DNA Nanoarchitectonics: Assembled DNA at Interfaces - Langmuir

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DNA Nanoarchitectonics: Assembled DNA at Interfaces Stefan Howorka* Department of Chemistry, Institute of Structural Molecular Biology, University College London, London, WC1H 0AJ, England, United Kingdom ABSTRACT: DNA is a powerful biomaterial for creating rationally designed and functionally enhanced nanostructures. DNA nanoarchitectures positioned at substrate interfaces can offer unique advantages leading to improved surface properties relevant to biosensing, nanotechnology, materials science, and cell biology. This Perspective highlights the benefits and challenges of using assembled DNA as a nanoscale building block for interfacial layers and surveys their applications in three areas: homogeneous dense surface coatings, bottom-up nanopatterning, and 3D nanoparticle lattices. Possible future research developments are discussed at the end of the Perspective.

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INTRODUCTION

DNA: AN IDEAL BUILDING MATERIAL? DNA is an ideal building material when it comes to creating complex yet predictable nanoarchitectures from the bottom up. What are the other advantages and limitations of assembled DNA? How does DNA compare to more conventional chemical components such as organic and biogenic polymers? Among other biopolymers39 or dendrimers,40,41 DNA stands out because virtually any nanoscale architecture can be constructed with angstrom-scale precision.25 In addition, dedicated software programs42 help to design the molecular origami devices from scratch, thereby defining the sequences of the constituent DNA strands, which can, in most cases, be readily obtained from commercial suppliers. Furthermore, chemically modified DNA strands can be equipped with attachment linkers or fluorophores to expand the functional repertoire of the DNA nanostructures. Finally, physicochemical knowledge on the immobilization of DNA and nanobio interfaces is available.36,43−45 Although the ease of fabricating defined structures is probably the most important advantage, there are several limitations. Compared to chemically more robust polymers, assembled DNA nanostructures cannot withstand harsh acidic or high-temperature conditions because of the depurination46 and unzipping of the constituent DNA duplexes, respectively. In addition, DNA is highly negatively charged, which can induce undesired electrostatic interactions with positively charged molecules.47,48 In a related fashion, the chemistry of DNA is somewhat limited because its scope of natural built-in functional groups pales in comparison to those available in polypeptides49−51 and other biopolymers.5 Furthermore, the overall high structural rigidity of the DNA nanoarchitectures can be undesirable when the sought-after functional perform-

Controlling the nanoscale structure of functional interfaces is a cornerstone of basic and applied surface science.1,2 One premier route for rationally engineering substrate interfaces relies on self-assembled molecular layers composed of organic molecules,3 polymers,4 or biopolymers.5 Interfacial layers play an important role as thin-film coatings in electronics,6−9 filtration,10 biosensing, and biomaterials.11−19 The bottom-up formation of interfacial layers is also the main strategy toward patterns of inorganic nanoparticles and biomolecules for applications in nanotechnology, photonics, biophysics, and cell biology.20−22 Bottom-up nanofabrication is expected to gain further prominence because the alternative top-down techniques have advanced to the point where integration with self-assembly is required23 to build novel and efficient functional nanostructured devices.24 Among the available repertoire of molecular building blocks suitable for interfacial layers, DNA nanoarchitectures are the most recent addition. DNA nanostructures of different shapes can be rationally designed and built from smaller nucleic acid strands. In general, DNA nanotechnology is a very successful research area,25−34 and DNA nanostructures have also been exploited for homogeneous substrate coatings and the creation of defined nanopatterns and nanoarrays.35−38 This Perspective will provide an overview of DNA nanoarchitectonics at substrate interfaces by covering the main concepts and highlighting exemplary studies. After assessing how assembled DNA compares to more conventional polymeric building blocks, we will discuss three areas of applications of DNA nanoarchitectonics: homogeneous films with an emphasis on biomolecular recognition, 2D nanopatterns that are produced via the bottom-up route in optional combination with top-down nanofabrication, and 3D superlattices of nanoparticles. A concluding section will identify some possible areas of future research for interfacial DNA nanostructures. © XXXX American Chemical Society

