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Title: Three-dimensional structural dynamics and fluctuations of DNA-nanogold conjugates by individual-particle electron tomography

Abstract

DNA base pairing has been used for many years to direct the arrangement of inorganic nanocrystals into small groupings and arrays with tailored optical and electrical properties. The control of DNA-mediated assembly depends crucially on a better understanding of three-dimensional structure of DNA-nanocrystal-hybridized building blocks. Existing techniques do not allow for structural determination of these flexible and heterogeneous samples. Here we report cryo-electron microscopy and negative-staining electron tomography approaches to image, and three-dimensionally reconstruct a single DNA-nanogold conjugate, an 84-bp double-stranded DNA with two 5-nm nanogold particles for potential substrates in plasmon-coupling experiments. By individual-particle electron tomography reconstruction, we obtain 14 density maps at ~ 2-nm resolution . Using these maps as constraints, we derive 14 conformations of dsDNA by molecular dynamics simulations. The conformational variation is consistent with that from liquid solution, suggesting that individual-particle electron tomography could be an expected approach to study DNA-assembling and flexible protein structure and dynamics.

Authors:
 [1];  [2];  [3];  [2];  [2];  [1];  [4];  [5];  [6];  [2]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Foundry; Xi'an Jiaotong Univ. (China). Dept. of Applied Physics
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Foundry
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Science Division; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry, Dept. of Materials Science
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Foundry; Xi'an Jiaotong Univ. (China). School of Life Science and Technology, Frontier Inst. of Science and Technology
  5. Xi'an Jiaotong Univ. (China). School of Life Science and Technology, Frontier Inst. of Science and Technology
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Science Division; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry, Dept. of Materials Science, Kavli Energy NanoScience Inst.
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1379251
Grant/Contract Number:  
AC02-05CH11231; DMR-1344290; R01GM104427
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; cryoelectron microscopy; electron microscopy; nanoparticles

Citation Formats

Zhang, Lei, Lei, Dongsheng, Smith, Jessica M., Zhang, Meng, Tong, Huimin, Zhang, Xing, Lu, Zhuoyang, Liu, Jiankang, Alivisatos, A. Paul, and Ren, Gang. Three-dimensional structural dynamics and fluctuations of DNA-nanogold conjugates by individual-particle electron tomography. United States: N. p., 2016. Web. doi:10.1038/ncomms11083.
Zhang, Lei, Lei, Dongsheng, Smith, Jessica M., Zhang, Meng, Tong, Huimin, Zhang, Xing, Lu, Zhuoyang, Liu, Jiankang, Alivisatos, A. Paul, & Ren, Gang. Three-dimensional structural dynamics and fluctuations of DNA-nanogold conjugates by individual-particle electron tomography. United States. doi:10.1038/ncomms11083.
Zhang, Lei, Lei, Dongsheng, Smith, Jessica M., Zhang, Meng, Tong, Huimin, Zhang, Xing, Lu, Zhuoyang, Liu, Jiankang, Alivisatos, A. Paul, and Ren, Gang. Wed . "Three-dimensional structural dynamics and fluctuations of DNA-nanogold conjugates by individual-particle electron tomography". United States. doi:10.1038/ncomms11083. https://www.osti.gov/servlets/purl/1379251.
@article{osti_1379251,
title = {Three-dimensional structural dynamics and fluctuations of DNA-nanogold conjugates by individual-particle electron tomography},
author = {Zhang, Lei and Lei, Dongsheng and Smith, Jessica M. and Zhang, Meng and Tong, Huimin and Zhang, Xing and Lu, Zhuoyang and Liu, Jiankang and Alivisatos, A. Paul and Ren, Gang},
abstractNote = {DNA base pairing has been used for many years to direct the arrangement of inorganic nanocrystals into small groupings and arrays with tailored optical and electrical properties. The control of DNA-mediated assembly depends crucially on a better understanding of three-dimensional structure of DNA-nanocrystal-hybridized building blocks. Existing techniques do not allow for structural determination of these flexible and heterogeneous samples. Here we report cryo-electron microscopy and negative-staining electron tomography approaches to image, and three-dimensionally reconstruct a single DNA-nanogold conjugate, an 84-bp double-stranded DNA with two 5-nm nanogold particles for potential substrates in plasmon-coupling experiments. By individual-particle electron tomography reconstruction, we obtain 14 density maps at ~ 2-nm resolution . Using these maps as constraints, we derive 14 conformations of dsDNA by molecular dynamics simulations. The conformational variation is consistent with that from liquid solution, suggesting that individual-particle electron tomography could be an expected approach to study DNA-assembling and flexible protein structure and dynamics.},
doi = {10.1038/ncomms11083},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {3}
}

