DNA nanoarchitectonics: assembled DNA at interfaces.

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.

[1]  Hao Yan,et al.  DNA nanotechnology: A cascade of activity. , 2009, Nature nanotechnology.

[2]  K. Hosokawa,et al.  Controlling the number and positions of oligonucleotides on gold nanoparticle surfaces. , 2009, Journal of the American Chemical Society.

[3]  S. Howorka,et al.  Painting with biomolecules at the nanoscale: biofunctionalization with tunable surface densities. , 2012, Nano letters.

[4]  B. Nordén,et al.  Soft-Surface DNA Nanotechnology: DNA Constructs Anchored and Aligned to Lipid Membrane** , 2011, Angewandte Chemie.

[5]  N. Seeman,et al.  DNA-Templated Self-Assembly of Metallic Nanocomponent Arrays on a Surface , 2004 .

[6]  Heinz Schmid,et al.  Siloxane Polymers for High-Resolution, High-Accuracy Soft Lithography , 2000 .

[7]  K. Qamhieh,et al.  Analytical model study of dendrimer/DNA complexes. , 2009, Biomacromolecules.

[8]  S. Lata,et al.  High-affinity adaptors for switchable recognition of histidine-tagged proteins. , 2005, Journal of the American Chemical Society.

[9]  Changyou Gao,et al.  Layer-by-layer assembly of microcapsules and their biomedical applications. , 2012, Chemical Society reviews.

[10]  M. Textor,et al.  Large area protein nanopatterning for biological applications. , 2006, Nano letters.

[11]  J. Kjems,et al.  Self-assembly of a nanoscale DNA box with a controllable lid , 2009, Nature.

[12]  Vincent M Rotello,et al.  Nano meets biology: structure and function at the nanoparticle interface. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[13]  Barbara Saccà,et al.  DNA origami: the art of folding DNA. , 2012, Angewandte Chemie.

[14]  A. Turberfield,et al.  Direct observation of stepwise movement of a synthetic molecular transporter. , 2011, Nature nanotechnology.

[15]  Katsuhiko Ariga,et al.  Two-dimensional nanoarchitectonics based on self-assembly. , 2010, Advances in colloid and interface science.

[16]  S. Howorka,et al.  Nanoscale DNA tetrahedra improve biomolecular recognition on patterned surfaces. , 2012, Small.

[17]  G. Braun,et al.  Cell-targeted self-assembled DNA nanostructures. , 2009, Journal of the American Chemical Society.

[18]  Hao Yan,et al.  DNA self-assembly for nanomedicine. , 2010, Advanced drug delivery reviews.

[19]  G. Danuser,et al.  A novel approach to produce biologically relevant chemical patterns at the nanometer scale: Selective molecular assembly patterning combined with colloidal lithography , 2002 .

[20]  Andrew J Turberfield,et al.  The single-step synthesis of a DNA tetrahedron. , 2004, Chemical communications.

[21]  Faisal A. Aldaye,et al.  Assembling Materials with DNA as the Guide , 2008, Science.

[22]  S. Howorka,et al.  Selective protein and DNA adsorption on PLL-PEG films modulated by ionic strength. , 2009 .

[23]  E. Winfree,et al.  Toward reliable algorithmic self-assembly of DNA tiles: a fixed-width cellular automaton pattern. , 2008, Nano letters.

[24]  Stefano Cabrini,et al.  DNA-directed self-assembly of gold nanoparticles onto nanopatterned surfaces: controlled placement of individual nanoparticles into regular arrays. , 2010, ACS nano.

[25]  J. Satulovsky,et al.  Kinetic and thermodynamic control of protein adsorption. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  M. Grunze,et al.  Preparation and characterization of self-assembled monolayers on indium tin oxide , 2000 .

[27]  D. Meldrum,et al.  Stability of DNA origami nanoarrays in cell lysate. , 2011, Nano letters.

[28]  M. Grunze,et al.  Modification of Alkanethiolate Monolayers by Low Energy Electron Irradiation: Dependence on the Substrate Material and on the Length and Isotopic Composition of the Alkyl Chains , 2000 .

[29]  Kemin Wang,et al.  Electrical switching of DNA monolayers investigated by surface plasmon resonance. , 2006, Langmuir : the ACS journal of surfaces and colloids.

[30]  Alexander W Peterson,et al.  Hybridization of mismatched or partially matched DNA at surfaces. , 2002, Journal of the American Chemical Society.

