Automated Sequence Design of 3D Polyhedral Wireframe DNA Origami with Honeycomb Edges
Abstract
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 robustlymore »
- Authors:
-
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- Stanford Univ., Stanford, CA (United States)
- Publication Date:
- Research Org.:
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1507153
- Grant/Contract Number:
- AC02-76SF00515; CCF-1564025; SC0016353; N000141210621; N000141612953; N000141512830; N000141310664; CMMI-1334109; P41GM103832
- Resource Type:
- Accepted Manuscript
- Journal Name:
- ACS Nano
- Additional Journal Information:
- Journal Volume: 13; Journal Issue: 2; Journal ID: ISSN 1936-0851
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 3D cryo-EM reconstruction; DNA nanotechnology; molecular dynamics; scaffolded DNA origami; six-helix bundle; wireframe origami
Citation Formats
Jun, Hyungmin, Shepherd, Tyson R., Zhang, Kaiming, Bricker, William P., Li, Shanshan, Chiu, Wah, and Bathe, Mark. Automated Sequence Design of 3D Polyhedral Wireframe DNA Origami with Honeycomb Edges. United States: N. p., 2019.
Web. doi:10.1021/acsnano.8b08671.
Jun, Hyungmin, Shepherd, Tyson R., Zhang, Kaiming, Bricker, William P., Li, Shanshan, Chiu, Wah, & Bathe, Mark. Automated Sequence Design of 3D Polyhedral Wireframe DNA Origami with Honeycomb Edges. United States. https://doi.org/10.1021/acsnano.8b08671
Jun, Hyungmin, Shepherd, Tyson R., Zhang, Kaiming, Bricker, William P., Li, Shanshan, Chiu, Wah, and Bathe, Mark. Thu .
"Automated Sequence Design of 3D Polyhedral Wireframe DNA Origami with Honeycomb Edges". United States. https://doi.org/10.1021/acsnano.8b08671. https://www.osti.gov/servlets/purl/1507153.
@article{osti_1507153,
title = {Automated Sequence Design of 3D Polyhedral Wireframe DNA Origami with Honeycomb Edges},
author = {Jun, Hyungmin and Shepherd, Tyson R. and Zhang, Kaiming and Bricker, William P. and Li, Shanshan and Chiu, Wah and Bathe, Mark},
abstractNote = {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.},
doi = {10.1021/acsnano.8b08671},
journal = {ACS Nano},
number = 2,
volume = 13,
place = {United States},
year = {2019},
month = {1}
}
Web of Science
Works referenced in this record:
Folding DNA to create nanoscale shapes and patterns
journal, March 2006
- Rothemund, Paul W. K.
- Nature, Vol. 440, Issue 7082, p. 297-302
DNA Origami with Complex Curvatures in Three-Dimensional Space
journal, April 2011
- Han, D.; Pal, S.; Nangreave, J.
- Science, Vol. 332, Issue 6027
Complex wireframe DNA origami nanostructures with multi-arm junction vertices
journal, July 2015
- Zhang, Fei; Jiang, Shuoxing; Wu, Siyu
- Nature Nanotechnology, Vol. 10, Issue 9
Computer-Aided Production of Scaffolded DNA Nanostructures from Flat Sheet Meshes
journal, June 2016
- Benson, Erik; Mohammed, Abdulmelik; Bosco, Alessandro
- Angewandte Chemie International Edition, Vol. 55, Issue 31
Fractal assembly of micrometre-scale DNA origami arrays with arbitrary patterns
journal, December 2017
- Tikhomirov, Grigory; Petersen, Philip; Qian, Lulu
- Nature, Vol. 552, Issue 7683
Autonomously designed free-form 2D DNA origami
journal, January 2019
- Jun, Hyungmin; Zhang, Fei; Shepherd, Tyson
- Science Advances, Vol. 5, Issue 1
Hierarchical self-assembly of DNA into symmetric supramolecular polyhedra
journal, March 2008
- He, Yu; Ye, Tao; Su, Min
- Nature, Vol. 452, Issue 7184
Self-assembly of DNA into nanoscale three-dimensional shapes
journal, May 2009
- Douglas, Shawn M.; Dietz, Hendrik; Liedl, Tim
- Nature, Vol. 459, Issue 7245
Folding DNA into Twisted and Curved Nanoscale Shapes
journal, August 2009
- Dietz, H.; Douglas, S. M.; Shih, W. M.