Special Issue: Interfacial Nanoarchitectonics Received: November 15, 2012 Revised: January 6, 2013

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ance requires dynamic flexibility, such as in surface-passivating polymeric films.11,52−55 Finally, DNA nanostructures are more expensive to synthesize than organic polymers and dendrimers. Nevertheless, within these boundaries, an impressive variety of surface-attached DNA nanomaterials have been created.

and high-affinity binding of the nanostructure to the substrate’s gold surface (Figure 1B).59 Consequently, molecular receptors linked to the forth top vertex were presented to the ambient environment.65 This resulted in an improved recognition of the cognate analytes in terms of specificity and sensitivity as demonstrated for DNA (Figure 1A,B),60 proteins,60,61 and cocaine (Figure 1C)62 when compared to the conventionally surface-immobilized receptors. Remarkably, the tetrahedradecorated surface was also protein-resistant and hence achieved high selectivity in the presence of a complex analyte matrix of serum.62 Reflecting the general interest in the biophysics of these nanoarchitectures,66 structurally related DNA tetrahedra with controllable porosity may also be exploited as surfacetethered nanocages to release enclosed matter for drug delivery.67

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THIN FILMS OF DNA NANOARCHITECTURES: IMPROVING BIOMOLECULAR RECOGNITION Molecularly thin and laterally dense films composed of DNA structures have been constructed to improve the biomolecular recognition at biointerfaces. In general, efficient and correct binding of biomolecules is relevant in biosensing, purification, and biophysics.11−17 However, the specific interaction of molecules at interfaces can be impaired56 by restricted target accessibility caused by imperfectly packed receptors on locally crowded surfaces.44,57,58 Homogeneous films made up of DNA nanoarchitectures were able to overcome some of these problems.59−62 In particular, the folded DNA nanostructures functioned as molecular display agents that presented immobilized receptors in an orientated and laterally controlled fashion to the ambient environment, thereby facilitating the binding of cognate analytes. The display agents were nanoscale tetrahedrons featuring edges composed of double-stranded DNA (Figure 1A).63,64 Three of the tetrahedron’s four vertices were chemically modified with disulfide legs to enable the oriented

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NANOPATTERNING OF PLANAR SURFACES WITH DNA NANOARCHITECTURES In addition to the homogeneous coatings of substrates, DNA nanoarchitectures are predominately utilized to pattern surfaces on the nanoscale. In principle, nanopatterning with DNA can be achieved either in a bottom-up fashion or in combination with top-down approaches. In both cases, producing nanopatterns can open up many applications in nanotechnology, biophysics, and cell biology.22,23,68−71 In its simplest form, bottom-up nanopatterns of nucleic acids can be made with isolated bases to form porous networks,72,73 from flexible single-stranded and surface-tethered DNA molecules to obtain a porous 2D pattern,74 and with chemically modified DNA duplexes that self-assemble into nanoribbon features.75 Bottom-Up Patterning with DNA Tiles. Structurally more defined DNA nanostructures such as DNA tiles are better suited to generating complex yet predictable patterns. DNA tiles are up to 10 nm-big 2D structural units and are assembled from synthetic DNA oligonucleotides. One of the most basic tiles features a double-crossover (DX) motif28 in which two parallel aligned duplexes are connected by two interlinks (Figure 2A). Other types of tiles with different geometries are available.28,33 Because tiles can be equipped with singlestranded overhangs, it is possible to hybridize multiple tiles into larger assembled superstructures. The overall symmetry and shape of these higher-order structures resemble the symmetry of the underlying smaller unit. For example, DXbased tiles produce regular flat rectangular scaffolds (Figure 2B).76 One powerful way to increase the functionality of DNA tiles is based on the incorporation of chemically modified DNA strands. For example, thiol, biotin, or other chemical groups or bioligands can be placed at defined positions within the tiles, thereby opening up the possibility to bind protein receptors or gold particles to the nanotiles, as shown for a 3D doublecrossover motif containing three duplexes (Figure 2C). The DNA scaffolds thus function as templates to form nanoparticle arrays with defined nanoscale spacing.77,78 Similarly, 2D scaffolding served as templates for quantum dot arrays,79 lattices containing multiple different nanocomponents,80,81 and regular assemblies of proteins82−85 and DNA.36,76 Although these highly repetitive surface patterns can be up to hundreds of micrometers large,36,76 one challenge is to create alternate less-repetitive structures where nanoscale cargo is attached at tunable yet predefined positions. One strategy toward this aim has been developed by assembling a 4 × 4 tile

