Three-dimensional structural dynamics of DNA origami Bennett linkages using individual-particle electron tomography

Lei, Dongsheng; Marras, Alexander E.; Liu, Jianfang; Huang, Chao-Min; Zhou, Lifeng; Castro, Carlos E.; Su, Hai-Jun; Ren, Gang

doi:10.1038/s41467-018-03018-0

Three-dimensional structural dynamics of DNA origami Bennett linkages using individual-particle electron tomography

Journal Article · Fri Feb 09 00:00:00 EST 2018 · Nature Communications

DOI:https://doi.org/10.1038/s41467-018-03018-0· OSTI ID:1433119

Lei, Dongsheng ^[1]; ^[2]; Liu, Jianfang ^[1]; Huang, Chao-Min ^[2]; Zhou, Lifeng ^[2]; ^[2]; Su, Hai-Jun ^[2]; Ren, Gang ^[1]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). The Molecular Foundry
The Ohio State Univ., Columbus, OH (United States). Dept. of Mechanical and Aerospace Engineering

Scaffolded DNA origami has proven to be a powerful and efficient technique to fabricate functional nanomachines by programming the folding of a single-stranded DNA template strand into three-dimensional (3D) nanostructures, designed to be precisely motion-controlled. Although two-dimensional (2D) imaging of DNA nanomachines using transmission electron microscopy and atomic force microscopy suggested these nanomachines are dynamic in 3D, geometric analysis based on 2D imaging was insufficient to uncover the exact motion in 3D. In this paper, we use the individual-particle electron tomography method and reconstruct 129 density maps from 129 individual DNA origami Bennett linkage mechanisms at ~6-14 nm resolution. The statistical analyses of these conformations lead to understanding the 3D structural dynamics of Bennett linkage mechanisms. Moreover, our effort provides experimental verification of a theoretical kinematics model of DNA origami, which can be used as feedback to improve the design and control of motion via optimized DNA sequences and routing.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Inst. of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); Univ. of California, San Francisco, CA (United States)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1433119

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 9; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (38)

