Programmable 3D Hexagonal Geometry of DNA Tensegrity Triangles

Lu, Brandon; Woloszyn, Karol; Ohayon, Yoel P.; Yang, Bena; Zhang, Cuizheng; Mao, Chengde; Seeman, Nadrian C.; Vecchioni, Simon; Sha, Ruojie

doi:10.1002/anie.202213451

Programmable 3D Hexagonal Geometry of DNA Tensegrity Triangles

Journal Article · Wed Dec 14 23:00:00 EST 2022 · Angewandte Chemie (International Edition)

DOI:https://doi.org/10.1002/anie.202213451· OSTI ID:2419790

Lu, Brandon ^[1]; Woloszyn, Karol ^[2]; Ohayon, Yoel P. ^[2]; Yang, Bena ^[2]; Zhang, Cuizheng ^[3]; Mao, Chengde ^[3]; Seeman, Nadrian C. ^[2]; Vecchioni, Simon ^[2]; ^[2]

New York Univ. (NYU), NY (United States); OSTI
New York Univ. (NYU), NY (United States)
Purdue Univ., West Lafayette, IN (United States)

Non-canonical interactions in DNA remain under-explored in DNA nanotechnology. Recently, many structures with non-canonical motifs have been discovered, notably a hexagonal arrangement of typically rhombohedral DNA tensegrity triangles that forms through non-canonical sticky end interactions. Here, in this study, we find a series of mechanisms to program a hexagonal arrangement using: the sticky end sequence; triangle edge torsional stress; and crystallization condition. We showcase cross-talking between Watson–Crick and non-canonical sticky ends in which the ratio between the two dictates segregation by crystal forms or combination into composite crystals. Finally, we develop a method for reconfiguring the long-range geometry of formed crystals from rhombohedral to hexagonal and vice versa. These data demonstrate fine control over non-canonical motifs and their topological self-assembly. This will vastly increase the programmability, functionality, and versatility of rationally designed DNA constructs.

View Accepted Manuscript (DOE)

Research Organization:: New York Univ. (NYU), NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC); US Department of the Navy, Office of Naval Research (ONR); National Science Foundation (NSF)

Grant/Contract Number:: SC0007991

OSTI ID:: 2419790

Alternate ID(s):: OSTI ID: 1922249

Journal Information:: Angewandte Chemie (International Edition), Journal Name: Angewandte Chemie (International Edition) Journal Issue: 6 Vol. 62; ISSN 1433-7851