- Science, Vol. 325, Issue 5941
Polyhedra Self-Assembled from DNA Tripods and Characterized with 3D DNA-PAINT
journal, March 2014
- Iinuma, Ryosuke; Ke, Yonggang; Jungmann, Ralf
- Science, Vol. 344, Issue 6179
DNA rendering of polyhedral meshes at the nanoscale
journal, July 2015
- Benson, Erik; Mohammed, Abdulmelik; Gardell, Johan
- Nature, Vol. 523, Issue 7561
Designer nanoscale DNA assemblies programmed from the top down
journal, May 2016
- Veneziano, R.; Ratanalert, S.; Zhang, K.
- Science, Vol. 352, Issue 6293
Design and Synthesis of Triangulated DNA Origami Trusses
journal, February 2016
- Matthies, Michael; Agarwal, Nayan P.; Schmidt, Thorsten L.
- Nano Letters, Vol. 16, Issue 3
Gigadalton-scale shape-programmable DNA assemblies
journal, December 2017
- Wagenbauer, Klaus F.; Sigl, Christian; Dietz, Hendrik
- Nature, Vol. 552, Issue 7683
Programmable self-assembly of three-dimensional nanostructures from 10,000 unique components
journal, December 2017
- Ong, Luvena L.; Hanikel, Nikita; Yaghi, Omar K.
- Nature, Vol. 552, Issue 7683
Algorithmic Self-Assembly of DNA Sierpinski Triangles
journal, December 2004
- Rothemund, Paul W. K.; Papadakis, Nick; Winfree, Erik
- PLoS Biology, Vol. 2, Issue 12
Dynamic DNA nanotechnology using strand-displacement reactions
journal, January 2011
- Zhang, David Yu; Seelig, Georg
- Nature Chemistry, Vol. 3, Issue 2
Building DNA Nanostructures for Molecular Computation, Templated Assembly, and Biological Applications
journal, April 2014
- Rangnekar, Abhijit; LaBean, Thomas H.
- Accounts of Chemical Research, Vol. 47, Issue 6
A spatially localized architecture for fast and modular DNA computing
journal, July 2017
- Chatterjee, Gourab; Dalchau, Neil; Muscat, Richard A.
- Nature Nanotechnology, Vol. 12, Issue 9
DNA-Directed Artificial Light-Harvesting Antenna
journal, August 2011
- Dutta, Palash K.; Varghese, Reji; Nangreave, Jeanette
- Journal of the American Chemical Society, Vol. 133, Issue 31
Plasmonic Harvesting of Light Energy for Suzuki Coupling Reactions
journal, April 2013
- Wang, Feng; Li, Chuanhao; Chen, Huanjun
- Journal of the American Chemical Society, Vol. 135, Issue 15
Structure-based model for light-harvesting properties of nucleic acid nanostructures
journal, December 2013
- Pan, Keyao; Boulais, Etienne; Yang, Lun
- Nucleic Acids Research, Vol. 42, Issue 4
Programmed coherent coupling in a synthetic DNA-based excitonic circuit
journal, November 2017
- Boulais, Étienne; Sawaya, Nicolas P. D.; Veneziano, Rémi
- Nature Materials, Vol. 17, Issue 2
DNA-Templated Self-Assembly of Protein Arrays and Highly Conductive Nanowires
journal, September 2003
- Yan, H.
- Science, Vol. 301, Issue 5641
Casting inorganic structures with DNA molds
journal, October 2014
- Sun, W.; Boulais, E.; Hakobyan, Y.
- Science, Vol. 346, Issue 6210
Shape-Controlled Synthesis of Gold Nanostructures Using DNA Origami Molds
journal, October 2014
- Helmi, Seham; Ziegler, Christoph; Kauert, Dominik J.
- Nano Letters, Vol. 14, Issue 11
DNA-Mold Templated Assembly of Conductive Gold Nanowires
journal, February 2018
- Bayrak, Türkan; Helmi, Seham; Ye, Jingjing
- Nano Letters, Vol. 18, Issue 3
Plasmonic nanostructures through DNA-assisted lithography
journal, February 2018
- Shen, Boxuan; Linko, Veikko; Tapio, Kosti
- Science Advances, Vol. 4, Issue 2
Programming DNA Tube Circumferences
journal, August 2008
- Yin, P.; Hariadi, R. F.; Sahu, S.
