Planar 2D wireframe DNA origami

Wang, Xiao; Li, Shanshan; Jun, Hyungmin; John, Torsten; Zhang, Kaiming; Fowler, Hannah; Doye, Jonathan P.K.; Chiu, Wah; Bathe, Mark

doi:10.1126/sciadv.abn0039

Title: Planar 2D wireframe DNA origami

Journal Article · Fri May 20 00:00:00 EDT 2022 · Science Advances

DOI:https://doi.org/10.1126/sciadv.abn0039· OSTI ID:1908739

^[1];

^[2];

^[3];

^[1];

^[2];

^[4];

^[5];

^[1]

Massachusetts Institute of Technology (MIT), Cambridge, MA (United States)
Stanford University, CA (United States); University of Science and Technology of China, Hefei (China)
Massachusetts Institute of Technology (MIT), Cambridge, MA (United States); Jeonbuk National University, Jeonju (Korea, Republic of)
University of Oxford (United Kingdom)
Stanford University, CA (United States); SLAC National Accelerator Laboratory, Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Two-dimensional (2D) DNA origami is widely used for applications ranging from excitonics to single-molecule biophysics. Conventional, single-layer 2D DNA origami exhibits flexibility and curvature in solution; however, that may limit its suitability as a 2D structural template. In contrast, 2D wireframe DNA origami rendered with six-helix bundle edges offers local control over duplex orientations with enhanced in-plane rigidity. Here, we investigate the 3D structure of these assemblies using cryo–electron microscopy (cryo-EM). 3D reconstructions reveal a high degree of planarity and homogeneity in solution for polygonal objects with and without internal mesh, enabling 10-Å resolution for a triangle. Coarse-grained simulations were in agreement with cryo-EM data, offering molecular structural insight into this class of 2D DNA origami. Our results suggest that these assemblies may be valuable for 2D material applications and geometries that require high structural fidelity together with local control over duplex orientations, rather than parallel duplex assembly.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); US Department of the Navy, Office of Naval Research (ONR); Army Research Office (ARO); Alexander von Humboldt Foundation; Engineering and Physical Sciences Research Council (EPSRC)

Grant/Contract Number:: AC02-76SF00515; CBET-1729397; CCF-1956054; N00014-21-1-4013; N00014-20-1-2084; W911NF-19-2-0026; EP/L015722/1

OSTI ID:: 1908739

Journal Information:: Science Advances, Vol. 8, Issue 20; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

References (56)

