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A Synthetic Nanomaterial for Virus Recognition Produced by Surface Imprinting

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A Synthetic Nanomaterial for Virus Recognition Produced by Surface Imprinting ARTICLE Received 8 Oct 2012 | Accepted 21 Jan 2013 | Published 19 Feb 2013 DOI: 10.1038/ncomms2529 A synthetic nanomaterial for virus recognition produced by surface imprinting Alessandro Cumbo1,2, Bernard Lorber3, Philippe F.-X. Corvini1,4, Wolfgang Meier2 & Patrick Shahgaldian1 Major stumbling blocks in the production of fully synthetic materials designed to feature virus recognition properties are that the target is large and its self-assembled architecture is fragile. Here we describe a synthetic strategy to produce organic/inorganic nanoparticulate hybrids that recognize non-enveloped icosahedral viruses in water at concentrations down to the picomolar range. We demonstrate that these systems bind a virus that, in turn, acts as a template during the nanomaterial synthesis. These virus imprinted particles then display remarkable selectivity and affinity. The reported method, which is based on surface imprinting using silica nanoparticles that act as a carrier material and organosilanes serving as biomi- metic building blocks, goes beyond simple shape imprinting. We demonstrate the formation of a chemical imprint, comparable to the formation of biosilica, due to the template effect of the virion surface on the synthesis of the recognition material. 1 School of Life Sciences, University of Applied Sciences and Arts Northwestern Switzerland, Gru¨ndenstrasse 40, Muttenz CH-4132, Switzerland. 2 Department of Chemistry, University of Basel, Klingelbergstrasse 80, CH-4056 Basel, Switzerland. 3 Architecture et Re´activite´ de l’ARN, Universite´ de Strasbourg, CNRS, IBMC, UPR9002, 15 rue Rene´ Descartes, 67000 Strasbourg, France. 4 School of the Environment, Nanjing University, 210093 Nanjing, China. Correspondence and requests for materials should be addressed to P.S. (email: [email protected]). NATURE COMMUNICATIONS | 4:1503 | DOI: 10.1038/ncomms2529 | www.nature.com/naturecommunications 1 & 2013 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms2529 he design of artificial molecular recognition (nano)mater- following the method developed by Sto¨ber31. The statistical ials is an active field in the chemical sciences, with analysis of micrographs acquired using high-resolution field- Tapplications ranging from medical diagnostic1,2 and emission scanning electron microscopy (FESEM) revealed a mean environmental monitoring3 to national security4. Since the diameter of 410 nm. The high propensity of those nanoparticles advent of supramolecular chemistry in the 1980s, considerable to self-assemble into three-dimensional colloidal arrays represents effort has been invested in developing molecules that possess an additional evidence of their high monodispersity (Fig. 2a). defined, predictable recognition properties5–7. Special focus has The first step in VIPs synthesis consisted of grafting the been placed on macrocyclic molecules, which have been shown to template virions on the surface of the SNPs. In order to provide possess remarkable recognition properties with respect to anchoring amine moieties for this cross-linking, the SNPs were anions8, cations9 and small neutral molecules10. However, partially modified with aminopropyltriethoxysilane (APTES). A owing to a size discrepancy between host and guest molecules low density of amine groups at the SNP surface is essential to that is typically one to two orders of magnitude, applications with leave enough silanol groups for the further surface-initiated poly- larger targets, such as proteins2,11,12, are limited. condensation of the recognition layer. Molecular imprinting represents an alternative approach to the Further coupling of the virions was carried out in water using design of materials that possess specific molecular recognition glutaraldehyde as a homo-bifunctional crosslinker. We used two properties13,14. It is based on the formation of a supramolecular small RNA plant viruses as model viruses. Tomato bushy stunt complex of organic monomers together with a template molecule virus (TBSV) and turnip yellow mosaic virus (TYMV) are non- before polymerization. This procedure enables the three- enveloped, icosahedral, single-stranded RNA viruses (Fig. 1b). dimensional positioning of the recognition units in the produced Their capsids are made of 180 copies of protein subunits, with a organic polymer15,16. Inorganic molecularly imprinted materials mass of 40 kDa for TBSV and 20 kDa for TYMV32. The virions have also been developed. For instance, Katz and David15 reported have diameters of 33 and 28 nm, molecular weights of 9.0 Â 103 on the imprinting of bulk microporous silica. The originality of and 5.5 Â 103 kDa, and isoelectric points of 