3D DNA Origami Nanoparticles: From Basic Design Principles to Emerging Applications in Soft Matter and (Bio-)Nanosciences.

Scaffold-based lattice-engineered 3D DNA origami is a powerful and versatile technique for the rational design and build-up of arbitrarily structured and monodisperse DNA-based 3D nanoobjects. Relying on the unsurpassed molecular programmability of sequence-specific DNA hybridization, a long DNA single strand (termed scaffold) is assembled with many short single-stranded oligomers (termed staples), which organize the scaffold into a 3D lattice in a single step, thereby leading to 3D nanoparticulate structures of the highest precision in high yields. Applications of 3D DNA origami are increasingly wide-spread and interface with numerous fields of sciences, for example, anisometric or anisotropically functionalized nanoparticles, fundamental investigations of superstructure formation, biomedicine, (bio)physics, sensors, and optical materials. This Minireview discusses the fundamentals and recent advances from structure formation to selected applications, with a mission to promote cross-disciplinary exchange.

[1]  P. Rothemund,et al.  Programmable molecular recognition based on the geometry of DNA nanostructures. , 2011, Nature chemistry.

[2]  William M. Shih,et al.  Addressing the Instability of DNA Nanostructures in Tissue Culture , 2014, ACS nano.

[3]  David J. Mooney,et al.  Oligolysine-based coating protects DNA nanostructures from low-salt denaturation and nuclease degradation , 2017, Nature Communications.

[4]  Tim Liedl,et al.  DNA-Assembled Advanced Plasmonic Architectures. , 2018, Chemical reviews.

[5]  Veikko Linko,et al.  Cationic polymers for DNA origami coating - examining their binding efficiency and tuning the enzymatic reaction rates. , 2016, Nanoscale.

[6]  Adam T Woolley,et al.  Polymerase chain reaction based scaffold preparation for the production of thin, branched DNA origami nanostructures of arbitrary sizes. , 2009, Nano letters.

[7]  Hao Yan,et al.  Interenzyme substrate diffusion for an enzyme cascade organized on spatially addressable DNA nanostructures. , 2012, Journal of the American Chemical Society.

[8]  Hendrik Dietz,et al.  Gigadalton-scale shape-programmable DNA assemblies , 2017, Nature.

[9]  H. Leonhardt,et al.  Universelles Superauflösungs‐Multiplexing durch DNA‐Austausch , 2017 .

[10]  Andreas Walther,et al.  Materials learning from life: concepts for active, adaptive and autonomous molecular systems. , 2017, Chemical Society reviews.

[11]  Hai-Jun Su,et al.  Mechanical design of DNA nanostructures. , 2015, Nanoscale.

[12]  Jejoong Yoo,et al.  Large-Conductance Transmembrane Porin Made from DNA Origami , 2016, ACS nano.

[13]  S. Howorka,et al.  Self-assembled DNA nanopores that span lipid bilayers. , 2013, Nano letters.

[14]  P. Tinnefeld,et al.  Broadband Fluorescence Enhancement with Self-Assembled Silver Nanoparticle Optical Antennas. , 2017, ACS nano.

[15]  Nicholas A W Bell,et al.  DNA origami nanopores. , 2012, Nano letters.

[16]  P. Tinnefeld,et al.  DNA origami–based standards for quantitative fluorescence microscopy , 2014, Nature Protocols.

[17]  Tao Zhang,et al.  Hierarchical assembly of metal nanoparticles, quantum dots and organic dyes using DNA origami scaffolds. , 2013, Nature nanotechnology.

[18]  Johannes B. Woehrstein,et al.  Multiplexed 3D Cellular Super-Resolution Imaging with DNA-PAINT and Exchange-PAINT , 2014, Nature Methods.

[19]  Johannes B. Woehrstein,et al.  Polyhedra Self-Assembled from DNA Tripods and Characterized with 3D DNA-PAINT , 2014, Science.