Understanding the Mechanical Properties of DNA Origami Tiles and Controlling the Kinetics of Their Folding and Unfolding Reconfiguration Chen, Haorong; Weng, Te-Wei; Riccitelli, Molly M. Journal of the American Chemical Society, Vol. 136, Issue 19 https://doi.org/10.1021/ja500612d	journal	May 2014
In situ structure and dynamics of DNA origami determined through molecular dynamics simulations Yoo, J.; Aksimentiev, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 50 https://doi.org/10.1073/pnas.1316521110	journal	November 2013
Rapid prototyping of 3D DNA-origami shapes with caDNAno Douglas, Shawn M.; Marblestone, Adam H.; Teerapittayanon, Surat Nucleic Acids Research, Vol. 37, Issue 15 https://doi.org/10.1093/nar/gkp436	journal	June 2009
Folding DNA into Twisted and Curved Nanoscale Shapes Dietz, H.; Douglas, S. M.; Shih, W. M. Science, Vol. 325, Issue 5941 https://doi.org/10.1126/science.1174251	journal	August 2009
TacoxDNA: A user‐friendly web server for simulations of complex DNA structures, from single strands to origami Suma, Antonio; Poppleton, Erik; Matthies, Michael Journal of Computational Chemistry, Vol. 40, Issue 29 https://doi.org/10.1002/jcc.26029	journal	July 2019
DNA-Directed Artificial Light-Harvesting Antenna Dutta, Palash K.; Varghese, Reji; Nangreave, Jeanette Journal of the American Chemical Society, Vol. 133, Issue 31 https://doi.org/10.1021/ja1115138	journal	August 2011
Programming Light-Harvesting Efficiency Using DNA Origami Hemmig, Elisa A.; Creatore, Celestino; Wünsch, Bettina Nano Letters, Vol. 16, Issue 4 https://doi.org/10.1021/acs.nanolett.5b05139	journal	March 2016
Coarse-grained modelling of the structural properties of DNA origami Snodin, Benedict E. K.; Schreck, John S.; Romano, Flavio Nucleic Acids Research, Vol. 47, Issue 3 https://doi.org/10.1093/nar/gky1304	journal	January 2019
DNA Origami as a Carrier for Circumvention of Drug Resistance Jiang, Qiao; Song, Chen; Nangreave, Jeanette Journal of the American Chemical Society, Vol. 134, Issue 32 https://doi.org/10.1021/ja304263n	journal	August 2012
Revealing the structures of megadalton-scale DNA complexes with nucleotide resolution Kube, Massimo; Kohler, Fabian; Feigl, Elija Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-20020-7	journal	December 2020
Automated sequence design of 2D wireframe DNA origami with honeycomb edges Jun, Hyungmin; Wang, Xiao; Bricker, William P. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13457-y	journal	November 2019
Ultra-thermostable RNA nanoparticles for solubilizing and high-yield loading of paclitaxel for breast cancer therapy Guo, Sijin; Vieweger, Mario; Zhang, Kaiming Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14780-5	journal	February 2020
Gigadalton-scale shape-programmable DNA assemblies Wagenbauer, Klaus F.; Sigl, Christian; Dietz, Hendrik Nature, Vol. 552, Issue 7683 https://doi.org/10.1038/nature24651	journal	December 2017
Folding DNA to create nanoscale shapes and patterns Rothemund, Paul W. K. Nature, Vol. 440, Issue 7082, p. 297-302 https://doi.org/10.1038/nature04586	journal	March 2006
Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT Jungmann, Ralf; Avendaño, Maier S.; Woehrstein, Johannes B. Nature Methods, Vol. 11, Issue 3 https://doi.org/10.1038/nmeth.2835	journal	February 2014
DNA Origami Chromophore Scaffold Exploiting HomoFRET Energy Transport to Create Molecular Photonic Wires Klein, William P.; Rolczynski, Brian S.; Oliver, Sean M. ACS Applied Nano Materials, Vol. 3, Issue 4 https://doi.org/10.1021/acsanm.0c00038	journal	March 2020
Capturing transient antibody conformations with DNA origami epitopes Zhang, Ping; Liu, Xiaoguo; Liu, Pi Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16949-4	journal	June 2020
Shape-Controlled Nanofabrication of Conducting Polymer on Planar DNA Templates Wang, Zhen-Gang; Liu, Qing; Ding, Baoquan Chemistry of Materials, Vol. 26, Issue 11 https://doi.org/10.1021/cm501445u	journal	June 2014
Single-Molecule Imaging of Dynamic Motions of Biomolecules in DNA Origami Nanostructures Using High-Speed Atomic Force Microscopy Endo, Masayuki; Sugiyama, Hiroshi Accounts of Chemical Research, Vol. 47, Issue 6 https://doi.org/10.1021/ar400299m	journal	March 2014
Routing of individual polymers in designed patterns Knudsen, Jakob Bach; Liu, Lei; Bank Kodal, Anne Louise Nature Nanotechnology, Vol. 10, Issue 10 https://doi.org/10.1038/nnano.2015.190	journal	August 2015