4.1 and 3.8, their approach lies on the choice of a building block that was used respectively. to occupy the micropores and to attach the functional groups to the Once the virions were bound, a silsesquioxane layer was grown walls of those pores. The so-produced materials were shown to from the surface of the SNPs. To produce this recognition layer possess shape-selective catalytic properties. by following a protein mimetic approach, we selected In spite of promising prospects for molecular imprinting, organosilanes that mimic the lateral chains of amino acids applications involving voluminous biomolecular targets are known to be of importance in protein–protein interactions hindered by the difficulty that arises when large biomolecules (Fig. 1c)33,34. We hypothesized that these building blocks will need access to binding sites within the produced polymer17. self-assemble at the surface of the virions before their covalent Nevertheless, examples of molecularly imprinted materials for incorporation within the recognition layer. This was expected to biomolecular recognition have been developed for proteins18–25. improve the recognition properties of the VIPs by creating not The most convincing examples had been developed using surface- only a shape but also a chemical imprint that is complementary to imprinting approaches. The imprinting of even bigger the surface of the virion. Hereinafter, the term VIPsOM stands for biomolecular entities, such as viruses, is of great interest, with particles imprinted with TYMV virions and having a recognition possible applications in purification, diagnostics and therapy. layer composed of an organosilanes mixture (OM), and the term Such imprinting also becomes more challenging as target size non-imprinted particles (NIPs)OM for NIPs produced in the increases. Few examples of virus imprinting using organic absence of template using the same OM. As controls, we selected polymers have been reported26–30. Nevertheless, the two additional formulations, one with tetraethyl orthosilicate performances of the materials produced are still fairly limited (TEOS) alone and one with a mixture of APTES and TEOS (AT). and virus imprinting remains a great challenge when the intent of The corresponding VIPs are abbreviated VIPsAT for TYMV- the design is ‘artificial antibodies’ that bind viral particles. Such imprinted particles having a recognition layer made of AT, and synthetic systems would undeniably find a number of possible NIPsAT for those produced under the same conditions in the applications, from virus production and diagnostics to, absence of template. ultimately, therapy. The kinetics of surface-initiated growth of the silsesquioxane Herein, we report a synthetic strategy leading to an artificial recognition layer in water at 10 °C followed by FESEM revealed organic–inorganic nanoparticulate material that possesses virus that the thickness of the external layer reached only 2 nm after imprints on its surface and that we name virus-imprinted 75 h when the poly-condensation reaction was performed with particles (VIPs). The method to produce VIPs is based on an TEOS alone (Fig. 2b). In the presence of APTES, the layer was sequential procedure consisting of three steps: (i) binding the 15 nm thick after 10 h. This faster growth can be safely attributed template virus on the surface of a carrier material (here, silica to the catalytic effect of the primary amine function of APTES on nanoparticles, SNPs), (ii) incubating these virus-modified nano- the hydrolysis of the organosilanes35. The size of the particles particles with a mixture of organosilanes, followed by the poly- prepared with the mixture of organosilanes increased according condensation of the latter to grow an organosilica (silsesquiox- to a sigmoidal function; the layer thickness reached 14 nm after ane) recognition layer thereby forming a replica of the virus; and 75 h (Fig. 2b). The slower kinetics as compared with that of the (iii) removing the template to free the imprints (Fig. 1). The APTES/TEOS mixture may be explained by the lower amount of possibility of controlling the kinetics of layer growth is APTES present in a constant total amount of organosilanes. demonstrated to enable the control of the size of the imprints These results demonstrate the possibility of growing an and, hence, the number of interaction points with the virion organosilanes layer at the surface of the nanoparticles under surface, ultimately permitting control of the affinity of the aqueous conditions. They also confirmed that neither the material for its template. crosslinking chemistry of the SNPs (using APTES and glutaraldehyde) nor the presence of the virions at the surface of the SNPs hampered this growth. Results An examination of the morphology of the particles produced VIPs synthesis and characterization. As the carrier
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