[20]  Na Liu,et al.  Selective control of reconfigurable chiral plasmonic metamolecules , 2017, Science Advances.

[21]  Tomoko Emura,et al.  Supporting Information Single-Molecule Observation of the Photoregulated Conformational Dynamics of DNAOrigami Nanoscissors , 2017 .

[22]  William M. Shih,et al.  A 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron , 2004, Nature.

[23]  N. Seeman DNA in a material world , 2003, Nature.

[24]  H. Dietz,et al.  Dynamic DNA devices and assemblies formed by shape-complementary, non–base pairing 3D components , 2015, Science.

[25]  E. Kool,et al.  Hydrogen bonding, base stacking, and steric effects in dna replication. , 2001, Annual review of biophysics and biomolecular structure.

[26]  T. G. Martin,et al.  Synthetic Lipid Membrane Channels Formed by Designed DNA Nanostructures , 2012, Science.

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

[28]  Tim Liedl,et al.  Single-molecule FRET ruler based on rigid DNA origami blocks. , 2011, Chemphyschem : a European journal of chemical physics and physical chemistry.

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

[30]  Hélder A Santos,et al.  Cellular delivery of enzyme-loaded DNA origami. , 2016, Chemical communications.

[31]  Antti-Pekka Eskelinen,et al.  Virus-encapsulated DNA origami nanostructures for cellular delivery. , 2014, Nano letters.

[32]  Hao Yan,et al.  Dna Origami: a History and Current Perspective This Review Comes from a Themed Issue on Nanotechnology and Miniaturization Edited Structural Development Assembly Approaches Single-molecule Detection Material Organization , 2022 .

[33]  Shawn M. Douglas,et al.  DNA-nanotube-induced alignment of membrane proteins for NMR structure determination , 2007, Proceedings of the National Academy of Sciences.

[34]  Na Liu,et al.  A plasmonic nanorod that walks on DNA origami , 2015, Nature Communications.

[35]  Luvena L. Ong,et al.  Three-Dimensional Structures Self-Assembled from DNA Bricks , 2012, Science.

[36]  Hierarchische Selbstassemblierung dreidimensional gedruckter Schlüssel/Schloss‐Kolloide durch Formerkennung , 2016 .

[37]  Hao Yan,et al.  Complex wireframe DNA origami nanostructures with multi-arm junction vertices. , 2015, Nature nanotechnology.

[38]  M. Bathe,et al.  Quantitative prediction of 3D solution shape and flexibility of nucleic acid nanostructures , 2011, Nucleic acids research.

[39]  Björn Högberg,et al.  Purification of functionalized DNA origami nanostructures. , 2015, ACS nano.

[40]  Wesley P. Wong,et al.  Protocol for sortase-mediated construction of DNA-protein hybrids and functional nanostructures. , 2014, Methods.

[41]  S. Howorka,et al.  A biomimetic DNA-based channel for the ligand-controlled transport of charged molecular cargo across a biological membrane. , 2016, Nature nanotechnology.

[42]  Shawn M. Douglas,et al.  Multilayer DNA origami packed on a square lattice. , 2009, Journal of the American Chemical Society.

[43]  Zhao Zhang,et al.  Placing and shaping liposomes with reconfigurable DNA nanocages. , 2017, Nature chemistry.

[44]  Nicholas A. W. Bell,et al.  Nanopores formed by DNA origami: A review , 2014, FEBS letters.

[45]  Joachim Müller,et al.  Cascades in Compartments: En Route to Machine-Assisted Biotechnology. , 2017, Angewandte Chemie.

[46]  Hao Yan,et al.  Single-stranded DNA and RNA origami , 2017, Science.

[47]  Dongsheng Liu,et al.  Folding DNA into a Lipid-Conjugated Nanobarrel for Controlled Reconstitution of Membrane Proteins. , 2018, Angewandte Chemie.

