Dynamic DNA Origami Devices: from Strand-Displacement Reactions to External-Stimuli Responsive Systems

DNA nanotechnology provides an excellent foundation for diverse nanoscale structures that can be used in various bioapplications and materials research. Among all existing DNA assembly techniques, DNA origami proves to be the most robust one for creating custom nanoshapes. Since its invention in 2006, building from the bottom up using DNA advanced drastically, and therefore, more and more complex DNA-based systems became accessible. So far, the vast majority of the demonstrated DNA origami frameworks are static by nature; however, there also exist dynamic DNA origami devices that are increasingly coming into view. In this review, we discuss DNA origami nanostructures that exhibit controlled translational or rotational movement when triggered by predefined DNA sequences, various molecular interactions, and/or external stimuli such as light, pH, temperature, and electromagnetic fields. The rapid evolution of such dynamic DNA origami tools will undoubtedly have a significant impact on molecular-scale precision measurements, targeted drug delivery and diagnostics; however, they can also play a role in the development of optical/plasmonic sensors, nanophotonic devices, and nanorobotics for numerous different tasks.

[1]  Jejoong Yoo,et al.  De novo reconstruction of DNA origami structures through atomistic molecular dynamics simulation , 2016, Nucleic acids research.

[2]  Toma E Tomov,et al.  DNA bipedal motor walking dynamics: an experimental and theoretical study of the dependency on step size , 2017, Nucleic acids research.

[3]  H. Su,et al.  DNA origami compliant nanostructures with tunable mechanical properties. , 2014, ACS nano.

[4]  N. Seeman,et al.  Programmable materials and the nature of the DNA bond , 2015, Science.

[5]  Veikko Linko,et al.  DNA nanostructure-directed assembly of metal nanoparticle superlattices , 2018, Journal of Nanoparticle Research.

[6]  Jing Pan,et al.  Recent progress on DNA based walkers. , 2015, Current opinion in biotechnology.

[7]  Nadrian C Seeman,et al.  RNA used to control a DNA rotary nanomachine. , 2006, Nano letters.

[8]  Noa Agmon,et al.  Molecular Robots Obeying Asimov's Three Laws of Robotics , 2017, Artificial Life.

[9]  Bernard Yurke,et al.  Dielectrophoretic trapping of DNA origami. , 2008, Small.

[10]  Veikko Linko,et al.  On the Stability of DNA Origami Nanostructures in Low-Magnesium Buffers. , 2018, Angewandte Chemie.

[11]  H. Sugiyama,et al.  Lipid-bilayer-assisted two-dimensional self-assembly of DNA origami nanostructures , 2015, Nature Communications.

[12]  Veikko Linko,et al.  DNA Nanostructures as Smart Drug-Delivery Vehicles and Molecular Devices. , 2015, Trends in biotechnology.

[13]  Veikko Linko,et al.  DNA-Based Enzyme Reactors and Systems , 2016, Nanomaterials.

[14]  D. Baker,et al.  The coming of age of de novo protein design , 2016, Nature.

[15]  Jenny V Le,et al.  Probing Nucleosome Stability with a DNA Origami Nanocaliper. , 2016, ACS nano.

[16]  Lulu Qian,et al.  Fractal assembly of micrometre-scale DNA origami arrays with arbitrary patterns , 2017, Nature.

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

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

[19]  M. Komiyama,et al.  Nanomechanical DNA origami 'single-molecule beacons' directly imaged by atomic force microscopy , 2011, Nature communications.

[20]  Jeremy J. Baumberg,et al.  Thermo‐Responsive Actuation of a DNA Origami Flexor , 2018 .

[21]  H. Dietz,et al.  Placing molecules with Bohr radius resolution using DNA origami. , 2016, Nature nanotechnology.

[22]  Wei Li,et al.  A cargo-sorting DNA robot , 2017, Science.

[23]  N. Seeman,et al.  A nanomechanical device based on the B–Z transition of DNA , 1999, Nature.

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

[25]  Michael Matthies,et al.  Structural Transformation of Wireframe DNA Origami via DNA Polymerase Assisted Gap-Filling. , 2018, ACS nano.