[31]  J. Hoh,et al.  Directed immobilization of protein-coated nanospheres to nanometer-scale patterns fabricated by electron beam lithography of poly(ethylene glycol) self-assembled monolayers. , 2006, Langmuir : the ACS journal of surfaces and colloids.

[32]  C. Mirkin,et al.  Polyvalent nucleic acid nanostructures. , 2011, Journal of the American Chemical Society.

[33]  Jonathan Bath,et al.  A DNA-based molecular motor that can navigate a network of tracks. , 2012, Nature nanotechnology.

[34]  Hao Yan,et al.  Toward reliable gold nanoparticle patterning on self-assembled DNA nanoscaffold. , 2008, Journal of the American Chemical Society.

[35]  Jennifer N Cha,et al.  Large-area spatially ordered arrays of gold nanoparticles directed by lithographically confined DNA origami. , 2010, Nature nanotechnology.

[36]  Hao Yan,et al.  Self-assembled peptide nanoarrays: an approach to studying protein-protein interactions. , 2007, Angewandte Chemie.

[37]  L. A. Baker,et al.  Nanopores: a makeover for membranes. , 2008, Nature nanotechnology.

[38]  E. Delamarche,et al.  Microfluidic Networks Made of Poly(dimethylsiloxane), Si, and Au Coated with Polyethylene Glycol for Patterning Proteins onto Surfaces , 2001 .

[39]  Chengde Mao,et al.  Reversibly switching the surface porosity of a DNA tetrahedron. , 2012, Journal of the American Chemical Society.

[40]  N. Seeman.  Nanomaterials based on DNA. , 2010, Annual review of biochemistry.

[41]  Jacob Piehler,et al.  Native protein nanolithography that can write, read and erase. , 2007, Nature nanotechnology.

[42]  F. Besenbacher,et al.  Control of self-assembled 2D nanostructures by methylation of guanine. , 2011, Small.

[43]  G. Zanchetta,et al.  DNA-Based Soft Phases , 2013 .

[44]  S. Howorka,et al.  Single-molecule AFM characterization of individual chemically tagged DNA tetrahedra. , 2011, ACS nano.

[45]  Hao Yan,et al.  Periodic square-like gold nanoparticle arrays templated by self-assembled 2D DNA Nanogrids on a surface. , 2006, Nano letters.

[46]  Adam T Woolley,et al.  Chemical alignment of DNA origami to block copolymer patterned arrays of 5 nm gold nanoparticles. , 2011, Nano letters.

[47]  Eileen M. Spain,et al.  Orienting DNA helices on gold using applied electric fields , 1998 .

[48]  V. Truskett,et al.  Trends in imprint lithography for biological applications. , 2006, Trends in biotechnology.

[49]  Joseph D. Andrade,et al.  Protein—surface interactions in the presence of polyethylene oxide , 1991 .

[50]  Hao Yan,et al.  Interconnecting gold islands with DNA origami nanotubes. , 2010, Nano letters.

[51]  Hao Yan,et al.  Charge transport within a three-dimensional DNA nanostructure framework. , 2012, Journal of the American Chemical Society.

[52]  Shana O Kelley,et al.  One-step DNA-programmed growth of luminescent and biofunctionalized nanocrystals. , 2009, Nature nanotechnology.

[53]  Itamar Willner,et al.  Enzyme cascades activated on topologically programmed DNA scaffolds. , 2009, Nature nanotechnology.

[54]  Hao Yan,et al.  Spatially addressable multiprotein nanoarrays templated by aptamer-tagged DNA nanoarchitectures. , 2007, Journal of the American Chemical Society.

[55]  Lei Zhu,et al.  Conformation transformation determined by different self-assembled phases in a DNA complex with cationic polyhedral oligomeric silsesquioxane lipid. , 2008, ACS nano.

[56]  Matthew B. Johnson,et al.  Fabrication of protein dot arrays via particle lithography. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[57]  R. Stutz,et al.  Microcontact Printing Using Poly(dimethylsiloxane) Stamps Hydrophilized by Poly(ethylene oxide) Silanes , 2003 .

[58]  Gang-Yu Liu,et al.  Hybridization with nanostructures of single-stranded DNA. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[59]  Faisal A. Aldaye,et al.  Long-range assembly of DNA into nanofibers and highly ordered networks using a block copolymer approach. , 2010, Journal of the American Chemical Society.

[60]  Robert J Fisher,et al.  Heparin-regulated release of growth factors in vitro and angiogenic response in vivo to implanted hyaluronan hydrogels containing VEGF and bFGF. , 2006, Biomaterials.