Figure 1. Films of DNA tetrahedra act as display agents to improve biomolecular recognition. (A) Molecular model of a DNA tetrahedron carrying disulfide groups via a carbon linker (red) at three vertices that bind to the gold surface to display the DNA strand at the top to the ambient environment.60 (B) DNA hybridization of two DNA strands, one labeled with a fluorophore, at the tip of DNA tetrahedra that are immobilized on gold rectangles. The size of the fluorescence microscopy image is 1 mm × 1 mm.60 (C) Gold-anchored DNA tetrahedra facilitate the cocaine-induced fusion of two-part anticocaine aptamers. This binding process is transduced to electrochemical signals via the specific binding of avidin−HRP conjugates to the biotin tag of one aptamer part. HRP catalyzes te electroreduction of hydrogen peroxide in the presence of an electroactive cosubstrate, TMB, to generate quantitative amperometric signals. The tetrahedra-based assay has a detection limit of 33 nM, which is 3 orders of magnitude lower than for a system where the aptamer parts are directly linked to the gold surface. Reprinted with permission from ref 62. B

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Figure 2. Nanopattering of surfaces with DNA nanoarchitectures. (A) DX motif interconnecting two DNA duplexes via two crossovers.28 (B) Twodimensional arrays of DX and DX + J tiles, which are labeled A and B*, respectively, and are held together by sticky ends, represented as geometrically complementary shapes at the tile termini. A DX − J tile features an additional duplex perpendicular to the DX duplexes, as indicated by a dot in the schematic drawing. The atomic force microscope (AFM) image shows stripes separated by ∼33 nm near the predicted distance of 32 nm.28 (C) Organizing gold nanoparticles with two different 3D double-crossover motifs containing 5 nm or 10 nm particles yielded a checkerboard nanoparticle array as shown by a transmission electron microscopy image.28,81 (D) Schematic drawing of DNA origami featuring a black scaffold strand and colored, shorter staple strands that stabilize the structure via crossovers.25 (E) Rigid rectangular DNA origami platform for the distancedependent binding of a bivalent protein. The platform spatially separates in rowlike fashion two aptamer-based receptors A and B (green and blue dots) by either 5.8 nm (A + B) or 20.7 nm (A and B). The two receptors recognize different parts of the same analyte. The thrombin analyte binds only to the more closely spaced apatamers as demonstrated by AFM topographic images (150 nm × 150 nm).88 (F) A DNA origami structure displays a centrally positioned photosensitizer (indium pyropheophorbide). It generates singlet oxygen, which can cleave up to four linker molecules (red rounded rectangle) carrying terminal biotin moieties (blue triangle). For reference purposes, one biotin tag is attached without a cleavable linker. Streptavidin binding and AFM read-out determine the integrity of the cleavable biotin linkers.89 (G) Decoration of an origami structure with chemical and bioaffinity groups for the site-specific coupling of cognate proteins. The orthogonal decoration was achieved by the stepwise addition of the different proteins (not shown) and AFM characterization of the target face.93 (H) A “superorigami” structure was assembled by binding regular DNA origami (blue) into a loose frame (red), which is assembled in origami fashion.99 (I) Programmed self-assembly of DNA jigsaw pieces carrying the letters “DNA”.100 Illustrations A, B, D, and F are reproduced with permission from refs 28, 28, 25, and 89, respectively, and illustrations C, E, G, H, and I have been adapted with permission from refs 28, 88, 93, 99 and 100, respectively.

