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

Jun, Hyungmin; Shepherd, Tyson R.; Zhang, Kaiming; Bricker, William P.; Li, Shanshan; Chiu, Wah; Bathe, Mark

doi:10.1021/acsnano.8b08671

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

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

DOI:https://doi.org/10.1021/acsnano.8b08671· OSTI ID:1507153

^[1]; ^[1]; ^[2]; ^[1]; Li, Shanshan ^[2]; Chiu, Wah ^[2]; ^[1]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Stanford Univ., Stanford, CA (United States)

3D polyhedral wireframe DNA nanoparticles (DNA-NPs) fabricated using scaffolded DNA origami offer complete and independent control over NP size, structure, and asymmetric functionalization on the 10–100 nm scale. However, the complex DNA sequence design needed for the synthesis of these versatile DNA-NPs has limited their widespread use to date. While the automated sequence design algorithms DAEDALUS and vHelix-BSCOR apply to DNA-NPs synthesized using either uniformly dual or hybrid single-dual duplex edges, respectively, these DNA-NPs are relatively compliant mechanically and are therefore of limited utility for some applications. Further, these algorithms are incapable of handling DNA-NP edge designs composed of more than two duplexes, which are needed to enhance DNA-NP mechanical stiffness. As an alternative, here we introduce the scaffolded DNA origami sequence design algorithm TALOS, which is a generalized procedure for the fully automated design of wireframe 3D polyhedra composed of edges of any cross section with an even number of duplexes, and apply it to DNA-NPs composed uniformly of single honeycomb edges. We also introduce a multiway vertex design that enables the fabrication of DNA-NPs with arbitrary edge lengths and vertex angles and apply it to synthesize a highly asymmetric origami object. Sequence designs are demonstrated to fold robustly into target DNA-NP shapes with high folding efficiency and structural fidelity that is verified using single particle cryo-electron microscopy and 3D reconstruction. Furthermore, in order to test its generality, we apply TALOS to design an in silico library of over 200 DNA-NPs of distinct symmetries and sizes, and for broad impact, we also provide the software as open source for the generation of custom NP designs.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-76SF00515; SC0016353

OSTI ID:: 1507153

Journal Information:: ACS Nano, Journal Name: ACS Nano Journal Issue: 2 Vol. 13; ISSN 1936-0851

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (68)