EMAN: Semiautomated Software for High-Resolution Single-Particle Reconstructions Ludtke, Steven J.; Baldwin, Philip R.; Chiu, Wah Journal of Structural Biology, Vol. 128, Issue 1 https://doi.org/10.1006/jsbi.1999.4174	journal	December 1999
CTF determination and correction in electron cryotomography Fernández, J. J.; Li, S.; Crowther, R. A. Ultramicroscopy, Vol. 106, Issue 7 https://doi.org/10.1016/j.ultramic.2006.02.004	journal	May 2006
Characterizing the Motion of Jointed DNA Nanostructures Using a Coarse-Grained Model Sharma, Rahul; Schreck, John S.; Romano, Flavio ACS Nano, Vol. 11, Issue 12 https://doi.org/10.1021/acsnano.7b06470	journal	October 2016
A DNA-fuelled molecular machine made of DNA Yurke, Bernard; Turberfield, Andrew J.; Mills, Allen P. Nature, Vol. 406, Issue 6796 https://doi.org/10.1038/35020524	journal	August 2000
Structural basis of transfer between lipoproteins by cholesteryl ester transfer protein Zhang, Lei; Yan, Feng; Zhang, Shengli Nature Chemical Biology, Vol. 8, Issue 4 https://doi.org/10.1038/nchembio.796	journal	February 2012
Structural diversity of supercoiled DNA Irobalieva, Rossitza N.; Fogg, Jonathan M.; Catanese, Daniel J. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9440	journal	October 2015
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
HDL surface lipids mediate CETP binding as revealed by electron microscopy and molecular dynamics simulation Zhang, Meng; Charles, River; Tong, Huimin Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08741	journal	March 2015
Erratum: Corrigendum: 3D Structural Fluctuation of IgG1 Antibody Revealed by Individual Particle Electron Tomography Zhang, Xing; Zhang, Lei; Tong, Huimin Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep17919	journal	January 2016
Fully Mechanically Controlled Automated Electron Microscopic Tomography Liu, Jinxin; Li, Hongchang; Zhang, Lei Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29231	journal	July 2016
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
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
Programmable motion of DNA origami mechanisms Marras, Alexander E.; Zhou, Lifeng; Su, Hai-Jun Proceedings of the National Academy of Sciences, Vol. 112, Issue 3 https://doi.org/10.1073/pnas.1408869112	journal	January 2015
Molecular Architecture of Contactin-associated Protein-like 2 (CNTNAP2) and Its Interaction with Contactin 2 (CNTN2) Lu, Zhuoyang; Reddy, M. V. V. V. Sekhar; Liu, Jianfang Journal of Biological Chemistry, Vol. 291, Issue 46 https://doi.org/10.1074/jbc.m116.748236	journal	September 2016
Quantitative prediction of 3D solution shape and flexibility of nucleic acid nanostructures Kim, Do-Nyun; Kilchherr, Fabian; Dietz, Hendrik Nucleic Acids Research, Vol. 40, Issue 7 https://doi.org/10.1093/nar/gkr1173	journal	December 2011
An optimized negative-staining protocol of electron microscopy for apoE4•POPC lipoprotein Zhang, Lei; Song, James; Newhouse, Yvonne Journal of Lipid Research, Vol. 51, Issue 5 https://doi.org/10.1194/jlr.d002493	journal	November 2009
Polyhedral 3D structure of human plasma very low density lipoproteins by individual particle cryo-electron tomography ¹ Yu, Yadong; Kuang, Yu-Lin; Lei, Dongsheng Journal of Lipid Research, Vol. 57, Issue 10 https://doi.org/10.1194/jlr.m070375	journal	August 2016
IPET and FETR: Experimental Approach for Studying Molecular Structure Dynamics by Cryo-Electron Tomography of a Single-Molecule Structure Zhang, Lei; Ren, Gang PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0030249	journal	January 2012
Compensation of Missing Wedge Effects with Sequential Statistical Reconstruction in Electron Tomography Paavolainen, Lassi; Acar, Erman; Tuna, Uygar PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0108978	journal	October 2014
Computer Visualization of Three-Dimensional Image Data Using IMOD Kremer, James R.; Mastronarde, David N.; McIntosh, J. Richard Journal of Structural Biology, Vol. 116, Issue 1 https://doi.org/10.1006/jsbi.1996.0013	journal	January 1996
Linking Regions Between Helices in Bacteriorhodopsin Revealed Agard, David A.; Stroud, Robert M. Biophysical Journal, Vol. 37, Issue 3 https://doi.org/10.1016/S0006-3495(21)00378-7	journal	March 1982
UCSF tomography: An integrated software suite for real-time electron microscopic tomographic data collection, alignment, and reconstruction Zheng, Shawn Q.; Keszthelyi, Bettina; Branlund, Eric Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.06.005	journal	January 2007
A simple Fourier filter for suppression of the missing wedge ray artefacts in single-axis electron tomographic reconstructions Kováčik, Lubomír; Kerïeche, Sami; Höög, Johanna L. Journal of Structural Biology, Vol. 186, Issue 1 https://doi.org/10.1016/j.jsb.2014.02.004	journal	April 2014
ICON: 3D reconstruction with ‘missing-information’ restoration in biological electron tomography Deng, Yuchen; Chen, Yu; Zhang, Yan Journal of Structural Biology, Vol. 195, Issue 1 https://doi.org/10.1016/j.jsb.2016.04.004	journal	July 2016
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
Three-dimensional structural dynamics and fluctuations of DNA-nanogold conjugates by individual-particle electron tomography Zhang, Lei; Lei, Dongsheng; Smith, Jessica M. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11083	journal	March 2016
GENFIRE: A generalized Fourier iterative reconstruction algorithm for high-resolution 3D imaging Pryor, Alan; Yang, Yongsoo; Rana, Arjun Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-09847-1	journal	September 2017
Peptide-Conjugation Induced Conformational Changes in Human IgG1 Observed by Optimized Negative-Staining and Individual-Particle Electron Tomography Tong, Huimin; Zhang, Lei; Kaspar, Allan Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep01089	journal	January 2013
3D Structural Fluctuation of IgG1 Antibody Revealed by Individual Particle Electron Tomography Zhang, Xing; Zhang, Lei; Tong, Huimin Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep09803	journal	May 2015
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
Calsyntenin-3 Molecular Architecture and Interaction with Neurexin 1α Lu, Zhuoyang; Wang, Yun; Chen, Fang Journal of Biological Chemistry, Vol. 289, Issue 50 https://doi.org/10.1074/jbc.M114.606806	journal	October 2014
Molecular Architecture of Contactin-associated Protein-like 2 (CNTNAP2) and Its Interaction with Contactin 2 (CNTN2) Lu, Zhuoyang; Reddy, M. V. V. V. Sekhar; Liu, Jianfang Journal of Biological Chemistry, Vol. 291, Issue 46 https://doi.org/10.1074/jbc.M116.748236	journal	September 2016
Missing wedge computed tomography by iterative algorithm DIRECTT: MISSING WEDGE COMPUTED TOMOGRAPHY BY ITERATIVE ALGORITHM DIRECTT Kupsch, Andreas; Lange, Axel; Hentschel, Manfred P. Journal of Microscopy, Vol. 261, Issue 1 https://doi.org/10.1111/jmi.12313	journal	January 2016
An optimized negative-staining protocol of electron microscopy for apoE4•POPC lipoprotein Zhang, Lei; Song, James; Newhouse, Yvonne Journal of Lipid Research, Vol. 51, Issue 5 https://doi.org/10.1194/jlr.D002493	journal	November 2009
Morphology and structure of lipoproteins revealed by an optimized negative-staining protocol of electron microscopy Zhang, Lei; Song, James; Cavigiolio, Giorgio Journal of Lipid Research, Vol. 52, Issue 1 https://doi.org/10.1194/jlr.D010959	journal	October 2010
Polyhedral 3D structure of human plasma very low density lipoproteins by individual particle cryo-electron tomography ¹ Yu, Yadong; Kuang, Yu-Lin; Lei, Dongsheng Journal of Lipid Research, Vol. 57, Issue 10 https://doi.org/10.1194/jlr.M070375	journal	August 2016
Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. Roth, Ronelle; Hillmer, Stefan; Funaya, Charlotta Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52956	text	January 2019
Optimized Negative Staining: a High-throughput Protocol for Examining Small and Asymmetric Protein Structure by Electron Microscopy Rames, Matthew; Yu, Yadong; Ren, Gang Journal of Visualized Experiments, Issue 90 https://doi.org/10.3791/51087	journal	January 2014

