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

Jun, Hyungmin; Wang, Xiao; Parsons, Molly F.; Bricker, William  P.; John, Torsten; Li, Shanshan; Jackson, Steve; Chiu, Wah; Bathe, Mark

doi:10.1093/nar/gkab762

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

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

DOI:https://doi.org/10.1093/nar/gkab762· OSTI ID:1873376

^[1]; ^[2]; ^[2]; ^[2]; ^[2]; ^[3]; Jackson, Steve ^[2]; Chiu, Wah ^[4]; ^[2]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Jeonbuk National University, Jeonju (Korea, Republic of)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Stanford Univ., CA (United States)
Stanford Univ., CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)

Wireframe DNA origami assemblies can now be programmed automatically from the top-down using simple wireframe target geometries, or meshes, in 2D and 3D, using either rigid, six-helix bundle (6HB) or more compliant, two-helix bundle (DX) edges. While these assemblies have numerous applications in nanoscale materials fabrication due to their nanoscale spatial addressability and high degree of customization, no easy-to-use graphical user interface software yet exists to deploy these algorithmic approaches within a single, standalone interface. Further, top-down sequence design of 3D DX-based objects previously enabled by DAEDALUS was limited to discrete edge lengths and uniform vertex angles, limiting the scope of objects that can be designed. Here, we introduce the open-source software package ATHENA with a graphical user interface that automatically renders single-stranded DNA scaffold routing and staple strand sequences for any target wireframe DNA origami using DX or 6HB edges, including irregular, asymmetric DX-based polyhedra with variable edge lengths and vertices demonstrated experimentally, which significantly expands the set of possible 3D DNA-based assemblies that can be designed. ATHENA also enables external editing of sequences using caDNAno, demonstrated using asymmetric nanoscale positioning of gold nanoparticles, as well as providing atomic-level models for molecular dynamics, coarse-grained dynamics with oxDNA, and other computational chemistry simulation approaches.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: National Science Foundation (NSF); US Army Research Office (ARO); US Department of the Navy, Office of Naval Research (ONR); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1873376

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 18 Vol. 49; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

All-atom empirical force field for nucleic acids: II. Application to molecular dynamics simulations of DNA and RNA in solution MacKerell, Alexander D.; Banavali, Nilesh K. Journal of Computational Chemistry, Vol. 21, Issue 2 https://doi.org/10.1002/(SICI)1096-987X(20000130)21:2<105::AID-JCC3>3.0.CO;2-P	journal	January 2000
All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data Foloppe, Nicolas; MacKerell, Jr., Alexander D. Journal of Computational Chemistry, Vol. 21, Issue 2 https://doi.org/10.1002/(SICI)1096-987X(20000130)21:2<86::AID-JCC2>3.0.CO;2-G	journal	January 2000
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
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
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
A standard reference frame for the description of nucleic acid base-pair geometry 1 1Edited by P. E. Wright 2 2This is a document of the Nomenclature Committee of IUBMB (NC-IUBMB)/IUPAC-IUBMB Joint Commission on Biochemical Nomenclature (JCBN), whose members are R. Cammack (chairman), A. Bairoch, H.M. Berman, S. Boyce, C.R. Cantor, K. Elliott, D. Horton, M. Kanehisa, A. Kotyk, G.P. Moss, N. Sharon and K.F. Tipton. Olson, Wilma K.; Bansal, Manju; Burley, Stephen K. Journal of Molecular Biology, Vol. 313, Issue 1 https://doi.org/10.1006/jmbi.2001.4987	journal	October 2001
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
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
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
Assessing the Current State of Amber Force Field Modifications for DNA Galindo-Murillo, Rodrigo; Robertson, James C.; Zgarbová, Marie Journal of Chemical Theory and Computation, Vol. 12, Issue 8 https://doi.org/10.1021/acs.jctc.6b00186	journal	July 2016
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
Rapid Computational Analysis of DNA Origami Assemblies at Near-Atomic Resolution Lee, Jae Young; Lee, Jae Gyung; Yun, Giseok ACS Nano, Vol. 15, Issue 1 https://doi.org/10.1021/acsnano.0c07717	journal	January 2021
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
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
Biotechnological mass production of DNA origami Praetorius, Florian; Kick, Benjamin; Behler, Karl L. Nature, Vol. 552, Issue 7683 https://doi.org/10.1038/nature24650	journal	December 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
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
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
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
In vitro synthesis of gene-length single-stranded DNA Veneziano, Rémi; Shepherd, Tyson R.; Ratanalert, Sakul Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-24677-5	journal	April 2018
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
Structural, mechanical, and thermodynamic properties of a coarse-grained DNA model Ouldridge, Thomas E.; Louis, Ard A.; Doye, Jonathan P. K. The Journal of Chemical Physics, Vol. 134, Issue 8 https://doi.org/10.1063/1.3552946	journal	February 2011
Sequence-dependent thermodynamics of a coarse-grained DNA model Šulc, Petr; Romano, Flavio; Ouldridge, Thomas E. The Journal of Chemical Physics, Vol. 137, Issue 13 https://doi.org/10.1063/1.4754132	journal	October 2012
Introducing improved structural properties and salt dependence into a coarse-grained model of DNA Snodin, Benedict E. K.; Randisi, Ferdinando; Mosayebi, Majid The Journal of Chemical Physics, Vol. 142, Issue 23 https://doi.org/10.1063/1.4921957	journal	June 2015
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
ProDy: Protein Dynamics Inferred from Theory and Experiments Bakan, A.; Meireles, L. M.; Bahar, I. Bioinformatics, Vol. 27, Issue 11, p. 1575-1577 https://doi.org/10.1093/bioinformatics/btr168	journal	April 2011
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
MrDNA: a multi-resolution model for predicting the structure and dynamics of DNA systems Maffeo, Christopher; Aksimentiev, Aleksei Nucleic Acids Research, Vol. 48, Issue 9 https://doi.org/10.1093/nar/gkaa200	journal	March 2020
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
Adenita: interactive 3D modelling and visualization of DNA nanostructures de Llano, Elisa; Miao, Haichao; Ahmadi, Yasaman Nucleic Acids Research, Vol. 48, Issue 15 https://doi.org/10.1093/nar/gkaa593	journal	July 2020
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
3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures Lu, X. -J. Nucleic Acids Research, Vol. 31, Issue 17 https://doi.org/10.1093/nar/gkg680	journal	September 2003
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
De novo reconstruction of DNA origami structures through atomistic molecular dynamics simulation Maffeo, Christopher; Yoo, Jejoong; Aksimentiev, Aleksei Nucleic Acids Research, Vol. 44, Issue 7 https://doi.org/10.1093/nar/gkw155	journal	March 2016
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
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
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
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
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

Similar Records

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

Journal Article · Wed Jan 02 19:00:00 EST 2019 · ACS Nano · OSTI ID:1507153

Planar 2D wireframe DNA origami

Journal Article · Thu May 19 20:00:00 EDT 2022 · Science Advances · OSTI ID:1908739

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
computational methods

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

Citation Formats

References (43)

Similar Records

Related Subjects