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

Abstract

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.

Authors:

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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)

Publication Date:: Fri May 20 00:00:00 EDT 2022

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

Sponsoring Org.:: 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)

OSTI Identifier:: 1908739

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

Resource Type:: Accepted Manuscript

Journal Name:: Science Advances

Additional Journal Information:: Journal Volume: 8; Journal Issue: 20; Journal ID: ISSN 2375-2548

Publisher:: AAAS

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Wang, Xiao, Li, Shanshan, Jun, Hyungmin, John, Torsten, Zhang, Kaiming, Fowler, Hannah, Doye, Jonathan P.K., Chiu, Wah, and Bathe, Mark. Planar 2D wireframe DNA origami.  United States: N. p., 2022. 
Web.  doi:10.1126/sciadv.abn0039.

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                    Wang, Xiao, Li, Shanshan, Jun, Hyungmin, John, Torsten, Zhang, Kaiming, Fowler, Hannah, Doye, Jonathan P.K., Chiu, Wah, & Bathe, Mark. Planar 2D wireframe DNA origami.  United States.  https://doi.org/10.1126/sciadv.abn0039

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                    Wang, Xiao, Li, Shanshan, Jun, Hyungmin, John, Torsten, Zhang, Kaiming, Fowler, Hannah, Doye, Jonathan P.K., Chiu, Wah, and Bathe, Mark. Fri .  
"Planar 2D wireframe DNA origami".  United States.  https://doi.org/10.1126/sciadv.abn0039.  https://www.osti.gov/servlets/purl/1908739.

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@article{osti_1908739,

  title        = {Planar 2D wireframe DNA origami},

  author       = {Wang, Xiao and Li, Shanshan and Jun, Hyungmin and John, Torsten and Zhang, Kaiming and Fowler, Hannah and Doye, Jonathan P.K. and Chiu, Wah and Bathe, Mark},

  abstractNote = {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.},

  doi          = {10.1126/sciadv.abn0039},

  journal      = {Science Advances},

  number       = 20,

  volume       = 8,

  place        = {United States},

  year         = {Fri May 20 00:00:00 EDT 2022},

  month        = {Fri May 20 00:00:00 EDT 2022}

}

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Title: Planar 2D wireframe DNA origami

Abstract

Citation Formats

Understanding the Mechanical Properties of DNA Origami Tiles and Controlling the Kinetics of Their Folding and Unfolding Reconfiguration journal, May 2014

In situ structure and dynamics of DNA origami determined through molecular dynamics simulations journal, November 2013

Rapid prototyping of 3D DNA-origami shapes with caDNAno journal, June 2009

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DNA-Directed Artificial Light-Harvesting Antenna journal, August 2011

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Revealing the structures of megadalton-scale DNA complexes with nucleotide resolution journal, December 2020

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Gigadalton-scale shape-programmable DNA assemblies journal, December 2017

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DNA Origami Chromophore Scaffold Exploiting HomoFRET Energy Transport to Create Molecular Photonic Wires journal, March 2020

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Programmed coherent coupling in a synthetic DNA-based excitonic circuit journal, November 2017

Design, optimization and analysis of large DNA and RNA nanostructures through interactive visualization, editing and molecular simulation journal, May 2020

Autonomously designed free-form 2D DNA origami journal, January 2019

Advancing Biophysics Using DNA Origami journal, May 2021

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Diamond family of nanoparticle superlattices journal, February 2016

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Position Accuracy of Gold Nanoparticles on DNA Origami Structures Studied with Small-Angle X-ray Scattering journal, March 2018

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RELION: Implementation of a Bayesian approach to cryo-EM structure determination journal, December 2012

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Optimized Assembly and Covalent Coupling of Single-Molecule DNA Origami Nanoarrays journal, November 2014

Rapid prototyping of arbitrary 2D and 3D wireframe DNA origami journal, September 2021

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journal, November 2013

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journal, June 2009

Folding DNA into Twisted and Curved Nanoscale Shapes
journal, August 2009

TacoxDNA: A user‐friendly web server for simulations of complex DNA structures, from single strands to origami
journal, July 2019

DNA-Directed Artificial Light-Harvesting Antenna
journal, August 2011

Programming Light-Harvesting Efficiency Using DNA Origami
journal, March 2016

Coarse-grained modelling of the structural properties of DNA origami
journal, January 2019

DNA Origami as a Carrier for Circumvention of Drug Resistance
journal, August 2012

Revealing the structures of megadalton-scale DNA complexes with nucleotide resolution
journal, December 2020