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Works referenced in this record:

Organization of 'nanocrystal molecules' using DNA
journal, August 1996

  • Alivisatos, A. Paul; Johnsson, Kai P.; Peng, Xiaogang
  • Nature, Vol. 382, Issue 6592
  • DOI: 10.1038/382609a0

A DNA-based method for rationally assembling nanoparticles into macroscopic materials
journal, August 1996

  • Mirkin, Chad A.; Letsinger, Robert L.; Mucic, Robert C.
  • Nature, Vol. 382, Issue 6592, p. 607-609
  • DOI: 10.1038/382607a0

Selective Colorimetric Detection of Polynucleotides Based on the Distance-Dependent Optical Properties of Gold Nanoparticles
journal, August 1997


Immunofluorescent labeling of cancer marker Her2 and other cellular targets with semiconductor quantum dots
journal, December 2002

  • Wu, Xingyong; Liu, Hongjian; Liu, Jianquan
  • Nature Biotechnology, Vol. 21, Issue 1
  • DOI: 10.1038/nbt764

Two-Dimensional Nanoparticle Arrays Show the Organizational Power of Robust DNA Motifs
journal, July 2006

  • Zheng, Jiwen; Constantinou, Pamela E.; Micheel, Christine
  • Nano Letters, Vol. 6, Issue 7
  • DOI: 10.1021/nl060994c

The surface plasmon modes of self-assembled gold nanocrystals
journal, January 2012

  • Barrow, Steven J.; Wei, Xingzhan; Baldauf, Julia S.
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms2289

Isolation of Discrete Nanoparticle−DNA Conjugates for Plasmonic Applications
journal, April 2008

  • Claridge, Shelley A.; Liang, Huiyang W.; Basu, S. Roger
  • Nano Letters, Vol. 8, Issue 4
  • DOI: 10.1021/nl0802032

Programmable materials and the nature of the DNA bond
journal, February 2015


Structure of the TRPV1 ion channel determined by electron cryo-microscopy
journal, December 2013


Cryo-electron tomography of bacteria: progress, challenges and future prospects
journal, August 2009

  • Milne, Jacqueline L. S.; Subramaniam, Sriram
  • Nature Reviews Microbiology, Vol. 7, Issue 9
  • DOI: 10.1038/nrmicro2183

Magnetosomes Are Cell Membrane Invaginations Organized by the Actin-Like Protein MamK
journal, January 2006


Molecular structure determination by electron microscopy of unstained crystalline specimens
journal, May 1975


3D Structural Fluctuation of IgG1 Antibody Revealed by Individual Particle Electron Tomography
journal, May 2015

  • Zhang, Xing; Zhang, Lei; Tong, Huimin
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep09803

Calsyntenin-3 Molecular Architecture and Interaction with Neurexin 1α
journal, October 2014

  • Lu, Zhuoyang; Wang, Yun; Chen, Fang
  • Journal of Biological Chemistry, Vol. 289, Issue 50
  • DOI: 10.1074/jbc.M114.606806

An optimized negative-staining protocol of electron microscopy for apoE4•POPC lipoprotein
journal, November 2009

  • Zhang, Lei; Song, James; Newhouse, Yvonne
  • Journal of Lipid Research, Vol. 51, Issue 5
  • DOI: 10.1194/jlr.D002493

Negative staining and image classification — powerful tools in modern electron microscopy
journal, January 2004

  • Ohi, Melanie; Li, Ying; Cheng, Yifan
  • Biological Procedures Online, Vol. 6, Issue 1
  • DOI: 10.1251/bpo70

Morphology and structure of lipoproteins revealed by an optimized negative-staining protocol of electron microscopy
journal, October 2010

  • Zhang, Lei; Song, James; Cavigiolio, Giorgio
  • Journal of Lipid Research, Vol. 52, Issue 1
  • DOI: 10.1194/jlr.D010959

Structural basis of transfer between lipoproteins by cholesteryl ester transfer protein
journal, February 2012