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

DNA Logic Circuits for Multiple Tumor Cells Identification Using Intracellular MicroRNA Molecular Bispecific Recognition Yang, Qiqi; Yang, Fan; Dai, Wenhao Advanced Healthcare Materials, Vol. 10, Issue 21 https://doi.org/10.1002/adhm.202101130	journal	September 2021
Core–Shell and Layer‐by‐Layer Assembly of 3D DNA Crystals McNeil, Ronald; Paukstelis, Paul J. Advanced Materials, Vol. 29, Issue 28 https://doi.org/10.1002/adma.201701019	journal	May 2017
Powering ≈50 µm Motion by a Molecular Event in DNA Crystals Zheng, Mengxi; Li, Zhe; Zhang, Cuizheng Advanced Materials, Vol. 34, Issue 26 https://doi.org/10.1002/adma.202200441	journal	May 2022
Augmented DNA Nanoarchitectures: A Structural Library of 3D Self‐Assembling Tensegrity Triangle Variants Woloszyn, Karol; Vecchioni, Simon; Ohayon, Yoel P. Advanced Materials https://doi.org/10.1002/adma.202206876	journal	October 2022
An Organic Semiconductor Organized into 3D DNA Arrays by “Bottom-up” Rational Design Wang, Xiao; Sha, Ruojie; Kristiansen, Martin Angewandte Chemie, Vol. 129, Issue 23 https://doi.org/10.1002/ange.201700462	journal	May 2017
Self-Assembly of a 3D DNA Crystal Structure with Rationally Designed Six-Fold Symmetry Zhang, Fei; Simmons, Chad R.; Gates, Jade Angewandte Chemie, Vol. 130, Issue 38 https://doi.org/10.1002/ange.201807223	journal	August 2018
Modulating Self-Assembly of DNA Crystals with Rationally Designed Agents Zhao, Jiemin; Zhao, Yue; Li, Zhe Angewandte Chemie, Vol. 130, Issue 50 https://doi.org/10.1002/ange.201809757	journal	November 2018
A Self‐Assembled Rhombohedral DNA Crystal Scaffold with Tunable Cavity Sizes and High‐Resolution Structural Detail Simmons, Chad R.; MacCulloch, Tara; Zhang, Fei Angewandte Chemie, Vol. 132, Issue 42 https://doi.org/10.1002/ange.202005505	journal	August 2020
Reconfigurable Two‐Dimensional DNA Lattices: Static and Dynamic Angle Control Wang, Wen; Chen, Chunyu; Vecchioni, Simon Angewandte Chemie, Vol. 133, Issue 49 https://doi.org/10.1002/ange.202112487	journal	November 2021
Orienting an Organic Semiconductor into DNA 3D Arrays by Covalent Bonds Wang, Xiao; Deshmukh, Rahul; Sha, Ruojie Angewandte Chemie, Vol. 134, Issue 5 https://doi.org/10.1002/ange.202115155	journal	December 2021
An Organic Semiconductor Organized into 3D DNA Arrays by “Bottom-up” Rational Design Wang, Xiao; Sha, Ruojie; Kristiansen, Martin Angewandte Chemie International Edition, Vol. 56, Issue 23 https://doi.org/10.1002/anie.201700462	journal	May 2017
Self-Assembly of a 3D DNA Crystal Structure with Rationally Designed Six-Fold Symmetry Zhang, Fei; Simmons, Chad R.; Gates, Jade Angewandte Chemie International Edition, Vol. 57, Issue 38 https://doi.org/10.1002/anie.201807223	journal	August 2018
Modulating Self-Assembly of DNA Crystals with Rationally Designed Agents Zhao, Jiemin; Zhao, Yue; Li, Zhe Angewandte Chemie International Edition, Vol. 57, Issue 50 https://doi.org/10.1002/anie.201809757	journal	November 2018
A Self‐Assembled Rhombohedral DNA Crystal Scaffold with Tunable Cavity Sizes and High‐Resolution Structural Detail Simmons, Chad R.; MacCulloch, Tara; Zhang, Fei Angewandte Chemie International Edition, Vol. 59, Issue 42 https://doi.org/10.1002/anie.202005505	journal	August 2020
Reconfigurable Two‐Dimensional DNA Lattices: Static and Dynamic Angle Control Wang, Wen; Chen, Chunyu; Vecchioni, Simon Angewandte Chemie International Edition, Vol. 60, Issue 49 https://doi.org/10.1002/anie.202112487	journal	November 2021
Orienting an Organic Semiconductor into DNA 3D Arrays by Covalent Bonds Wang, Xiao; Deshmukh, Rahul; Sha, Ruojie Angewandte Chemie International Edition, Vol. 61, Issue 5 https://doi.org/10.1002/anie.202115155	journal	December 2021
Highly Symmetric, Self‐Assembling 3D DNA Crystals with Cubic and Trigonal Lattices Lu, Brandon; Vecchioni, Simon; Ohayon, Yoel P. Small https://doi.org/10.1002/smll.202205830	journal	November 2022
Nucleic acid junctions and lattices Seeman, Nadrian C. Journal of Theoretical Biology, Vol. 99, Issue 2 https://doi.org/10.1016/0022-5193(82)90002-9	journal	November 1982
Crystal Structure of a Continuous Three-Dimensional DNA Lattice Paukstelis, Paul J.; Nowakowski, Jacek; Birktoft, Jens J. Chemistry & Biology, Vol. 11, Issue 8 https://doi.org/10.1016/j.chembiol.2004.05.021	journal	August 2004