- Science, Vol. 321, Issue 5890
Control of Self-Assembly of DNA Tubules Through Integration of Gold Nanoparticles
journal, January 2009
- Sharma, J.; Chhabra, R.; Cheng, A.
- Science, Vol. 323, Issue 5910
Programming Self-Assembly of DNA Origami Honeycomb Two-Dimensional Lattices and Plasmonic Metamaterials
journal, June 2016
- Wang, Pengfei; Gaitanaros, Stavros; Lee, Seungwoo
- Journal of the American Chemical Society, Vol. 138, Issue 24
Diamond family of nanoparticle superlattices
journal, February 2016
- Liu, W.; Tagawa, M.; Xin, H. L.
- Science, Vol. 351, Issue 6273, p. 582-586
A primer to scaffolded DNA origami
journal, February 2011
- Castro, Carlos Ernesto; Kilchherr, Fabian; Kim, Do-Nyun
- Nature Methods, Vol. 8, Issue 3
DNA double-crossover molecules
journal, April 1993
- Fu, Tsu Ju; Seeman, Nadrian C.
- Biochemistry, Vol. 32, Issue 13
Assembly and Characterization of 8-Arm and 12-Arm DNA Branched Junctions
journal, July 2007
- Wang, Xing; Seeman, Nadrian C.
- Journal of the American Chemical Society, Vol. 129, Issue 26
Rapid prototyping of 3D DNA-origami shapes with caDNAno
journal, June 2009
- Douglas, Shawn M.; Marblestone, Adam H.; Teerapittayanon, Surat
- Nucleic Acids Research, Vol. 37, Issue 15
Six-Helix Bundles Designed from DNA
journal, April 2005
- Mathieu, Frederick; Liao, Shiping; Kopatsch, Jens
- Nano Letters, Vol. 5, Issue 4
Direct Mechanical Measurements Reveal the Material Properties of Three-Dimensional DNA Origami
journal, December 2011
- Kauert, Dominik J.; Kurth, Thomas; Liedl, Tim
- Nano Letters, Vol. 11, Issue 12
Self-assembly of three-dimensional prestressed tensegrity structures from DNA
journal, June 2010
- Liedl, Tim; Högberg, Björn; Tytell, Jessica
- Nature Nanotechnology, Vol. 5, Issue 7
Nanoscale Structure and Microscale Stiffness of DNA Nanotubes
journal, July 2013
- Schiffels, Daniel; Liedl, Tim; Fygenson, Deborah K.
- ACS Nano, Vol. 7, Issue 8
Cytoskeletal Bundle Mechanics
journal, April 2008
- Bathe, Mark; Heussinger, Claus; Claessens, Mireille M. A. E.
- Biophysical Journal, Vol. 94, Issue 8
Mechanical design of DNA nanostructures
journal, January 2015
- Castro, Carlos E.; Su, Hai-Jun; Marras, Alexander E.
- Nanoscale, Vol. 7, Issue 14
Addressing the Instability of DNA Nanostructures in Tissue Culture
journal, August 2014
- Hahn, Jaeseung; Wickham, Shelley F. J.; Shih, William M.
- ACS Nano, Vol. 8, Issue 9
Oligolysine-based coating protects DNA nanostructures from low-salt denaturation and nuclease degradation
journal, May 2017
- Ponnuswamy, Nandhini; Bastings, Maartje M. C.; Nathwani, Bhavik
- Nature Communications, Vol. 8, Issue 1
Virus-Inspired Membrane Encapsulation of DNA Nanostructures To Achieve In Vivo Stability
journal, April 2014
- Perrault, Steven D.; Shih, William M.
- ACS Nano, Vol. 8, Issue 5
Lattice engineering through nanoparticle–DNA frameworks
journal, February 2016
- Tian, Ye; Zhang, Yugang; Wang, Tong
- Nature Materials, Vol. 15, Issue 6, p. 654-661
Prescribed nanoparticle cluster architectures and low-dimensional arrays built using octahedral DNA origami frames
journal, May 2015
- Tian, Ye; Wang, Tong; Liu, Wenyan
- Nature Nanotechnology, Vol. 10, Issue 7
Complex silica composite nanomaterials templated with DNA origami
journal, July 2018
- Liu, Xiaoguo; Zhang, Fei; Jing, Xinxin
- Nature, Vol. 559, Issue 7715
Sequence-programmable covalent bonding of designed DNA assemblies
journal, August 2018
- Gerling, Thomas; Kube, Massimo; Kick, Benjamin
- Science Advances, Vol. 4, Issue 8
Probing Nucleosome Stability with a DNA Origami Nanocaliper
journal, July 2016
- Le, Jenny V.; Luo, Yi; Darcy, Michael A.