[48]  Zhao Zhang,et al.  DNA Origami Rotaxanes: Tailored Synthesis and Controlled Structure Switching. , 2016, Angewandte Chemie.

[49]  Tim Liedl,et al.  DNA Origami Seesaws as Comparative Binding Assay , 2016, Chembiochem : a European journal of chemical biology.

[50]  T. G. Martin,et al.  Facile and Scalable Preparation of Pure and Dense DNA Origami Solutions** , 2014, Angewandte Chemie.

[51]  Hendrik Dietz,et al.  Efficient Production of Single-Stranded Phage DNA as Scaffolds for DNA Origami , 2015, Nano letters.

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

[53]  N. Seeman,et al.  Construction of a DNA-Truncated Octahedron , 1994 .

[54]  Almogit Abu-Horowitz,et al.  Universal computing by DNA origami robots in a living animal , 2014, Nature nanotechnology.

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

[56]  Mark Bathe,et al.  Programming Self-Assembly of DNA Origami Honeycomb Two-Dimensional Lattices and Plasmonic Metamaterials. , 2016, Journal of the American Chemical Society.

[57]  Wolfgang Fritzsche,et al.  Isothermal DNA origami folding: avoiding denaturing conditions for one-pot, hybrid-component annealing. , 2015, Nanoscale.

[58]  G. Seelig,et al.  Dynamic DNA nanotechnology using strand-displacement reactions. , 2011, Nature chemistry.

[59]  Tim Liedl,et al.  Molecular force spectroscopy with a DNA origami–based nanoscopic force clamp , 2016, Science.

[60]  J. Kjems,et al.  DNA nanovehicles and the biological barriers. , 2016, Advanced drug delivery reviews.

[61]  N. Seeman,et al.  Exponential growth and selection in self-replicating materials from DNA origami rafts. , 2017, Nature materials.

[62]  Hendrik Dietz,et al.  Magnesium-free self-assembly of multi-layer DNA objects , 2012, Nature Communications.

[63]  Hendrik Dietz,et al.  Biotechnological mass production of DNA origami , 2017, Nature.

[64]  Shawn M. Douglas,et al.  A Logic-Gated Nanorobot for Targeted Transport of Molecular Payloads , 2012, Science.

[65]  Cai‐Feng Wang,et al.  Versatile Bifunctional Magnetic‐Fluorescent Responsive Janus Supraballs Towards the Flexible Bead Display , 2011, Advanced materials.

[66]  Peng Yin,et al.  Universal Super-Resolution Multiplexing by DNA Exchange. , 2017, Angewandte Chemie.

[67]  F. Besenbacher,et al.  Self-assembly of DNA origami and single-stranded tile structures at room temperature. , 2013, Angewandte Chemie.

[68]  Philip Tinnefeld,et al.  Fluorescence and super-resolution standards based on DNA origami , 2012, Nature Methods.

[69]  Hao Yan,et al.  Multi-enzyme complexes on DNA scaffolds capable of substrate channelling with an artificial swinging arm. , 2014, Nature nanotechnology.

[70]  Hai-Jun Su,et al.  Programmable motion of DNA origami mechanisms , 2015, Proceedings of the National Academy of Sciences.

[71]  Hendrik Dietz,et al.  Exploring Nucleosome Unwrapping Using DNA Origami. , 2016, Nano letters.

[72]  A. Turberfield,et al.  Guiding the folding pathway of DNA origami , 2015, Nature.

[73]  Tanmay A M Bharat,et al.  Design of a molecular support for cryo-EM structure determination , 2016, Proceedings of the National Academy of Sciences.

[74]  E. Greene,et al.  DNA Dynamics and Single-Molecule Biology , 2014, Chemical reviews.

[75]  Philip Tinnefeld,et al.  DNA Origami Nanoantennas with over 5000-fold Fluorescence Enhancement and Single-Molecule Detection at 25 μM. , 2015, Nano letters.