[26]  Mette D. E. Jepsen,et al.  Construction of a 4 zeptoliters switchable 3D DNA box origami. , 2012, ACS nano.

[27]  Samara L. Reck-Peterson,et al.  Tug-of-War in Motor Protein Ensembles Revealed with a Programmable DNA Origami Scaffold , 2012, Science.

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

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

[30]  Victoria Birkedal,et al.  Multifluorophore DNA Origami Beacon as a Biosensing Platform. , 2018, ACS nano.

[31]  Veikko Linko,et al.  Automated design of DNA origami , 2016, Nature Biotechnology.

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

[33]  Casey Grun,et al.  Programmable self-assembly of three-dimensional nanostructures from 104 unique components , 2017, Nature.

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

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

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

[37]  Mark Bathe,et al.  DNA Nanotechnology: A foundation for Programmable Nanoscale Materials , 2017 .

[38]  Carlos E Castro,et al.  Real-time magnetic actuation of DNA nanodevices via modular integration with stiff micro-levers , 2018, Nature Communications.

[39]  Bernard Yurke,et al.  A DNA-based molecular device switchable between three distinct mechanical states , 2002 .

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

[41]  Tim Liedl,et al.  3D DNA Origami Crystals. , 2018, Advanced materials.

[42]  Veikko Linko,et al.  Evolution of Structural DNA Nanotechnology , 2018, Advanced materials.

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

[44]  F. Crick,et al.  Molecular Structure of Nucleic Acids: A Structure for Deoxyribose Nucleic Acid , 1953, Nature.

[45]  Mark Bathe,et al.  A primer to scaffolded DNA origami , 2011, Nature Methods.

[46]  Kurt V. Gothelf,et al.  Chemical modifications and reactions in DNA nanostructures , 2017 .

[47]  Hao Yan,et al.  DNA Origami with Complex Curvatures in Three-Dimensional Space , 2011, Science.

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

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

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

[51]  Hyunung Lee,et al.  A Reconfigurable DNA Accordion Rack. , 2018, Angewandte Chemie.

[52]  Veikko Linko,et al.  Plasmonic nanostructures through DNA-assisted lithography , 2018, Science Advances.

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

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

[55]  Carlos E. Castro,et al.  DNA origami devices for molecular-scale precision measurements , 2017 .

[56]  Baoquan Ding,et al.  A DNA nanorobot functions as a cancer therapeutic in response to a molecular trigger in vivo , 2018, Nature Biotechnology.

[57]  Xue Han,et al.  Light sensitization of DNA nanostructures via incorporation of photo-cleavable spacers. , 2015, Chemical communications.

[58]  W. Chiu,et al.  Designer nanoscale DNA assemblies programmed from the top down , 2016, Science.

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

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

[61]  F. Crick,et al.  Molecular structure of nucleic acids , 2004, JAMA.

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

[63]  Cheng Zhu,et al.  Programmable Multivalent DNA-Origami Tension Probes for Reporting Cellular Traction Forces. , 2018, Nano letters.

[64]  Hao Yan,et al.  A DNA tweezer-actuated enzyme nanoreactor , 2013, Nature Communications.

[65]  V. Linko,et al.  The enabled state of DNA nanotechnology. , 2013, Current opinion in biotechnology.

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

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

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

[69]  Jing Pan,et al.  Dynamic and Progressive Control of DNA Origami Conformation by Modulating DNA Helicity with Chemical Adducts. , 2016, ACS nano.

[70]  Yamuna Krishnan,et al.  Designing DNA nanodevices for compatibility with the immune system of higher organisms. , 2015, Nature nanotechnology.

[71]  Dongsheng Liu,et al.  Regulation of an enzyme cascade reaction by a DNA machine. , 2013, Small.

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

[73]  Keiichi Namba,et al.  Photoresponsive DNA nanocapsule having an open/close system for capture and release of nanomaterials. , 2014, Chemistry.

[74]  Friedrich C. Simmel,et al.  Membrane-Assisted Growth of DNA Origami Nanostructure Arrays , 2015, ACS nano.