replacing one or more staples with strands carrying the additional module. Unlike DNA tiles, the positions of these groups on DNA origami can be unique and do not have to be repeated over the nanopattern. One class of DNA origami structures that are very suitable for the nanofunctionalization of interfaces comprises flat rectangles or other planar geometric shapes (Figure 2E). These flat structures can be considered to be nanoscale pegboards onto which any molecule or moiety can be placed at any position. The power of this rational design approach has been demonstrated in several studies. For example, two molecular recognition motifs composed of DNA aptamers were positioned on a flat DNA rectangle (Figure 2E).88 By varying the spacing between the two recognition motifs, it was

lattice in which each tile can be addressed individually as demonstrated by depositing single streptavidin molecules to represent different letters.86 Nevertheless, larger and more complex patterns with optional cargo cannot be easily generated with DNA tiles. Bottom-Up Patterning with DNA Origami. Several of the limitations of DNA tiles are addressed by DNA origami. These DNA nanostructures of up to 100 nm are formed by the assembly of at least one long scaffold strand and smaller oligonucleotide DNA staple strands (Figure 2D).25,29,87 In addition to the larger size, DNA origami can be made into unique 2D and 3D shapes that are not readily accessible by DNA tiles. Furthermore, DNA origami can be equipped at predefined sites with functional or chemical modules by C

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Figure 3. Nanopatterns generated by combining bottom-up DNA nanoarchitectures and physical top-down routes. (A) Generation of patterns of DNA triangles. (a) Synthesis scheme for DNA origami triangles and atomic force microscopy height image showing random deposition on mica. Scale bar, 100 nm. (b) Fabrication of DNA origami binding sites via photolithography. The inset highlights the differentiation of the background and features (background/features) for the trimethylsilyl (TMS) monolayer and diamondlike carbon (DLC) films. Silanol groups occur in oxidized areas of the TMS monolayers. Features etched into the DLC template layer are 0.5−1.5 nm deep. DNA triangles can bind into the templated layer featuring complementary-shaped binding sites as illustrated by the AFM height image (right) of DNA triangles on 110 nm patterned triangle sites on a DLC/DLC surfaces.119 (B) Two-dimensional nanoparticle arrays are formed by binding DNA-coated nanocrystals (green with a golden core) onto the edges of DNA origami triangles via hybridization. The hybrid structures adsorb onto the electron-beam lithographically nanopatterned surface that features hydrophilic triangular binding sites (gray) surrounded by a hydrophobic coating (orange). AFM image of gold-nanoparticlefunctionalized origami triangles bound to top-down generated columns of equilateral triangles with sides of 100 nm, alternately oriented up and down. Scale bar, 500 nm.120 (C) Block-copolymer-patterned arrays of 5 nm gold nanoparticles (red) were connected with DNA origami (green). The connection was mediated by hybridization between the single-stranded DNA-thiol-modified gold nanoparticles and the sticky end-modified DNA origami.122 (D) Structures formed by connecting lithographically generated gold islands with DNA origami tubes: (a) triangle, (b) hexagon, (c) square, and (d) z shape. All scale bars are 300 nm. The DNA origami nanotubes of approximately 380 nm in length were composed of six DNA helices bundled with a hexagonal cross section and carried thiolated groups near their termini. The distance between the thiolated groups located near each end is approximately 320 nm.123 Illustrations A, C, and D are reprinted with permission from refs 119, 122, and 123, respectively, and illustration B has been adapted with permission from ref 120.