[76]  Hao Yan,et al.  Assembly of multienzyme complexes on DNA nanostructures , 2016, Nature Protocols.

[77]  M. Zacharias,et al.  Single-molecule dissection of stacking forces in DNA , 2016, Science.

[78]  Pascal Lill,et al.  Hierarchical Assembly of DNA Filaments with Designer Elastic Properties. , 2017, ACS nano.

[79]  Yonggang Ke,et al.  Two design strategies for enhancement of multilayer-DNA-origami folding: underwinding for specific intercalator rescue and staple-break positioning. , 2012, Chemical science.

[80]  M. Rief,et al.  Rigid DNA Beams for High-Resolution Single-Molecule Mechanics** , 2013, Angewandte Chemie.

[81]  Na Liu,et al.  Optically Resolving the Dynamic Walking of a Plasmonic Walker Couple. , 2015, Nano letters.

[82]  Na Liu,et al.  A light-driven three-dimensional plasmonic nanosystem that translates molecular motion into reversible chiroptical function , 2016, Nature Communications.

[83]  N. Seeman,et al.  Synthesis from DNA of a molecule with the connectivity of a cube , 1991, Nature.

[84]  Hierarchical Self-Assembly of 3D-Printed Lock-and-Key Colloids through Shape Recognition. , 2016, Angewandte Chemie.

[85]  Stefan Howorka,et al.  Building membrane nanopores. , 2017, Nature nanotechnology.

[86]  Hendrik Dietz,et al.  Nanoscale rotary apparatus formed from tight-fitting 3D DNA components , 2016, Science Advances.

[87]  J. Chao,et al.  Folding super-sized DNA origami with scaffold strands from long-range PCR. , 2012, Chemical communications.

[88]  Shawn M. Douglas,et al.  Folding DNA into Twisted and Curved Nanoscale Shapes , 2009, Science.

[89]  Daniel G. Anderson,et al.  Molecularly Self-Assembled Nucleic Acid Nanoparticles for Targeted In Vivo siRNA Delivery , 2012, Nature nanotechnology.

[90]  Kersten S. Rabe,et al.  Kaskaden in Kompartimenten: auf dem Weg zu maschinengestützter Biotechnologie , 2017 .

[91]  Richard A. Muscat,et al.  DNA nanotechnology from the test tube to the cell. , 2015, Nature nanotechnology.

[92]  Vivek V. Thacker,et al.  Lipid-Bilayer-Spanning DNA Nanopores with a Bifunctional Porphyrin Anchor , 2013, Angewandte Chemie.

[93]  Luvena L. Ong,et al.  DNA Brick Crystals with Prescribed Depth , 2014, Nature chemistry.

[94]  Hendrik Dietz,et al.  How We Make DNA Origami , 2017, Chembiochem : a European journal of chemical biology.

[95]  K. Gothelf,et al.  Multilayer DNA origami packed on hexagonal and hybrid lattices. , 2012, Journal of the American Chemical Society.

[96]  F. Simmel,et al.  DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response , 2011, Nature.

[97]  Andreas Walther,et al.  3D DNA Origami Cuboids as Monodisperse Patchy Nanoparticles for Switchable Hierarchical Self-Assembly. , 2016, Nano letters.

[98]  William M. Shih,et al.  Virus-Inspired Membrane Encapsulation of DNA Nanostructures To Achieve In Vivo Stability , 2014, ACS nano.

[99]  Björn Högberg,et al.  Enzymatic production of 'monoclonal stoichiometric' single-stranded DNA oligonucleotides , 2013, Nature Methods.

[100]  Ebbe Sloth Andersen,et al.  Control of enzyme reactions by a reconfigurable DNA nanovault , 2017, Nature Communications.

[101]  H. Dietz,et al.  Uncovering the forces between nucleosomes using DNA origami , 2016, Science Advances.

