, thereby blocking the virus from entering the cells.30\nA few years ago, it was shown that curcumin could prevent the replication and the budding of RSV,31 but the disadvantage of poor solubility and low bioavailability limited its clinical application.32 Curcumin was used as a reducing and capping agent to prepare stable curcumin AgNPs (cAgNPs) under physiological conditions. cAgNPs could reduce cytopathic effects induced by RSV and showed efficient antiviral activity against infection by directly inactivating the virus prior to entry into the host cells. Its antiviral effect was higher than curcumin alone or unmodified AgNPs (Figure 3).33\nFigure 3 Schematic representation of the synthesis of cAgNPs (A) and a proposed inhibition mode of cAgNPs against RSV infection (B). The inhibition mode of (B) shows that cAgNPs can reduce the binding ability of virus with the binding centers on the surface of cells (b) as compared to those without cAgNPs (a). Reproduced with permission from ref (33). Copyright 2016 Royal Chemistry Society. Alternatively, Zhu et al. prepared AgNPs surface-modified with oseltamivir, amantadine, and zanamivir (Ag@OTV,34 Ag@AM,35 and Ag@ZNV36), by chemical methods. The results showed that these nanoparticles can directly interact with the virions, resulting in viral function damages.\nOverall different studies have reported the capacity of AgNPs to block viral entry. However, there is not a concerted antiviral mechanism, but their activity differs from case to case, based on viral particle adsorption, capsid structure alteration, or surface protein denaturation. For AgNPs, the antiviral activity can be associated with different parameters including size, shape, surface charge, and functionalization but also to the topical release of silver ions able to disturb the viral cycle replication. As described before, bare AgNPs can be used as disinfectant agents, however their use in biological media is limited by their low colloidal stability and potential cytotoxicity. Surface functionalization can alleviate cytotoxicity, but it can also mask the nanoparticle surface, reducing their affinity for viral particles, thus reducing AgNP antiviral activity. For these reasons, AgNPs at the moment could find application mainly for surface disinfection and for topical administration. Further studies are needed to prepare safer AgNP formulations for systemic administration. In particular, the clarification of the antiviral mechanisms and the use of surface functional groups able to stabilize AgNPs in biological fluids without affecting their prominent antiviral activity are probably the most important challenges to 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