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WIREs Nanomed Nanobiotechnol
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Bridge over troubled waters: understanding the synthetic and biological identities of engineered nanomaterials

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Abstract Engineered nanomaterials offer exciting opportunities for ‘smart’ drug delivery and in vivo imaging of disease processes, as well as in regenerative medicine. The ability to manipulate matter at the nanoscale enables many new properties that are both desirable and exploitable, but the same properties could also give rise to unexpected toxicities that may adversely affect human health. Understanding the physicochemical properties that drive toxicological outcomes is a formidable challenge as it is not trivial to separate and, hence, to pinpoint individual material characteristics of nanomaterials. In addition, nanomaterials that interact with biological systems are likely to acquire a surface corona of biomolecules that may dictate their biological behavior. Indeed, we propose that it is the combination of material‐intrinsic properties (the ‘synthetic identity’) and context‐dependent properties determined, in part, by the bio‐corona of a given biological compartment (the ‘biological identity’) that will determine the interactions of engineered nanomaterials with cells and tissues and subsequent outcomes. The delineation of these entwined ‘identities’ of engineered nanomaterials constitutes the bridge between nanotoxicological research and nanomedicine. WIREs Nanomed Nanobiotechnol 2013, 5:111–129. doi: 10.1002/wnan.1206 This article is categorized under: Toxicology and Regulatory Issues in Nanomedicine > Toxicology of Nanomaterials

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Bridging nanotoxicology and nanomedicine. We posit that careful assessment of the physicochemical properties of engineered nanomaterials constitutes the ‘bridge’ between nanotoxicological research and nanomedicine insofar as a detailed understanding of material properties, i.e., the ‘synthetic identity’ is critical both for toxicological assessment of nanomaterials and for the development of novel nanomedicines (a). Furthermore, understanding the ‘synthetic’ and ‘biological’ identities of nanomaterials will facilitate the bridging of preclinical studies and the use of nanomaterials in medical imaging, drug delivery, and regenerative medicine (b). The ‘biological’ identity of a nanomaterial is largely determined by the ‘corona’ of biomolecules that forms in a biological environment; see text for details.

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Synthetic and biological identities of nanomaterials. Schematic view of the ‘synthetic’ identity of nanomaterials that is determined by material‐intrinsic properties and the ‘biological’ identity that is manifested in a living system and can be viewed as the sum of the context‐dependent properties of the nanomaterial. As discussed in this review, the biological identity is shaped, in part, by the adsorption of biomolecules (proteins and lipids) that form a ‘corona’ on the surface of nanoparticles; the composition of the bio‐corona depends on the particular biofluid (e.g., blood, lung fluid, and gastrointestinal fluid) and may exhibit dynamic changes as the nanoparticle crosses from one biological compartment to another. The physiological responses to nanomaterials are dictated by the synthetic and biological identities; a partial list of possible biological/toxicological outcomes is shown in this figure.

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Protein corona: role in proinflammatory responses. Fibrinogen is the major human plasma protein bound by poly(acrylic acid)‐coated gold nanoparticles (PAA–GNP). (a) SDS–PAGE of human plasma proteins bound to PAA–GNP with diameters of 5, 10, and 20 nm. Three major protein bands were observed at 65, 55, and 45 kDa. (b) Unbound fibrinogen following pull‐down with PAA–GNP with diameters of 5 nm (blue) or 20 nm (red). Purified fibrinogen (0.6 mg) was incubated with increasing amounts of PAA–GNP. Inset: unbound fibrinogen is plotted against total surface area for the two nanoparticles. (c) Crystal structure of fibrinogen. The protein was drawn using Swiss‐PdbViewer and coordinates for PDB entry 3GHG. Common domains are shown. Inset: the C‐terminus of the g chain (purple) that interacts with the Mac‐1 receptor. (Reprinted with permission from Ref 79. Copyright 2011 Macmillan Publishers Ltd.) (d) The schematic diagram illustrates how unfolding of fibrinogen on the surface of PAA–GNP leads to interaction with the integrin receptor, Mac‐1, on the surface of THP.1 monocytes, which in turn increases NF‐κB signaling leading to secretion of tumor necrosis factor‐α. It is pertinent to note that fibrinogen, which has a length of 45 nm and a diameter of 5 nm, is much larger than the 5‐nm PAA–GNP. Deng et al.79 showed that the maximum protein binding was 2 µg for the 5‐nm PAA–GNP, which represents one to two nanoparticles per fibrinogen molecule.

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