[102]  Tim Liedl,et al.  DNA-Assembled Nanoparticle Rings Exhibit Electric and Magnetic Resonances at Visible Frequencies , 2015, Nano letters.

[103]  Friedrich C Simmel,et al.  Long-range movement of large mechanically interlocked DNA nanostructures , 2016, Nature Communications.

[104]  Philipp C Nickels,et al.  DNA origami nanopillars as standards for three-dimensional superresolution microscopy. , 2013, Nano letters.

[105]  Matthew J. A. Wood,et al.  DNA cage delivery to mammalian cells. , 2011, ACS nano.

[106]  Shawn M. Douglas,et al.  Self-assembly of DNA into nanoscale three-dimensional shapes , 2009, Nature.

[107]  A. Turberfield,et al.  A DNA-fuelled molecular machine made of DNA , 2022 .

[108]  Victor Pan,et al.  The Beauty and Utility of DNA Origami , 2017 .

[109]  Philip Tinnefeld,et al.  Fluorescence Enhancement at Docking Sites of DNA-Directed Self-Assembled Nanoantennas , 2012, Science.

[110]  A. Kuzyk,et al.  Reconfigurable 3D plasmonic metamolecules. , 2014, Nature materials.

[111]  Tao Zhang,et al.  Chiral plasmonic DNA nanostructures with switchable circular dichroism , 2013, Nature Communications.

[112]  Fei Zhang,et al.  DNA Origami: Scaffolds for Creating Higher Order Structures. , 2017, Chemical reviews.

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

[114]  Carlos E Castro,et al.  Dynamic DNA Origami Device for Measuring Compressive Depletion Forces. , 2017, ACS nano.

[115]  Peng Yin,et al.  Submicrometre geometrically encoded fluorescent barcodes self-assembled from DNA. , 2012, Nature chemistry.

[116]  Hao Yan,et al.  A Three‐Enzyme Pathway with an Optimised Geometric Arrangement to Facilitate Substrate Transfer , 2016, Chembiochem : a European journal of chemical biology.

[117]  J. Wang,et al.  Helical repeat of DNA in solution. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[118]  N. Seeman Nucleic acid junctions and lattices. , 1982, Journal of theoretical biology.

[119]  Pekka Orponen,et al.  DNA rendering of polyhedral meshes at the nanoscale , 2015, Nature.

[120]  Friedrich C Simmel,et al.  Molecular transport through large-diameter DNA nanopores , 2016, Nature Communications.

[121]  Jin Zhu,et al.  DNA polygonal cavities with tunable shapes and sizes. , 2015, Chemical communications.

[122]  Ralf Seidel,et al.  Shape-controlled synthesis of gold nanostructures using DNA origami molds. , 2014, Nano letters.

[123]  Hao Yan,et al.  Nanocaged enzymes with enhanced catalytic activity and increased stability against protease digestion , 2016, Nature Communications.

[124]  T. G. Martin,et al.  Cryo-EM structure of a 3D DNA-origami object , 2012, Proceedings of the National Academy of Sciences.

[125]  Veikko Linko,et al.  A modular DNA origami-based enzyme cascade nanoreactor. , 2015, Chemical communications.

[126]  Tim Liedl,et al.  Quantitative Single-Molecule Surface-Enhanced Raman Scattering by Optothermal Tuning of DNA Origami-Assembled Plasmonic Nanoantennas. , 2016, ACS nano.

[127]  Stephan Barcikowski,et al.  Tailored protein encapsulation into a DNA host using geometrically organized supramolecular interactions , 2017, Nature Communications.

[128]  Chenxiang Lin,et al.  Recovery of intact DNA nanostructures after agarose gel–based separation , 2011, Nature Methods.

[129]  S. Glotzer,et al.  Anisotropy of building blocks and their assembly into complex structures. , 2007, Nature materials.

[130]  Hendrik Dietz,et al.  Molecular engineering of chiral colloidal liquid crystals using DNA origami. , 2017, Nature materials.