[61]  Hao Yan,et al.  DNA origami: a history and current perspective. , 2010, Current opinion in chemical biology.

[62]  Federico Capasso,et al.  DNA-enabled self-assembly of plasmonic nanoclusters. , 2011, Nano letters.

[63]  Derek N. Woolfson,et al.  Rational design and application of responsive α-helical peptide hydrogels , 2009, Nature materials.

[64]  T. Xia,et al.  Understanding biophysicochemical interactions at the nano-bio interface. , 2009, Nature materials.

[65]  Philip Tinnefeld,et al.  DNA origami as biocompatible surface to match single-molecule and ensemble experiments , 2012, Nucleic acids research.

[66]  S. Howorka,et al.  Glass surfaces grafted with high-density poly(ethylene glycol) as substrates for DNA oligonucleotide microarrays. , 2006, Langmuir : the ACS journal of surfaces and colloids.

[67]  S. Tosatti,et al.  Enhanced bone apposition around biofunctionalized sandblasted and acid-etched titanium implant surfaces. A histomorphometric study in miniature pigs. , 2006, Clinical oral implants research.

[68]  Chunhai Fan,et al.  Regenerable electrochemical immunological sensing at DNA nanostructure-decorated gold surfaces. , 2011, Chemical communications.

[69]  Taolei Sun,et al.  Spatially controlled DNA nanopatterns by "click" chemistry using oligonucleotides with different anchoring sites. , 2010, Journal of the American Chemical Society.

[70]  M. Mikkola.  Controlling the Number of Tooth Rows , 2009, Science Signaling.

[71]  Stefan Howorka,et al.  Engineering and exploiting protein assemblies in synthetic biology. , 2009, Molecular bioSystems.

[72]  Xiang Zhang,et al.  Light-driven nanoscale plasmonic motors. , 2010, Nature nanotechnology.

[73]  P. Nealey,et al.  Localization of multiple DNA sequences on nanopatterns. , 2011, ACS nano.

[74]  G. Whitesides,et al.  Self-assembled monolayers of thiolates on metals as a form of nanotechnology. , 2005, Chemical reviews.

[75]  Wilhelm T. S. Huck,et al.  Nanocontact Printing: A Route to Sub-50-nm-Scale Chemical and Biological Patterning , 2003 .

[76]  Ryan J. Kershner,et al.  Placement and orientation of individual DNA shapes on lithographically patterned surfaces. , 2009, Nature nanotechnology.

[77]  K. Ariga,et al.  Thin-film-based nanoarchitectures for soft matter: controlled assemblies into two-dimensional worlds. , 2011, Small.

[78]  G. Scoles,et al.  Quantitative study of the effect of coverage on the hybridization efficiency of surface-bound DNA nanostructures. , 2008, Nano letters.

[79]  H. Sugiyama,et al.  Programmed-assembly system using DNA jigsaw pieces. , 2010, Chemistry.

[80]  W. Xu,et al.  Supramolecular porous network formed by molecular recognition between chemically modified nucleobases guanine and cytosine. , 2010, Angewandte Chemie.

[81]  Alberto Piqué,et al.  Functionalization of indium tin oxide. , 2006, Langmuir : the ACS journal of surfaces and colloids.

[82]  Hao Yan,et al.  Tiles for Label-Free RNA Hybridization Assays Self-Assembled Water-Soluble Nucleic Acid Probe , 2008 .

[83]  Matthias Franzreb,et al.  Multiplexed lipid dip-pen nanolithography on subcellular scales for the templating of functional proteins and cell culture. , 2008, Small.

[84]  A Paul Alivisatos,et al.  Two-dimensional nanoparticle arrays show the organizational power of robust DNA motifs. , 2006, Nano letters.

[85]  J. Reif,et al.  Finite-size, fully addressable DNA tile lattices formed by hierarchical assembly procedures. , 2006, Angewandte Chemie.

[86]  Jennifer E. Padilla,et al.  Nanohedra: Using symmetry to design self assembling protein cages, layers, crystals, and filaments , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Joseph D. Andrade,et al.  Protein—surface interactions in the presence of polyethylene oxide: II. Effect of protein size , 1991 .

[88]  William A. Goddard,et al.  Starburst Dendrimers: Molecular‐Level Control of Size, Shape, Surface Chemistry, Topology, and Flexibility from Atoms to Macroscopic Matter , 1990 .