Self-Assembly of 3D DNA Crystals Containing a Torsionally Stressed Component Hernandez, Carina; Birktoft, Jens J.; Ohayon, Yoel P. Cell Chemical Biology, Vol. 24, Issue 11 https://doi.org/10.1016/j.chembiol.2017.08.018	journal	November 2017
Factors Controlling Persistent Needle Crystal Growth: The Importance of Dominant One-Dimensional Secondary Bonding, Stacked Structures, and van der Waals Contact Civati, Francesco; O’Malley, Ciaran; Erxleben, Andrea Crystal Growth & Design, Vol. 21, Issue 6 https://doi.org/10.1021/acs.cgd.1c00217	journal	May 2021
Crystal Defect Doping on Antiferromagnetic Topological Insulator Candidate EuMg₂Bi₂ Marshall, Madalynn; Xie, Weiwei The Journal of Physical Chemistry C, Vol. 126, Issue 1 https://doi.org/10.1021/acs.jpcc.1c08980	journal	December 2021
DNA Nanotechnology at 40 Seeman, Nadrian C. Nano Letters, Vol. 20, Issue 3 https://doi.org/10.1021/acs.nanolett.0c00325	journal	February 2020
Programming the Curvatures in Reconfigurable DNA Domino Origami by Using Asymmetric Units Wang, Dongfang; Yu, Lei; Ji, Bin Nano Letters, Vol. 20, Issue 11 https://doi.org/10.1021/acs.nanolett.0c03348	journal	October 2020
3D Hexagonal Arrangement of DNA Tensegrity Triangles Lu, Brandon; Vecchioni, Simon; Ohayon, Yoel P. ACS Nano, Vol. 15, Issue 10 https://doi.org/10.1021/acsnano.1c06963	journal	October 2021
Exciton Delocalization in a DNA-Templated Organic Semiconductor Dimer Assembly Wang, Xiao; Sha, Ruojie; Knowlton, William B. ACS Nano, Vol. 16, Issue 1 https://doi.org/10.1021/acsnano.1c09143	journal	January 2022
Impact of Heterogeneity and Lattice Bond Strength on DNA Triangle Crystal Growth Stahl, Evi; Praetorius, Florian; de Oliveira Mann, Carina C. ACS Nano, Vol. 10, Issue 10 https://doi.org/10.1021/acsnano.6b04787	journal	September 2016
Designing Higher Resolution Self-Assembled 3D DNA Crystals via Strand Terminus Modifications Ohayon, Yoel P.; Hernandez, Carina; Chandrasekaran, Arun Richard ACS Nano, Vol. 13, Issue 7 https://doi.org/10.1021/acsnano.9b02430	journal	June 2019
DNA Nanotechnology Based on i-Motif Structures Dong, Yuanchen; Yang, Zhongqiang; Liu, Dongsheng Accounts of Chemical Research, Vol. 47, Issue 6 https://doi.org/10.1021/ar500073a	journal	May 2014
Comparative Effects of Salt, Organic, and Polymer Precipitants on Protein Phase Behavior and Implications for Vapor Diffusion Dumetz, André C.; Chockla, Aaron M.; Kaler, Eric W. Crystal Growth & Design, Vol. 9, Issue 2 https://doi.org/10.1021/cg700956b	journal	February 2009
Tensegrity: Construction of Rigid DNA Triangles with Flexible Four-Arm DNA Junctions Liu, Dage; Wang, Mingsheng; Deng, Zhaoxiang Journal of the American Chemical Society, Vol. 126, Issue 8 https://doi.org/10.1021/ja031754r	journal	March 2004
A DNA Crystal Designed to Contain Two Molecules per Asymmetric Unit Wang, Tong; Sha, Ruojie; Birktoft, Jens Journal of the American Chemical Society, Vol. 132, Issue 44 https://doi.org/10.1021/ja104833t	journal	November 2010
DNA Crystals as Vehicles for Biocatalysis Geng, Chun; Paukstelis, Paul J. Journal of the American Chemical Society, Vol. 136, Issue 22 https://doi.org/10.1021/ja502356m	journal	May 2014
Programming DNA Self-Assembly by Geometry Zhang, Cuizheng; Zheng, Mengxi; Ohayon, Yoel P. Journal of the American Chemical Society, Vol. 144, Issue 19 https://doi.org/10.1021/jacs.2c02456	journal	May 2022
Self-Assembly of Molecule-like Nanoparticle Clusters Directed by DNA Nanocages Li, Yulin; Liu, Zhiyu; Yu, Guimei Journal of the American Chemical Society, Vol. 137, Issue 13 https://doi.org/10.1021/jacs.5b01196	journal	March 2015
Construction and Structure Determination of a Three-Dimensional DNA Crystal Simmons, Chad R.; Zhang, Fei; Birktoft, Jens J. Journal of the American Chemical Society, Vol. 138, Issue 31 https://doi.org/10.1021/jacs.6b06508	journal	August 2016
Tuning the Cavity Size and Chirality of Self-Assembling 3D DNA Crystals Simmons, Chad R.; Zhang, Fei; MacCulloch, Tara Journal of the American Chemical Society, Vol. 139, Issue 32 https://doi.org/10.1021/jacs.7b06485	journal	August 2017
DNA nanotechnology Seeman, Nadrian C.; Sleiman, Hanadi F. Nature Reviews Materials, Vol. 3, Issue 1 https://doi.org/10.1038/natrevmats.2017.68	journal	November 2017