Computer-Aided Production of Scaffolded DNA Nanostructures from Flat Sheet Meshes Benson, Erik; Mohammed, Abdulmelik; Bosco, Alessandro Angewandte Chemie International Edition, Vol. 55, Issue 31 https://doi.org/10.1002/anie.201602446	journal	June 2016
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
A finite element framework for computation of protein normal modes and mechanical response Bathe, Mark Proteins: Structure, Function, and Bioinformatics, Vol. 70, Issue 4 https://doi.org/10.1002/prot.21708	journal	November 2007
EMAN2: An extensible image processing suite for electron microscopy Tang, Guang; Peng, Liwei; Baldwin, Philip R. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.009	journal	January 2007
Design and Synthesis of Triangulated DNA Origami Trusses Matthies, Michael; Agarwal, Nayan P.; Schmidt, Thorsten L. Nano Letters, Vol. 16, Issue 3 https://doi.org/10.1021/acs.nanolett.6b00381	journal	February 2016
DNA-Mold Templated Assembly of Conductive Gold Nanowires Bayrak, Türkan; Helmi, Seham; Ye, Jingjing Nano Letters, Vol. 18, Issue 3 https://doi.org/10.1021/acs.nanolett.8b00344	journal	February 2018
Self-Assembly of Large DNA Origami with Custom-Designed Scaffolds Chen, Xiaoxing; Wang, Qian; Peng, Jin ACS Applied Materials & Interfaces, Vol. 10, Issue 29 https://doi.org/10.1021/acsami.8b09222	journal	July 2018
Probing Nucleosome Stability with a DNA Origami Nanocaliper Le, Jenny V.; Luo, Yi; Darcy, Michael A. ACS Nano, Vol. 10, Issue 7 https://doi.org/10.1021/acsnano.6b03218	journal	July 2016
Building DNA Nanostructures for Molecular Computation, Templated Assembly, and Biological Applications Rangnekar, Abhijit; LaBean, Thomas H. Accounts of Chemical Research, Vol. 47, Issue 6 https://doi.org/10.1021/ar500023b	journal	April 2014
DNA double-crossover molecules Fu, Tsu Ju; Seeman, Nadrian C. Biochemistry, Vol. 32, Issue 13 https://doi.org/10.1021/bi00064a003	journal	April 1993
Optimization of the CHARMM Additive Force Field for DNA: Improved Treatment of the BI/BII Conformational Equilibrium Hart, Katarina; Foloppe, Nicolas; Baker, Christopher M. Journal of Chemical Theory and Computation, Vol. 8, Issue 1 https://doi.org/10.1021/ct200723y	journal	December 2011
Magnesium Ion–Water Coordination and Exchange in Biomolecular Simulations Allnér, Olof; Nilsson, Lennart; Villa, Alessandra Journal of Chemical Theory and Computation, Vol. 8, Issue 4 https://doi.org/10.1021/ct3000734	journal	March 2012
Assembly and Characterization of 8-Arm and 12-Arm DNA Branched Junctions Wang, Xing; Seeman, Nadrian C. Journal of the American Chemical Society, Vol. 129, Issue 26 https://doi.org/10.1021/ja0693441	journal	July 2007
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
Plasmonic Harvesting of Light Energy for Suzuki Coupling Reactions Wang, Feng; Li, Chuanhao; Chen, Huanjun Journal of the American Chemical Society, Vol. 135, Issue 15 https://doi.org/10.1021/ja310501y	journal	April 2013
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
Six-Helix Bundles Designed from DNA Mathieu, Frederick; Liao, Shiping; Kopatsch, Jens Nano Letters, Vol. 5, Issue 4 https://doi.org/10.1021/nl050084f	journal	April 2005
Direct Mechanical Measurements Reveal the Material Properties of Three-Dimensional DNA Origami Kauert, Dominik J.; Kurth, Thomas; Liedl, Tim Nano Letters, Vol. 11, Issue 12 https://doi.org/10.1021/nl203503s	journal	December 2011
Shape-Controlled Synthesis of Gold Nanostructures Using DNA Origami Molds Helmi, Seham; Ziegler, Christoph; Kauert, Dominik J. Nano Letters, Vol. 14, Issue 11 https://doi.org/10.1021/nl503441v	journal	October 2014
Nanoscale Structure and Microscale Stiffness of DNA Nanotubes Schiffels, Daniel; Liedl, Tim; Fygenson, Deborah K. ACS Nano, Vol. 7, Issue 8 https://doi.org/10.1021/nn401362p	journal	July 2013
Virus-Inspired Membrane Encapsulation of DNA Nanostructures To Achieve In Vivo Stability Perrault, Steven D.; Shih, William M. ACS Nano, Vol. 8, Issue 5 https://doi.org/10.1021/nn5011914	journal	April 2014