[89]  Kinam Park,et al.  Prevention of Protein Adsorption by Tethered Poly(ethylene oxide) Layers: Experiments and Single-Chain Mean-Field Analysis , 1998 .

[90]  Kurt V. Gothelf,et al.  Single molecule atomic force microscopy studies of photosensitized singlet oxygen behavior on a DNA origami template. , 2010, ACS nano.

[91]  Hao Yan,et al.  Organizing DNA origami tiles into larger structures using preformed scaffold frames. , 2011, Nano letters.

[92]  Hao Yan,et al.  Self-assembled DNA nanostructures for distance-dependent multivalent ligand-protein binding. , 2008, Nature nanotechnology.

[93]  G. Scoles,et al.  Control of steric hindrance on restriction enzyme reactions with surface-bound DNA nanostructures. , 2008, Nano letters.

[94]  Marya Lieberman,et al.  DNA origami nanopatterning on chemically modified graphene. , 2012, Angewandte Chemie.

[95]  Chengde Mao,et al.  Antibody Nanoarrays with a Pitch of ∼20 Nanometers , 2006 .

[96]  David Neff,et al.  NTA directed protein nanopatterning on DNA Origami nanoconstructs. , 2009, Journal of the American Chemical Society.

[97]  Youdong Mao,et al.  Reversibly switchable DNA nanocompartment on surfaces. , 2004, Nucleic acids research.

[98]  D. Grainger.  DNA nanotechnology: Geometric sorting boards. , 2009, Nature nanotechnology.

[99]  Chad A. Mirkin,et al.  Nanobiotechnology II: More Concepts and Applications , 2007 .

[100]  B. Liedberg,et al.  Protein-protein interactions in reversibly assembled nanopatterns. , 2008, Nano letters.

[101]  Kersten S. Rabe,et al.  Orthogonal protein decoration of DNA origami. , 2010, Angewandte Chemie.

[102]  H. Gaub,et al.  Single-Molecule Cut-and-Paste Surface Assembly , 2008, Science.

[103]  P. Rothemund.  Folding DNA to create nanoscale shapes and patterns , 2006, Nature.

[104]  I. Willner,et al.  Functional nucleic acid nanostructures and DNA machines. , 2010, Current opinion in biotechnology.

[105]  Hao Yan,et al.  Programmable DNA self-assemblies for nanoscale organization of ligands and proteins. , 2005, Nano letters.

[106]  Sung Yong Park,et al.  DNA-programmable nanoparticle crystallization , 2008, Nature.

[107]  Chad A. Mirkin,et al.  Nanobiotechnology :concepts, applications and perspectives , 2005 .

[108]  Minghui Liu,et al.  Spatially-interactive biomolecular networks organized by nucleic acid nanostructures. , 2012, Accounts of chemical research.

[109]  J. Wiedenmann,et al.  Polyelectrolyte-mediated protein adsorption: fluorescent protein binding to individual polyelectrolyte nanospheres. , 2005, The journal of physical chemistry. B.

[110]  Karin Musier-Forsyth,et al.  Sequence-encoded self-assembly of multiple-nanocomponent arrays by 2D DNA scaffolding. , 2005, Nano letters.

[111]  Martin R. Willis,et al.  Organic electroluminescent devices: enhanced carrier injection using SAM derivatized ITO electrodes , 2000 .

[112]  Jie Chao,et al.  Dynamic Patterning Programmed by DNA Tiles Captured on a DNA Origami Substrate , 2009, Nature nanotechnology.

[113]  Ilker S. Bayer,et al.  Advances in top-down and bottom-up surface nanofabrication: techniques, applications & future prospects. , 2012, Advances in colloid and interface science.

[114]  S. Howorka,et al.  Nanopatterning of biomolecules with microscale beads. , 2005, Chemphyschem : a European journal of chemical physics and physical chemistry.

[115]  K. Christman,et al.  Nanopatterning proteins and peptides. , 2006, Soft matter.

[116]  Russell P. Goodman,et al.  Rapid Chiral Assembly of Rigid DNA Building Blocks for Molecular Nanofabrication , 2005, Science.

[117]  Chunhai Fan,et al.  DNA nanostructure-decorated surfaces for enhanced aptamer-target binding and electrochemical cocaine sensors. , 2011, Analytical chemistry.

[118]  J. Preece,et al.  Bio-nanopatterning of Surfaces , 2007, Nanoscale research letters.

[119]  Sung Yong Park,et al.  DNA-controlled assembly of a NaTl lattice structure from gold nanoparticles and protein nanoparticles. , 2010, Nature materials.