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

[76]  Flavio Romano,et al.  Characterizing the Motion of Jointed DNA Nanostructures Using a Coarse-Grained Model. , 2017, ACS nano.

[77]  A. Turberfield,et al.  DNA nanomachines. , 2007, Nature nanotechnology.

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

[79]  Michael Matthies,et al.  Block Copolymer Micellization as a Protection Strategy for DNA Origami. , 2017, Angewandte Chemie.

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

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

[82]  Moon Ki Kim,et al.  Fabrication and Characterization of Finite-Size DNA 2D Ring and 3D Buckyball Structures , 2018, International journal of molecular sciences.

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

[84]  Barbara Saccà,et al.  Enzyme-functionalized DNA nanostructures as tools for organizing and controlling enzymatic reactions , 2017 .

[85]  Maximilian T. Strauss,et al.  Multiplexed 3D super-resolution imaging of whole cells using spinning disk confocal microscopy and DNA-PAINT , 2017, Nature Communications.

[86]  Hélder A. Santos,et al.  Protein Coating of DNA Nanostructures for Enhanced Stability and Immunocompatibility , 2017, Advanced healthcare materials.

[87]  Carlos E. Castro,et al.  Conformational Dynamics of Mechanically Compliant DNA Nanostructures from Coarse-Grained Molecular Dynamics Simulations. , 2017, ACS nano.

[88]  Travis A. Meyer,et al.  Regulation at a distance of biomolecular interactions using a DNA origami nanoactuator , 2016, Nature Communications.

[89]  Jiashu Sun,et al.  Stimulus-Responsive Plasmonic Chiral Signals of Gold Nanorods Organized on DNA Origami. , 2017, Nano letters.

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

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

[92]  William L. Hughes,et al.  Nanometrology and super-resolution imaging with DNA , 2017, MRS bulletin.

[93]  Hendrik Dietz,et al.  Dielectrophoretic trapping of multilayer DNA origami nanostructures and DNA origami‐induced local destruction of silicon dioxide , 2015, Electrophoresis.

[94]  Jie Song,et al.  Reconfiguration of DNA molecular arrays driven by information relay , 2017, Science.

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

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

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

[98]  Itamar Willner,et al.  pH-Stimulated Reconfiguration and Structural Isomerization of Origami Dimer and Trimer Systems. , 2016, Nano letters.

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

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

[101]  Hendrik Dietz,et al.  Time-Resolved Small-Angle X-ray Scattering Reveals Millisecond Transitions of a DNA Origami Switch. , 2018, Nano letters.

[102]  Maximilian T. Strauss,et al.  Super-resolution microscopy with DNA-PAINT , 2017, Nature Protocols.

[103]  N. Seeman,et al.  A robust DNA mechanical device controlled by hybridization topology , 2002, Nature.

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

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

[106]  Hai-Jun Su,et al.  Direct design of an energy landscape with bistable DNA origami mechanisms. , 2015, Nano letters.

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

[108]  Yangyang Yang,et al.  Photo-controllable DNA origami nanostructures assembling into predesigned multiorientational patterns. , 2012, Journal of the American Chemical Society.

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

[110]  H. Pei,et al.  Programmable and Multifunctional DNA‐Based Materials for Biomedical Applications , 2018, Advanced materials.

[111]  Satoshi Murata,et al.  Stepping operation of a rotary DNA origami device. , 2017, Chemical communications.

[112]  Matt A. King,et al.  Three-Dimensional Structures Self-Assembled from DNA Bricks , 2012 .

[113]  Veikko Linko,et al.  Metallic Nanostructures Based on DNA Nanoshapes , 2016, Nanomaterials.

[114]  C. Mao,et al.  DNA nanotechnology. , 2004, BioTechniques.

[115]  Satoshi Murata,et al.  Environment‐Dependent Self‐Assembly of DNA Origami Lattices on Phase‐Separated Lipid Membranes , 2018 .

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

[117]  Friedrich C Simmel,et al.  A self-assembled nanoscale robotic arm controlled by electric fields , 2018, Science.

[118]  Tom Quirk,et al.  There’s Plenty of Room at the Bottom , 2006, Size Really Does Matter.