Addressing the Instability of DNA Nanostructures in Tissue Culture Hahn, Jaeseung; Wickham, Shelley F. J.; Shih, William M. ACS Nano, Vol. 8, Issue 9 https://doi.org/10.1021/nn503513p	journal	August 2014
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
Hierarchical self-assembly of DNA into symmetric supramolecular polyhedra He, Yu; Ye, Tao; Su, Min Nature, Vol. 452, Issue 7184 https://doi.org/10.1038/nature06597	journal	March 2008
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
DNA rendering of polyhedral meshes at the nanoscale Benson, Erik; Mohammed, Abdulmelik; Gardell, Johan Nature, Vol. 523, Issue 7561 https://doi.org/10.1038/nature14586	journal	July 2015
Programmable self-assembly of three-dimensional nanostructures from 10,000 unique components Ong, Luvena L.; Hanikel, Nikita; Yaghi, Omar K. Nature, Vol. 552, Issue 7683 https://doi.org/10.1038/nature24648	journal	December 2017
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
Fractal assembly of micrometre-scale DNA origami arrays with arbitrary patterns Tikhomirov, Grigory; Petersen, Philip; Qian, Lulu Nature, Vol. 552, Issue 7683 https://doi.org/10.1038/nature24655	journal	December 2017
Dynamic DNA nanotechnology using strand-displacement reactions Zhang, David Yu; Seelig, Georg Nature Chemistry, Vol. 3, Issue 2 https://doi.org/10.1038/nchem.957	journal	January 2011
Oligolysine-based coating protects DNA nanostructures from low-salt denaturation and nuclease degradation Ponnuswamy, Nandhini; Bastings, Maartje M. C.; Nathwani, Bhavik Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15654	journal	May 2017
Magnesium-free self-assembly of multi-layer DNA objects Martin, Thomas G.; Dietz, Hendrik Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms2095	journal	January 2012
Lattice engineering through nanoparticle–DNA frameworks Tian, Ye; Zhang, Yugang; Wang, Tong Nature Materials, Vol. 15, Issue 6, p. 654-661 https://doi.org/10.1038/nmat4571	journal	February 2016
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
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
Spatial control of membrane receptor function using ligand nanocalipers Shaw, Alan; Lundin, Vanessa; Petrova, Ekaterina Nature Methods, Vol. 11, Issue 8 https://doi.org/10.1038/nmeth.3025	journal	July 2014
MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul Nature Methods, Vol. 14, Issue 4 https://doi.org/10.1038/nmeth.4193	journal	February 2017
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
Prescribed nanoparticle cluster architectures and low-dimensional arrays built using octahedral DNA origami frames Tian, Ye; Wang, Tong; Liu, Wenyan Nature Nanotechnology, Vol. 10, Issue 7 https://doi.org/10.1038/nnano.2015.105	journal	May 2015
Complex wireframe DNA origami nanostructures with multi-arm junction vertices Zhang, Fei; Jiang, Shuoxing; Wu, Siyu Nature Nanotechnology, Vol. 10, Issue 9 https://doi.org/10.1038/nnano.2015.162	journal	July 2015
A spatially localized architecture for fast and modular DNA computing Chatterjee, Gourab; Dalchau, Neil; Muscat, Richard A. Nature Nanotechnology, Vol. 12, Issue 9 https://doi.org/10.1038/nnano.2017.127	journal	July 2017
Complex silica composite nanomaterials templated with DNA origami Liu, Xiaoguo; Zhang, Fei; Jing, Xinxin Nature, Vol. 559, Issue 7715 https://doi.org/10.1038/s41586-018-0332-7	journal	July 2018
Mechanical design of DNA nanostructures Castro, Carlos E.; Su, Hai-Jun; Marras, Alexander E. Nanoscale, Vol. 7, Issue 14 https://doi.org/10.1039/C4NR07153K	journal	January 2015
Two design strategies for enhancement of multilayer–DNA-origami folding: underwinding for specific intercalator rescue and staple-break positioning Ke, Yonggang; Bellot, Gaëtan; Voigt, Niels V. Chemical Science, Vol. 3, Issue 8 https://doi.org/10.1039/c2sc20446k	journal	January 2012