Cited By (13)

Single-molecule 3D imaging of human plasma intermediate-density lipoproteins reveals a polyhedral structure Lei, Dongsheng; Yu, Yadong; Kuang, Yu-Lin Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1864, Issue 3 https://doi.org/10.1016/j.bbalip.2018.12.004	journal	March 2019
Measuring Internal Forces in Single-Stranded DNA: Application to a DNA Force Clamp Engel, Megan C.; Romano, Flavio; Louis, Ard. A. Journal of Chemical Theory and Computation, Vol. 16, Issue 12 https://doi.org/10.1021/acs.jctc.0c00286	journal	November 2020
Coarse-grained modelling of the structural properties of DNA origami Snodin, Benedict E. K.; Schreck, John S.; Romano, Flavio arXiv https://doi.org/10.48550/arxiv.1809.08430	text	January 2018
Paper Origami-Inspired Design and Actuation of DNA Nanomachines with Complex Motions Zhou, Lifeng; Marras, Alexander E.; Huang, Chao-Min Small, Vol. 14, Issue 47 https://doi.org/10.1002/smll.201802580	journal	October 2018
Imaging of Unstained DNA Origami Triangles with Electron Microscopy Londono‐Calderon, Alejandra; Hossen, Md Mir; Palo, Pierre E. Small Methods, Vol. 3, Issue 12 https://doi.org/10.1002/smtd.201900393	journal	August 2019
Low-cost, simple, and scalable self-assembly of DNA origami nanostructures Halley, Patrick D.; Patton, Randy A.; Chowdhury, Amjad Nano Research, Vol. 12, Issue 5 https://doi.org/10.1007/s12274-019-2384-x	journal	April 2019
Creating Linkage Permutations to Prevent Self-Intersection and Enable Deployable Networks of Thick-Origami Yellowhorse, Alden; Lang, Robert J.; Tolman, Kyler Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-31180-4	journal	August 2018
Single-Molecule 3D Images of “Hole-Hole” IgG1 Homodimers by Individual-Particle Electron Tomography Lei, Dongsheng; Liu, Jianfang; Liu, Hongbin Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-44978-7	journal	June 2019
Uncertainty quantification of a DNA origami mechanism using a coarse-grained model and kinematic variance analysis Huang, Chao-Min; Kucinic, Anjelica; Le, Jenny V. Nanoscale, Vol. 11, Issue 4 https://doi.org/10.1039/c8nr06377j	journal	January 2019
Dynamic DNA nanotechnology: toward functional nanoscale devices DeLuca, Marcello; Shi, Ze; Castro, Carlos E. Nanoscale Horizons, Vol. 5, Issue 2 https://doi.org/10.1039/c9nh00529c	journal	January 2020
Coarse-grained modelling of the structural properties of DNA origami Snodin, Benedict E. K.; Schreck, John S.; Romano, Flavio Nucleic Acids Research, Vol. 47, Issue 3 https://doi.org/10.1093/nar/gky1304	journal	January 2019
Developable mechanisms on developable surfaces Nelson, Todd G.; Zimmerman, Trent K.; Magleby, Spencer P. Science Robotics, Vol. 4, Issue 27 https://doi.org/10.1126/scirobotics.aau5171	journal	February 2019
IgG Antibody 3D Structures and Dynamics Jay, Jacob; Bray, Brinkley; Qi, Yaozhi Antibodies, Vol. 7, Issue 2 https://doi.org/10.3390/antib7020018	journal	April 2018

Similar Records

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
77 NANOSCIENCE AND NANOTECHNOLOGY
Cryoelectron tomography
DNA and RNA
Molecular machines and motors
Organizing materials with DNA

Three-dimensional structural dynamics of DNA origami Bennett linkages using individual-particle electron tomography

Citation Formats

References (38)

Cited By (13)

Similar Records

Related Subjects