[120]  Liming Ying,et al.  Writing with DNA and protein using a nanopipet for controlled delivery. , 2002, Journal of the American Chemical Society.

[121]  Russell P. Goodman,et al.  Reconfigurable, braced, three-dimensional DNA nanostructures. , 2008, Nature nanotechnology.

[122]  B. Grzybowski,et al.  Controlling the properties of self-assembled monolayers by substrate curvature. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[123]  D. Sholl,et al.  Chiral selection on inorganic crystalline surfaces , 2003, Nature materials.

[124]  Hyunwoo Noh,et al.  Surface-driven DNA assembly of binary cubic 3D nanocrystal superlattices. , 2011, Small.

[125]  C. Pradier,et al.  Grafting of lysozyme and/or poly(ethylene glycol) to prevent biofilm growth on stainless steel surfaces. , 2009, The journal of physical chemistry. B.

[126]  Joachim P Spatz,et al.  Impact of order and disorder in RGD nanopatterns on cell adhesion. , 2009, Nano letters.

[127]  Chad A Mirkin,et al.  The evolution of dip-pen nanolithography. , 2004, Angewandte Chemie.

[128]  T. Lindahl,et al.  Rate of depurination of native deoxyribonucleic acid. , 1972, Biochemistry.

[129]  Dongsheng Liu,et al.  An electrochemically actuated reversible DNA switch. , 2010, Nano letters.

[130]  Erik Winfree,et al.  Molecular robots guided by prescriptive landscapes , 2010, Nature.

[131]  Francis C Szoka,et al.  Designing dendrimers for biological applications , 2005, Nature Biotechnology.

[132]  A. Zinchenko,et al.  DNA-assisted "double-templating" approach for the construction of hollow meshed inorganic nanoshells. , 2011, Langmuir : the ACS journal of surfaces and colloids.

[133]  Adam H. Marblestone,et al.  Rapid prototyping of 3D DNA-origami shapes with caDNAno , 2009, Nucleic acids research.

[134]  S. Howorka,et al.  Semipermeable poly(ethylene glycol) films: the relationship between permeability and molecular structure of polymer chains , 2009 .

[135]  J. Cha,et al.  Recent advances in DNA-based directed assembly on surfaces. , 2010, Nanoscale.

[136]  P. Messersmith,et al.  The present and future of biologically inspired adhesive interfaces and materials. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[137]  George C Schatz,et al.  Tailoring DNA structure to increase target hybridization kinetics on surfaces. , 2010, Journal of the American Chemical Society.

[138]  S. Howorka.  Rationally engineering natural protein assemblies in nanobiotechnology. , 2011, Current opinion in biotechnology.

[139]  Joachim P. Spatz,et al.  Micellar Inorganic–Polymer Hybrid Systems—A Tool for Nanolithography , 1999 .

[140]  U. Rant,et al.  Conformations of end-tethered DNA molecules on gold surfaces: influences of applied electric potential, electrolyte screening, and temperature. , 2010, Journal of the American Chemical Society.

[141]  J. Lahann,et al.  Stimuli-responsive monolayers for biotechnology , 2010 .

[142]  Hao Yan,et al.  Immobilization and one-dimensional arrangement of virus capsids with nanoscale precision using DNA origami. , 2010, Nano letters.

[143]  J. Crocker,et al.  Probing interfacial equilibration in microsphere crystals formed by DNA-directed assembly. , 2009, Nature materials.

[144]  C. Hunter,et al.  Site-specific immobilization and micrometer and nanometer scale photopatterning of yellow fluorescent protein on glass surfaces. , 2009, Journal of the American Chemical Society.

[145]  Hao Yan,et al.  DNA-tile-directed self-assembly of quantum dots into two-dimensional nanopatterns. , 2008, Angewandte Chemie.

[146]  A DNA nanostructure for the functional assembly of chemical groups with tunable stoichiometry and defined nanoscale geometry. , 2009, Angewandte Chemie.

[147]  Hua-Zhong Yu,et al.  A robust electronic switch made of immobilized duplex/quadruplex DNA. , 2010, Angewandte Chemie.

[148]  B. Pettitt,et al.  Accurate prediction of binding thermodynamics for DNA on surfaces. , 2011, The journal of physical chemistry. B.

[149]  D. Lelie,et al.  DNA-guided crystallization of colloidal nanoparticles , 2008, Nature.

[150]  Thomas Tørring,et al.  DNA origami: a quantum leap for self-assembly of complex structures. , 2011, Chemical Society reviews.