Optimized particle-mesh Ewald/multiple-time step integration for molecular dynamics simulations Batcho, Paul F.; Case, David A.; Schlick, Tamar The Journal of Chemical Physics, Vol. 115, Issue 9 https://doi.org/10.1063/1.1389854	journal	September 2001
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Constant pressure molecular dynamics simulation: The Langevin piston method Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W. The Journal of Chemical Physics, Vol. 103, Issue 11 https://doi.org/10.1063/1.470648	journal	September 1995
Cryo-EM structure of a 3D DNA-origami object Bai, X. -c.; Martin, T. G.; Scheres, S. H. W. Proceedings of the National Academy of Sciences, Vol. 109, Issue 49 https://doi.org/10.1073/pnas.1215713109	journal	November 2012
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
Structure-based model for light-harvesting properties of nucleic acid nanostructures Pan, Keyao; Boulais, Etienne; Yang, Lun Nucleic Acids Research, Vol. 42, Issue 4 https://doi.org/10.1093/nar/gkt1269	journal	December 2013
Structure and conformational dynamics of scaffolded DNA origami nanoparticles Pan, Keyao; Bricker, William P.; Ratanalert, Sakul Nucleic Acids Research, Vol. 45, Issue 11 https://doi.org/10.1093/nar/gkx378	journal	May 2017
Uncovering the forces between nucleosomes using DNA origami Funke, Jonas J.; Ketterer, Philip; Lieleg, Corinna Science Advances, Vol. 2, Issue 11 https://doi.org/10.1126/sciadv.1600974	journal	November 2016
Plasmonic nanostructures through DNA-assisted lithography Shen, Boxuan; Linko, Veikko; Tapio, Kosti Science Advances, Vol. 4, Issue 2 https://doi.org/10.1126/sciadv.aap8978	journal	February 2018
Sequence-programmable covalent bonding of designed DNA assemblies Gerling, Thomas; Kube, Massimo; Kick, Benjamin Science Advances, Vol. 4, Issue 8 https://doi.org/10.1126/sciadv.aau1157	journal	August 2018
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
DNA-Templated Self-Assembly of Protein Arrays and Highly Conductive Nanowires Yan, H. Science, Vol. 301, Issue 5641 https://doi.org/10.1126/science.1089389	journal	September 2003
Programming DNA Tube Circumferences Yin, P.; Hariadi, R. F.; Sahu, S. Science, Vol. 321, Issue 5890 https://doi.org/10.1126/science.1157312	journal	August 2008
Control of Self-Assembly of DNA Tubules Through Integration of Gold Nanoparticles Sharma, J.; Chhabra, R.; Cheng, A. Science, Vol. 323, Issue 5910 https://doi.org/10.1126/science.1165831	journal	January 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
DNA Origami with Complex Curvatures in Three-Dimensional Space Han, D.; Pal, S.; Nangreave, J. Science, Vol. 332, Issue 6027 https://doi.org/10.1126/science.1202998	journal	April 2011
Predictive Self-Assembly of Polyhedra into Complex Structures Damasceno, P. F.; Engel, M.; Glotzer, S. C. Science, Vol. 337, Issue 6093 https://doi.org/10.1126/science.1220869	journal	July 2012
Polyhedra Self-Assembled from DNA Tripods and Characterized with 3D DNA-PAINT Iinuma, Ryosuke; Ke, Yonggang; Jungmann, Ralf Science, Vol. 344, Issue 6179 https://doi.org/10.1126/science.1250944	journal	March 2014
Casting inorganic structures with DNA molds Sun, W.; Boulais, E.; Hakobyan, Y. Science, Vol. 346, Issue 6210 https://doi.org/10.1126/science.1258361	journal	October 2014
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
Designer nanoscale DNA assemblies programmed from the top down Veneziano, R.; Ratanalert, S.; Zhang, K. Science, Vol. 352, Issue 6293 https://doi.org/10.1126/science.aaf4388	journal	May 2016
Algorithmic Self-Assembly of DNA Sierpinski Triangles Rothemund, Paul W. K.; Papadakis, Nick; Winfree, Erik PLoS Biology, Vol. 2, Issue 12 https://doi.org/10.1371/journal.pbio.0020424	journal	December 2004
Cytoskeletal Bundle Mechanics Bathe, Mark; Heussinger, Claus; Claessens, Mireille M. A. E. Biophysical Journal, Vol. 94, Issue 8 https://doi.org/10.1529/biophysj.107.119743	journal	April 2008

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