Programmed coherent coupling in a synthetic DNA-based excitonic circuit Boulais, Étienne; Sawaya, Nicolas P. D.; Veneziano, Rémi Nature Materials, Vol. 17, Issue 2 https://doi.org/10.1038/nmat5033	journal	November 2017
Design, optimization and analysis of large DNA and RNA nanostructures through interactive visualization, editing and molecular simulation Poppleton, Erik; Bohlin, Joakim; Matthies, Michael Nucleic Acids Research, Vol. 48, Issue 12 https://doi.org/10.1093/nar/gkaa417	journal	May 2020
Autonomously designed free-form 2D DNA origami Jun, Hyungmin; Zhang, Fei; Shepherd, Tyson Science Advances, Vol. 5, Issue 1 https://doi.org/10.1126/sciadv.aav0655	journal	January 2019
Advancing Biophysics Using DNA Origami Engelen, Wouter; Dietz, Hendrik Annual Review of Biophysics, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-biophys-110520-125739	journal	May 2021
Quantitative prediction of 3D solution shape and flexibility of nucleic acid nanostructures Kim, Do-Nyun; Kilchherr, Fabian; Dietz, Hendrik Nucleic Acids Research, Vol. 40, Issue 7 https://doi.org/10.1093/nar/gkr1173	journal	December 2011
Role of nanoscale antigen organization on B-cell activation probed using DNA origami Veneziano, Rémi; Moyer, Tyson J.; Stone, Matthew B. Nature Nanotechnology, Vol. 15, Issue 8 https://doi.org/10.1038/s41565-020-0719-0	journal	June 2020
Optimal Determination of Particle Orientation, Absolute Hand, and Contrast Loss in Single-particle Electron Cryomicroscopy Rosenthal, Peter B.; Henderson, Richard Journal of Molecular Biology, Vol. 333, Issue 4 https://doi.org/10.1016/j.jmb.2003.07.013	journal	October 2003
Diamond family of nanoparticle superlattices Liu, W.; Tagawa, M.; Xin, H. L. Science, Vol. 351, Issue 6273, p. 582-586 https://doi.org/10.1126/science.aad2080	journal	February 2016
Design and Characterization of 1D Nanotubes and 2D Periodic Arrays Self-Assembled from DNA Multi-Helix Bundles Wang, Tong; Schiffels, Daniel; Martinez Cuesta, Sergio Journal of the American Chemical Society, Vol. 134, Issue 3 https://doi.org/10.1021/ja207976q	journal	January 2012
DNA Origami as an In Vivo Drug Delivery Vehicle for Cancer Therapy Zhang, Qian; Jiang, Qiao; Li, Na ACS Nano, Vol. 8, Issue 7 https://doi.org/10.1021/nn502058j	journal	June 2014
Roadmap on biological pathways for electronic nanofabrication and materials Bathe, Mark; Chrisey, Linda A.; Herr, Daniel J. C. Nano Futures, Vol. 3, Issue 1 https://doi.org/10.1088/2399-1984/aaf7d5	journal	January 2019
Engineering and mapping nanocavity emission via precision placement of DNA origami Gopinath, Ashwin; Miyazono, Evan; Faraon, Andrei Nature, Vol. 535, Issue 7612 https://doi.org/10.1038/nature18287	journal	July 2016
Position Accuracy of Gold Nanoparticles on DNA Origami Structures Studied with Small-Angle X-ray Scattering Hartl, Caroline; Frank, Kilian; Amenitsch, Heinz Nano Letters, Vol. 18, Issue 4 https://doi.org/10.1021/acs.nanolett.8b00412	journal	March 2018
Construction of a DNA Origami Based Molecular Electro-optical Modulator Wang, Xiao; Li, Chen; Niu, Dong Nano Letters, Vol. 18, Issue 3 https://doi.org/10.1021/acs.nanolett.8b00332	journal	February 2018
Photophysics of J-Aggregate-Mediated Energy Transfer on DNA Banal, James L.; Kondo, Toru; Veneziano, Rémi The Journal of Physical Chemistry Letters, Vol. 8, Issue 23 https://doi.org/10.1021/acs.jpclett.7b01898	journal	November 2017
RELION: Implementation of a Bayesian approach to cryo-EM structure determination Scheres, Sjors H. W. Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530 https://doi.org/10.1016/j.jsb.2012.09.006	journal	December 2012
Single-molecule chemical reactions on DNA origami Voigt, Niels V.; Tørring, Thomas; Rotaru, Alexandru Nature Nanotechnology, Vol. 5, Issue 3 https://doi.org/10.1038/nnano.2010.5	journal	February 2010
FRET efficiency and antenna effect in multi-color DNA origami-based light harvesting systems Olejko, L.; Bald, I. RSC Advances, Vol. 7, Issue 39 https://doi.org/10.1039/C7RA02114C	journal	January 2017
Optimized Assembly and Covalent Coupling of Single-Molecule DNA Origami Nanoarrays Gopinath, Ashwin; Rothemund, Paul W. K. ACS Nano, Vol. 8, Issue 12 https://doi.org/10.1021/nn506014s	journal	November 2014
Rapid prototyping of arbitrary 2D and 3D wireframe DNA origami Jun, Hyungmin; Wang, Xiao; Parsons, Molly F. Nucleic Acids Research, Vol. 49, Issue 18 https://doi.org/10.1093/nar/gkab762	journal	September 2021