where a structural state is a function of information in the surroundings. Another type of device was implemented to mimic robotic behavior. In particular, DNA origami was used as a track to guide the movement of “molecular spiders” containing three DNA-made legs. The DNA origami tracks carried several signals that directed the molecular spider to perform start, follow, turn, and stop actions autonomously.95 The signals were spatially arranged DNA strands onto which the spider legs could hybridize to form duplexes. Directional movement of the spider was imparted by the enzyme-mediated cleavage of the duplexes’ signal strands to release the full-length spider legs. Other studies also exploited DNA platforms for robotic movement.34,96 DNA origami is also versatile with regard to the substrates onto which they can bind, as shown for gold, silicon, and graphene.97 Although DNA surface binding creates nanopattered substrates, it should be acknowledged that several DNA origami platforms can fulfill their function in suspension. Adsorption onto surfaces hence facilitates their readout with single-molecule techniques such as atomic force and

possible to probe the distance-dependent binding of bivalent analytes and shed light on the biophysics of this process.88 In another example, the physicochemical aspects of oxidation were studied by locating a photosensitizer and photocleavable moieties at specific positions on the flat DNA rectangle (Figure 2F).89 Light activation of the individual photosensitizer generated singlet oxygen, which led to the distance-dependent oxidation of organic moieties, as shown by atomic force microscopy.89 In addition to attaching DNA aptamers and small-molecule moieties, chemically tagged DNA origami platforms also enabled the point-specific immobilization of individual viral particles,90 gold nanoparticles,91 or different individual proteins29,92 resembling a nanoscale version of a smiling human face (Figure 2G).29,93 Other approaches are available to expand the range of functional roles of flat DNA origami. For example, DNA origami was used for a dynamic form of nanopattering94 whereby two independently programmed smaller DNA structures were captured as a function of the first bound element. This system represents simple DNA computation D

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fluorescence microscopy.98 In this respect, DNA origami rectangles are biocompatible platforms that match singlemolecule analysis on substrates and ensemble experiments in solution.98 Irrespective of surface attachment, a recurring question is how DNA origami can be arranged into larger lattices. Several approaches are available. These include the interlinking of several identical origami rectangles with sticky DNA ends and short complementary DNA oligonucleotides,90 or the use of large preformed DNA-based scaffold frames onto which smaller origami units can be assembled to form a superorigami structure (Figure 2H).99 Another creative route toward higher-order structures relies on rationally designed DNA jigsaw pieces that can assemble into a lattice based on the complementarity of their concave and convex shapes.100 In an extension of this work, each jigsaw piece was engineered to carry one letter within its topographic relief structure, enabling the writing of three-letter (Figure 2I) and five-letter words.100 Combining Bottom-Up DNA Nanoarchitectures with Physical Top-Down Nanopatterns. The alternative route to nanopatterned surfaces combines bottom-up DNA materials with a top-down nanofabrication approach. This combination is highly synergistic because the separate strategies cover two different length scales. Whereas the physical top-down approach can pattern microscale areas with feature sizes frequently down to 10−100 nm, the bottom-up approach can afford atomically precise DNA nanostructures of up to but not beyond overall dimensions of a few hundred nanometers. Furthermore, unlike physical nanopatterns, DNA nanostructures facilitate molecular recognition. Synergistically combining both strategies thus marries the best features of each route. Practically, this is achieved by decorating top-down-generated physical or chemical nanopatterned surfaces with structurally fine-tuned DNA nanoarchitectures. A wide range of top-down methods is available, including ebeam and UV lithography,101−105 nanoimprint lithography,106 nanocontact printing,107,108 dip-pen nanolithography,109−111 AFM-based nanografting,112 and direct deposition with a nanopipette113 or AFM cantilever.114 It is noted that these patterns may also be generated via bottom-up routes such as micelle,70,115 particle,68 and transfer nanolithography.116 A lot of work has been done by biofunctionalizing physical nanopatterns with conventional DNA strands, as described in a recent review,117 including 1D assemblies118 which are not covered here. Two prominent studies illustrate the benefits of decorating inorganic nanopatterns with 2D DNA nanostructures.119,120 In the first report, e-beam lithography and oxidative etching were applied to create DNA origami-shaped binding sites on technologically useful materials such as SiO2 and diamondlike carbon (Figure 3A).119 Complementarily shaped DNA origami was subsequently bound with high selectivity and good orientation to the preformed sites (Figure 3A). For example, 70−95% of sites had individual origami aligned in a defined orientation. These geometric sorting boards121 may be exploited to create nanoelectronic or nano-optical devices.119 In a related study, origami-decorated lithographic patterns were applied to create arrays of gold nanoparticles.120 The new defining feature of the patterns was that the surface-bound DNA origami carried gold nanoparticles at predefined nanoscale sites. Nanoparticles (10 nm each) with a DNA coat were attached via hybridization to the corners of a 80−120 nm DNA triangle (Figure 3B).120 The resulting nanometer-scale ordered nanoparticle arrays were unique because they could not have