- ACS Nano, Vol. 10, Issue 7
Uncovering the forces between nucleosomes using DNA origami
journal, November 2016
- Funke, Jonas J.; Ketterer, Philip; Lieleg, Corinna
- Science Advances, Vol. 2, Issue 11
Spatial control of membrane receptor function using ligand nanocalipers
journal, July 2014
- Shaw, Alan; Lundin, Vanessa; Petrova, Ekaterina
- Nature Methods, Vol. 11, Issue 8
A finite element framework for computation of protein normal modes and mechanical response
journal, November 2007
- Bathe, Mark
- Proteins: Structure, Function, and Bioinformatics, Vol. 70, Issue 4
Two design strategies for enhancement of multilayer–DNA-origami folding: underwinding for specific intercalator rescue and staple-break positioning
journal, January 2012
- Ke, Yonggang; Bellot, Gaëtan; Voigt, Niels V.
- Chemical Science, Vol. 3, Issue 8
Magnesium-free self-assembly of multi-layer DNA objects
journal, January 2012
- Martin, Thomas G.; Dietz, Hendrik
- Nature Communications, Vol. 3, Issue 1
Cryo-EM structure of a 3D DNA-origami object
journal, November 2012
- Bai, X. -c.; Martin, T. G.; Scheres, S. H. W.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 49
Structure and conformational dynamics of scaffolded DNA origami nanoparticles
journal, May 2017
- Pan, Keyao; Bricker, William P.; Ratanalert, Sakul
- Nucleic Acids Research, Vol. 45, Issue 11
Self-Assembly of Large DNA Origami with Custom-Designed Scaffolds
journal, July 2018
- Chen, Xiaoxing; Wang, Qian; Peng, Jin
- ACS Applied Materials & Interfaces, Vol. 10, Issue 29
Predictive Self-Assembly of Polyhedra into Complex Structures
journal, July 2012
- Damasceno, P. F.; Engel, M.; Glotzer, S. C.
- Science, Vol. 337, Issue 6093
MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy
journal, February 2017
- Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul
- Nature Methods, Vol. 14, Issue 4
EMAN2: An extensible image processing suite for electron microscopy
journal, January 2007
- Tang, Guang; Peng, Liwei; Baldwin, Philip R.
- Journal of Structural Biology, Vol. 157, Issue 1
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Comparison of simple potential functions for simulating liquid water
journal, July 1983
- Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
- The Journal of Chemical Physics, Vol. 79, Issue 2
Scalable molecular dynamics with NAMD
journal, January 2005
- Phillips, James C.; Braun, Rosemary; Wang, Wei
- Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
Optimization of the CHARMM Additive Force Field for DNA: Improved Treatment of the BI/BII Conformational Equilibrium
journal, December 2011
- Hart, Katarina; Foloppe, Nicolas; Baker, Christopher M.
- Journal of Chemical Theory and Computation, Vol. 8, Issue 1
Magnesium Ion–Water Coordination and Exchange in Biomolecular Simulations
journal, March 2012
- Allnér, Olof; Nilsson, Lennart; Villa, Alessandra
- Journal of Chemical Theory and Computation, Vol. 8, Issue 4
Optimized particle-mesh Ewald/multiple-time step integration for molecular dynamics simulations
journal, September 2001
- Batcho, Paul F.; Case, David A.; Schlick, Tamar
- The Journal of Chemical Physics, Vol. 115, Issue 9
Constant pressure molecular dynamics simulation: The Langevin piston method
journal, September 1995
- Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W.
- The Journal of Chemical Physics, Vol. 103, Issue 11
Works referencing / citing this record:
The Topology of Scaffold Routings on Non-Spherical Mesh Wireframes
text, January 2020
- Mohammed, Abdulmelik; Jonoska, Nataša; Saito, Masahico
- Schloss Dagstuhl - Leibniz-Zentrum für Informatik
ENSnano: A 3D Modeling Software for DNA Nanostructures
text, January 2021
- Levy, Nicolas; Schabanel, Nicolas
- Schloss Dagstuhl - Leibniz-Zentrum für Informatik