Automated sequence design of 2D wireframe DNA origami with honeycomb edges
journal, November 2019

Ultra-thermostable RNA nanoparticles for solubilizing and high-yield loading of paclitaxel for breast cancer therapy
journal, February 2020

Gigadalton-scale shape-programmable DNA assemblies
journal, December 2017

Folding DNA to create nanoscale shapes and patterns
journal, March 2006

Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT
journal, February 2014

DNA Origami Chromophore Scaffold Exploiting HomoFRET Energy Transport to Create Molecular Photonic Wires
journal, March 2020

Capturing transient antibody conformations with DNA origami epitopes
journal, June 2020

Shape-Controlled Nanofabrication of Conducting Polymer on Planar DNA Templates
journal, June 2014

Single-Molecule Imaging of Dynamic Motions of Biomolecules in DNA Origami Nanostructures Using High-Speed Atomic Force Microscopy
journal, March 2014

Routing of individual polymers in designed patterns
journal, August 2015

Programmed coherent coupling in a synthetic DNA-based excitonic circuit
journal, November 2017

Design, optimization and analysis of large DNA and RNA nanostructures through interactive visualization, editing and molecular simulation
journal, May 2020

Autonomously designed free-form 2D DNA origami
journal, January 2019

Advancing Biophysics Using DNA Origami
journal, May 2021

Quantitative prediction of 3D solution shape and flexibility of nucleic acid nanostructures
journal, December 2011

Role of nanoscale antigen organization on B-cell activation probed using DNA origami
journal, June 2020

Optimal Determination of Particle Orientation, Absolute Hand, and Contrast Loss in Single-particle Electron Cryomicroscopy
journal, October 2003

Diamond family of nanoparticle superlattices
journal, February 2016

Design and Characterization of 1D Nanotubes and 2D Periodic Arrays Self-Assembled from DNA Multi-Helix Bundles
journal, January 2012

DNA Origami as an In Vivo Drug Delivery Vehicle for Cancer Therapy
journal, June 2014

Roadmap on biological pathways for electronic nanofabrication and materials
journal, January 2019

Engineering and mapping nanocavity emission via precision placement of DNA origami
journal, July 2016

Position Accuracy of Gold Nanoparticles on DNA Origami Structures Studied with Small-Angle X-ray Scattering
journal, March 2018

Construction of a DNA Origami Based Molecular Electro-optical Modulator
journal, February 2018

Photophysics of J-Aggregate-Mediated Energy Transfer on DNA
journal, November 2017

RELION: Implementation of a Bayesian approach to cryo-EM structure determination
journal, December 2012

Single-molecule chemical reactions on DNA origami
journal, February 2010

FRET efficiency and antenna effect in multi-color DNA origami-based light harvesting systems
journal, January 2017

Optimized Assembly and Covalent Coupling of Single-Molecule DNA Origami Nanoarrays
journal, November 2014

Rapid prototyping of arbitrary 2D and 3D wireframe DNA origami
journal, September 2021

Self-assembly of three-dimensional prestressed tensegrity structures from DNA
journal, June 2010

OxDNA.org: a public webserver for coarse-grained simulations of DNA and RNA nanostructures
journal, May 2021

Designer DNA architecture offers precise and multivalent spatial pattern-recognition for viral sensing and inhibition
journal, November 2019

DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response
journal, March 2012

Programming Self-Assembly of DNA Origami Honeycomb Two-Dimensional Lattices and Plasmonic Metamaterials
journal, June 2016

Dynamic and Progressive Control of DNA Origami Conformation by Modulating DNA Helicity with Chemical Adducts
journal, April 2016

A comparison between parallelization approaches in molecular dynamics simulations on GPUs
journal, October 2014

Dimensions and Global Twist of Single-Layer DNA Origami Measured by Small-Angle X-ray Scattering
journal, May 2018

A primer to scaffolded DNA origami
journal, February 2011

Effect of DNA Hairpin Loops on the Twist of Planar DNA Origami Tiles
journal, December 2011

Programming Structured DNA Assemblies to Probe Biophysical Processes
journal, May 2019

cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination
journal, February 2017

A Single Molecule Polyphenylene-Vinylene Photonic Wire
journal, May 2021

Self-Assembled DNA Photonic Wire for Long-Range Energy Transfer
journal, November 2008

Bioproduction of pure, kilobase-scale single-stranded DNA
journal, April 2019

Self-assembly of DNA into nanoscale three-dimensional shapes
journal, May 2009