been formed at similar throughput by lithography. The DNA nanoarchitectures thus bridged the two size regimes of the lithographically generated patterns and the 10 nm particles. Nanopatterns can be created via alternative routes by synergistically combining DNA origami with structured inorganic surface patterns. In one study, individual 5 nm gold nanoparticles within a regular assembly were connected with elongated DNA rectangles, resulting in a hybrid DNA− inorganic superstructure (Figure 3C).122 Using a related approach, smaller assemblies of a few gold islands were interconnected with DNA origami nanotubes (Figure 3D).123

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DNA INTERFACES AT SPHERICAL SUBSTRATES Another exciting area of DNA nanoarchitectonics is concerned with colloids and suspensions of nanoparticles. The nanobio interface at spherical substrates is of great interest because it provides several unique advantages and characteristics not available at flat substrates,37 such as the ability to self-assemble nanoparticles into complex 3D supramolecular arrays.117,124 Although most of the existing studies on the DNA-mediated assembly of nanoparticles have been performed using coatings composed of simple oligonucleotides, future work can exploit the existing knowledge and expand the area with DNA nanoarchitectonics. A great wealth of information is available about the physicochemical interactions at the interface of nanoscalecurved substrates.125 The surface modification is unique with regard to the immobilization of DNA strands. Curvature was found to increase the surface density of thiol-terminated singlestranded DNA by a factor of 130 when comparing 10 nm gold particles with flat gold surfaces.126 However, the higher density does not always translate into better hybridization efficiency because long tethered strands can bend back to reduce steric accessibility for the binding of targets.127 This can be avoided by using short duplex stems that increase the persistence length127 or by carefully controlling the number of immobilized oligonucleotides.128 DNA structures on nanoscale-curved substrates offer additional possibilities. DNA networks assembled on spherical gold nanoparticles can be isolated by dissolving the underlying inorganic template (Figure 4A). Because the hollow nucleic acid nanostructures are chemically cross-linked, they feature high nuclease resistance that is relevant to their application as antisense agent in cell biology.129 Alternatively, spherical DNA networks may themselves serve as templates to induce mineralization by CdS to form inorganic nanoshells.130 The DNA-mediated formation of nanoparticle assemblies is probably the most impressive area for exploiting the unique properties at the DNA−nanomaterial interface. The crystallization of nanoparticles was a breakthrough117,124 because the resulting lattice symmetry was programmable by carefully choosing the DNA sequences (Figure 4B).117 In an extension of this work, binary clusters could be formed with DNAmediated assembly whereby the plasmonic heteropentamer cluster was composed of a small gold sphere surrounded by a ring of four large spheres (Figure 4C). In addition to mediating the selective assembly of the clusters, the DNA coats functioned as an insulating spacer between the conductive nanoparticles.131 The DNA approach is furthermore applicable to creating hybrid lattices of protein-based capsid particles and gold nanoparticles.132 The crystallization was successful despite the different particle properties because surface modification adjusted the nanoparticles to similar effective radii. Similar to E