  • Zhang, Lei; Yan, Feng; Zhang, Shengli
  • Nature Chemical Biology, Vol. 8, Issue 4
  • DOI: 10.1038/nchembio.796

3D Motion of DNA-Au Nanoconjugates in Graphene Liquid Cell Electron Microscopy
journal, August 2013

  • Chen, Qian; Smith, Jessica M.; Park, Jungwon
  • Nano Letters, Vol. 13, Issue 9
  • DOI: 10.1021/nl402694n

Probing the Conformational Distributions of Subpersistence Length DNA
journal, September 2009

  • Mastroianni, Alexander J.; Sivak, David A.; Geissler, Phillip L.
  • Biophysical Journal, Vol. 97, Issue 5
  • DOI: 10.1016/j.bpj.2009.06.031

All-atom empirical force field for nucleic acids: II. Application to molecular dynamics simulations of DNA and RNA in solution
journal, January 2000


Single-molecule studies of DNA mechanics
journal, June 2000


Ten years of tension: single-molecule DNA mechanics
journal, January 2003

  • Bustamante, Carlos; Bryant, Zev; Smith, Steven B.
  • Nature, Vol. 421, Issue 6921
  • DOI: 10.1038/nature01405

NAMD2: Greater Scalability for Parallel Molecular Dynamics
journal, May 1999

  • Kalé, Laxmikant; Skeel, Robert; Bhandarkar, Milind
  • Journal of Computational Physics, Vol. 151, Issue 1
  • DOI: 10.1006/jcph.1999.6201

VMD: Visual molecular dynamics
journal, February 1996


Method for the Observation of Macromolecules with the Electron Microscope Illustrated with Micrographs of DNA
journal, September 1956

  • Hall, Cecil E.
  • The Journal of Biophysical and Biochemical Cytology, Vol. 2, Issue 5
  • DOI: 10.1083/jcb.2.5.625

Electron microscopy of unbroken DNA molecules
journal, June 1961


ELECTRON STAINS: I. Chemical Studies on the Interaction of DNA with Uranyl Salts
journal, July 1961


Electron stains II: Electron microscopic studies on the visibility of stained DNA molecules
journal, December 1961


DNA Base Identification by Electron Microscopy
journal, October 2012

  • Bell, David C.; Thomas, W. Kelley; Murtagh, Katelyn M.
  • Microscopy and Microanalysis, Vol. 18, Issue 5
  • DOI: 10.1017/S1431927612012615

Electron tomography at 2.4-ångström resolution
journal, March 2012

  • Scott, M. C.; Chen, Chien-Chun; Mecklenburg, Matthew
  • Nature, Vol. 483, Issue 7390
  • DOI: 10.1038/nature10934

HDL surface lipids mediate CETP binding as revealed by electron microscopy and molecular dynamics simulation
journal, March 2015

  • Zhang, Meng; Charles, River; Tong, Huimin
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep08741

Assessment of the Validity of the Double Superhelix Model for Reconstituted High Density Lipoproteins: A COMBINED COMPUTATIONAL-EXPERIMENTAL APPROACH
journal, October 2010

  • Jones, Martin K.; Zhang, Lei; Catte, Andrea
  • Journal of Biological Chemistry, Vol. 285, Issue 52
  • DOI: 10.1074/jbc.M110.187799

EMAN: Semiautomated Software for High-Resolution Single-Particle Reconstructions
journal, December 1999

  • Ludtke, Steven J.; Baldwin, Philip R.; Chiu, Wah
  • Journal of Structural Biology, Vol. 128, Issue 1
  • DOI: 10.1006/jsbi.1999.4174

Computer Visualization of Three-Dimensional Image Data Using IMOD
journal, January 1996

  • Kremer, James R.; Mastronarde, David N.; McIntosh, J. Richard
  • Journal of Structural Biology, Vol. 116, Issue 1
  • DOI: 10.1006/jsbi.1996.0013

CTF determination and correction in electron cryotomography
journal, May 2006


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
  • DOI: 10.1002/jcc.20084

Targeted molecular dynamics: A new approach for searching pathways of conformational transitions
journal, June 1994


Easy DNA Modeling and More with GraphiteLifeExplorer
journal, January 2013


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
  • DOI: 10.1063/1.470648

Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems
journal, June 1993

  • Darden, Tom; York, Darrin; Pedersen, Lee
  • The Journal of Chemical Physics, Vol. 98, Issue 12
  • DOI: 10.1063/1.464397

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