Self-assembly of three-dimensional prestressed tensegrity structures from DNA Liedl, Tim; Högberg, Björn; Tytell, Jessica Nature Nanotechnology, Vol. 5, Issue 7 https://doi.org/10.1038/nnano.2010.107	journal	June 2010
OxDNA.org: a public webserver for coarse-grained simulations of DNA and RNA nanostructures Poppleton, Erik; Romero, Roger; Mallya, Aatmik Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab324	journal	May 2021
Designer DNA architecture offers precise and multivalent spatial pattern-recognition for viral sensing and inhibition Kwon, Paul S.; Ren, Shaokang; Kwon, Seok-Joon Nature Chemistry, Vol. 12, Issue 1 https://doi.org/10.1038/s41557-019-0369-8	journal	November 2019
DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response Kuzyk, Anton; Schreiber, Robert; Fan, Zhiyuan Nature, Vol. 483, Issue 7389 https://doi.org/10.1038/nature10889	journal	March 2012
Programming Self-Assembly of DNA Origami Honeycomb Two-Dimensional Lattices and Plasmonic Metamaterials Wang, Pengfei; Gaitanaros, Stavros; Lee, Seungwoo Journal of the American Chemical Society, Vol. 138, Issue 24 https://doi.org/10.1021/jacs.6b03966	journal	June 2016
Dynamic and Progressive Control of DNA Origami Conformation by Modulating DNA Helicity with Chemical Adducts Chen, Haorong; Zhang, Hanyu; Pan, Jing ACS Nano, Vol. 10, Issue 5 https://doi.org/10.1021/acsnano.6b01339	journal	April 2016
A comparison between parallelization approaches in molecular dynamics simulations on GPUs Rovigatti, Lorenzo; Šulc, Petr; Reguly, István Z. Journal of Computational Chemistry, Vol. 36, Issue 1 https://doi.org/10.1002/jcc.23763	journal	October 2014
Dimensions and Global Twist of Single-Layer DNA Origami Measured by Small-Angle X-ray Scattering Baker, Matthew A. B.; Tuckwell, Andrew J.; Berengut, Jonathan F. ACS Nano, Vol. 12, Issue 6 https://doi.org/10.1021/acsnano.8b01669	journal	May 2018
A primer to scaffolded DNA origami Castro, Carlos Ernesto; Kilchherr, Fabian; Kim, Do-Nyun Nature Methods, Vol. 8, Issue 3 https://doi.org/10.1038/nmeth.1570	journal	February 2011
Effect of DNA Hairpin Loops on the Twist of Planar DNA Origami Tiles Li, Zhe; Wang, Lei; Yan, Hao Langmuir, Vol. 28, Issue 4 https://doi.org/10.1021/la2037873	journal	December 2011
Programming Structured DNA Assemblies to Probe Biophysical Processes Wamhoff, Eike-Christian; Banal, James L.; Bricker, William P. Annual Review of Biophysics, Vol. 48, Issue 1 https://doi.org/10.1146/annurev-biophys-052118-115259	journal	May 2019
cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination Punjani, Ali; Rubinstein, John L.; Fleet, David J. Nature Methods, Vol. 14, Issue 3 https://doi.org/10.1038/nmeth.4169	journal	February 2017
A Single Molecule Polyphenylene-Vinylene Photonic Wire Madsen, Mikael; Bakke, Mette R.; Gudnason, Daniel A. ACS Nano, Vol. 15, Issue 6 https://doi.org/10.1021/acsnano.0c10922	journal	May 2021
Self-Assembled DNA Photonic Wire for Long-Range Energy Transfer Hannestad, Jonas K.; Sandin, Peter; Albinsson, Bo Journal of the American Chemical Society, Vol. 130, Issue 47 https://doi.org/10.1021/ja803407t	journal	November 2008
Bioproduction of pure, kilobase-scale single-stranded DNA Shepherd, Tyson R.; Du, Rebecca R.; Huang, Hellen Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-42665-1	journal	April 2019
Self-assembly of DNA into nanoscale three-dimensional shapes Douglas, Shawn M.; Dietz, Hendrik; Liedl, Tim Nature, Vol. 459, Issue 7245 https://doi.org/10.1038/nature08016	journal	May 2009

Similar Records

Automated Sequence Design of 3D Polyhedral Wireframe DNA Origami with Honeycomb Edges

Journal Article · Thu Jan 03 00:00:00 EST 2019 · ACS Nano · OSTI ID:1908739

Jun, Hyungmin; Shepherd, Tyson R.; Zhang, Kaiming; +4 more

Rapid prototyping of arbitrary 2D and 3D wireframe DNA origami

Journal Article · Sat Sep 11 00:00:00 EDT 2021 · Nucleic Acids Research · OSTI ID:1908739

Jun, Hyungmin; Wang, Xiao; Parsons, Molly F.; +6 more

The path towards functional nanoparticle-DNA origami composites

Journal Article · Thu Aug 29 00:00:00 EDT 2019 · Materials Science and Engineering. R, Reports · OSTI ID:1908739

Johnson, Joshua A.; Dehankar, Abhilasha; Robbins, Ariel; +7 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Planar 2D wireframe DNA origami

Citation Formats

References (56)

Similar Records

Related Subjects