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CONCLUSIONS The use of DNA nanostructures at substrate interfaces has led to impressive feats as summarized in this Perspective. Where can DNA nanoarchitectonics continue to grow? One area is the increased exploitation of DNA origami for 3D lattices of nanoparticles. In the future, this might lead to the creation of photonic crystals with switchable collective properties139 that are controlled by DNA interparticle spacers of tunable distance.140 In more general terms, DNA nanostructures at interfaces could be integrated into functional devices whose properties can be actuated by external triggers.141 Indeed, the development of new devices can be guided by previous achievements142 using single- or double-stranded DNA where their conformation and molecular orientation was controlled by applying an electrical potential143,144 or adding effector cations.145 This helped to tune the DNA’s hybridization efficiency.146 Alternatively, the binding of complementary ssDNA to a layer of surface-tethered DNA strands created reversibly switchable nanocompartments.147 In the more biologically oriented disciplines, DNA could be used with other types of biomolecules such as lipid bilayers. Because DNA origami is biocompatible with biological cells in terms of recognition of membrane proteins148 and resistance to cellular lysates,149 an exciting prospect would be the use of DNA scaffolds as artificial cytoskeletons at free or supported lipid bilayer interfaces.150 The new structures could be used as model systems for new model systems for investigating membrane stability and curvature without inducing undesired DNA−lipid aggregates.151 An increasing trend in DNA nanotechnology is a focus on applications that ultimately lead to commercially viable products,152 which is compatible with some funding agencies’ call for greater economic benefit from scientific research. Although an emphasis on real-world applications is understandable, one should also consider that DNA nanoarchitectonics at interfaces is a relatively new research area compared to that of very established polymeric film coatings. Nevertheless, research activities are underway toward high added-value devices153 where the higher costs of DNA scaffolds are justified. In conclusion, DNA architectonics at interfaces is a highly interdisciplinary field that spans the nano- and microscale with numerous applications in materials and life science.

Figure 4. DNA coating of nanospheres leads to new structure and function. (A) Scheme illustrating the synthesis of hollow nucleic acid nanostructures from alkyne-modified thiolated DNA strands via crosslinking and dissolution of the gold nanoparticle template.129 (B) Gold nanoparticle−DNA conjugates can be programmed to assemble into different crystallographic arrangements by changing the sequence of the DNA linkers. A single-component assembly system (fcc) is obtained from gold nanoparticles coated with one DNA sequence, and a binary-component assembly system (bcc) results from gold nanoparticles with two different DNA linkers.117 (C) Assembly of DNA-functionalized nanoparticles into heteropentamer clusters, which consist of a smaller gold sphere surrounded by a ring of four larger spheres. Magnetic and Fano-like resonances are observed in individual clusters, indicating that DNA also functions as an insulating spacer between the conductive nanoparticles.131 Illustrations A and B are reprinted with permission from refs 129 and 117, respectively, and illustration C has been adapted with permission from ref 131.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Tel: 0044 20 7679 4702. Notes

The author declares no competing financial interest.

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ACKNOWLEDGMENTS This project was supported by the Leverhulme Trust (project RPG-170).

previous studies, the DNA linker could help tune the lattice symmetry.132 Finally, DNA-mediated 3D binary nanoparticle superlattices were formed on top-down-structured substrates aided by hybridization to DNA-coated surfaces,133 which is related to previous work on the DNA-guided positioning of particles.134,135 All of these studies can benefit from a deeper biophysical understanding of the hybridization of DNAmodified particles136,137 and the availability of innovative approaches to forming novel nanoparticles from nucleic acid analogues.138

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dx.doi.org/10.1021/la3045785 | Langmuir XXXX, XXX, XXX−XXX