Crystal structure of a junction between B-DNA and Z-DNA reveals two extruded bases Ha, Sung Chul; Lowenhaupt, Ky; Rich, Alexander Nature, Vol. 437, Issue 7062 https://doi.org/10.1038/nature04088	journal	October 2005
From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal Zheng, Jianping; Birktoft, Jens J.; Chen, Yi Nature, Vol. 461, Issue 7260 https://doi.org/10.1038/nature08274	journal	September 2009
DNA brick crystals with prescribed depths Ke, Yonggang; Ong, Luvena L.; Sun, Wei Nature Chemistry, Vol. 6, Issue 11 https://doi.org/10.1038/nchem.2083	journal	October 2014
A device that operates within a self-assembled 3D DNA crystal Hao, Yudong; Kristiansen, Martin; Sha, Ruojie Nature Chemistry, Vol. 9, Issue 8 https://doi.org/10.1038/nchem.2745	journal	March 2017
Nanocaged enzymes with enhanced catalytic activity and increased stability against protease digestion Zhao, Zhao; Fu, Jinglin; Dhakal, Soma Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10619	journal	February 2016
The biological applications of DNA nanomaterials: current challenges and future directions Ma, Wenjuan; Zhan, Yuxi; Zhang, Yuxin Signal Transduction and Targeted Therapy, Vol. 6, Issue 1 https://doi.org/10.1038/s41392-021-00727-9	journal	October 2021
The influence of Holliday junction sequence and dynamics on DNA crystal self-assembly Simmons, Chad R.; MacCulloch, Tara; Krepl, Miroslav Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-30779-6	journal	June 2022
Complex assemblies and crystals guided by DNA Jiang, Shuoxing; Zhang, Fei; Yan, Hao Nature Materials, Vol. 19, Issue 7 https://doi.org/10.1038/s41563-020-0719-3	journal	June 2020
Charge splitters and charge transport junctions based on guanine quadruplexes Sha, Ruojie; Xiang, Limin; Liu, Chaoren Nature Nanotechnology, Vol. 13, Issue 4 https://doi.org/10.1038/s41565-018-0070-x	journal	February 2018
Construction and characterization of metal ion-containing DNA nanowires for synthetic biology and nanotechnology Vecchioni, Simon; Capece, Mark C.; Toomey, Emily Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-43316-1	journal	May 2019
Spontaneous and frequent conformational dynamics induced by A…A mismatch in d(CAA)·d(TAG) duplex Ajjugal, Yogeeshwar; Tomar, Kripi; Rao, D. Krishna Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-82669-4	journal	February 2021
Supramolecular assembly of DNA on graphene nanoribbons Reuven, Darkeyah G.; Mihiri Shashikala, H. B.; Mandal, Sanjay Journal of Materials Chemistry B, Vol. 1, Issue 32 https://doi.org/10.1039/c3tb20397b	journal	January 2013
A DNA-based nanomechanical device with three robust states Chakraborty, Banani; Sha, Ruojie; Seeman, Nadrian C. Proceedings of the National Academy of Sciences, Vol. 105, Issue 45 https://doi.org/10.1073/pnas.0707681105	journal	November 2008
DNA-mediated engineering of multicomponent enzyme crystals Brodin, Jeffrey D.; Auyeung, Evelyn; Mirkin, Chad A. Proceedings of the National Academy of Sciences, Vol. 112, Issue 15 https://doi.org/10.1073/pnas.1503533112	journal	March 2015
Optimization of crystallization conditions for biological macromolecules McPherson, Alexander; Cudney, Bob Acta Crystallographica Section F Structural Biology Communications, Vol. 70, Issue 11 https://doi.org/10.1107/S2053230X14019670	journal	October 2014
The parallel-stranded d(CGA) duplex is a highly predictable structural motif with two conformationally distinct strands Luteran, Emily M.; Paukstelis, Paul J. Acta Crystallographica Section D Structural Biology, Vol. 78, Issue 3 https://doi.org/10.1107/S2059798322000304	journal	February 2022
Resilient three-dimensional ordered architectures assembled from nanoparticles by DNA Majewski, Pawel W.; Michelson, Aaron; Cordeiro, Marco A. L. Science Advances, Vol. 7, Issue 12 https://doi.org/10.1126/sciadv.abf0617	journal	March 2021
Hachimoji DNA and RNA: A genetic system with eight building blocks Hoshika, Shuichi; Leal, Nicole A.; Kim, Myong-Jung Science, Vol. 363, Issue 6429 https://doi.org/10.1126/science.aat0971	journal	February 2019
Bottom-Up Self-Assembly Based on DNA Nanotechnology Yan, Xuehui; Huang, Shujing; Wang, Yong Nanomaterials, Vol. 10, Issue 10 https://doi.org/10.3390/nano10102047	journal	October 2020

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