Altering DNA-Programmable Colloidal Crystallization Paths by Modulating Particle Repulsion
Abstract
Colloidal crystal engineering with DNA can be used to realize precise control over nanoparticle (NP) arrangement. Here, we investigate a case of DNA-based assembly where the properties of DNA as a polyelectrolyte brush are employed to alter a hybridization-driven NP crystallization pathway. Using the co-assembly of DNA-conjugated proteins and spherical gold 2 nanoparticles (AuNPs) as a model system, we explore how steric repulsion between non-complementary, neighboring DNA-NPs due to overlapping DNA shells can influence their ligand-directed behavior. Specifically, our experimental data coupled with coarse-grained molecular dynamics (MD) simulations reveal that by changing factors related to NP repulsion, two structurally distinct outcomes can be achieved. When steric repulsion between DNA-AuNPs is significantly greater than that between DNA-proteins, a lower packing density crystal lattice is favored over the structure that is predicted by design rules based on DNA-hybridization considerations alone. This is enabled by the large difference in DNA density on AuNPs versus proteins and can be tuned by modulating the flexibility, and thus conformational entropy, of the DNA on the constituent particles. At intermediate ligand flexibility, the crystallization pathways are energetically similar and the structural outcome can be adjusted using the density of DNA duplexes on DNA-AuNPs and by screening themore »
- Authors:
-
- X-Ray Science Division, Argonne National Laboratory, 9700 S. Cass Avenue, Argonne, Illinois 60439, United States
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Bio-Inspired Energy Science (CBES)
- Sponsoring Org.:
- US Department of the Navy, Office of Naval Research (ONR); Air Force Research Laboratory (AFRL) - Air Force Office of Scientific Research (AFOSR); USDOE Office of Science - Energy Frontier Research Center - Center for Bio-Inspired Energy Science (CBES); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); Natural Sciences and Engineering Research Council of Canada (NSERC)
- OSTI Identifier:
- 1395868
- DOE Contract Number:
- AC02-06CH11357
- Resource Type:
- Journal Article
- Journal Name:
- Nano Letters
- Additional Journal Information:
- Journal Volume: 17; Journal Issue: 8; Journal ID: ISSN 1530-6984
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- DNA; colloidal crystals; nanomaterials; nanoparticle superlattice; protein assembly; self-assembly
Citation Formats
Wang, Mary X., Brodin, Jeffrey D., Millan, Jaime A., Seo, Soyoung E., Girard, Martin, Olvera de la Cruz, Monica, Lee, Byeongdu, and Mirkin, Chad A. Altering DNA-Programmable Colloidal Crystallization Paths by Modulating Particle Repulsion. United States: N. p., 2017.
Web. doi:10.1021/acs.nanolett.7b02502.
Wang, Mary X., Brodin, Jeffrey D., Millan, Jaime A., Seo, Soyoung E., Girard, Martin, Olvera de la Cruz, Monica, Lee, Byeongdu, & Mirkin, Chad A. Altering DNA-Programmable Colloidal Crystallization Paths by Modulating Particle Repulsion. United States. https://doi.org/10.1021/acs.nanolett.7b02502
Wang, Mary X., Brodin, Jeffrey D., Millan, Jaime A., Seo, Soyoung E., Girard, Martin, Olvera de la Cruz, Monica, Lee, Byeongdu, and Mirkin, Chad A. 2017.
"Altering DNA-Programmable Colloidal Crystallization Paths by Modulating Particle Repulsion". United States. https://doi.org/10.1021/acs.nanolett.7b02502.
@article{osti_1395868,
title = {Altering DNA-Programmable Colloidal Crystallization Paths by Modulating Particle Repulsion},
author = {Wang, Mary X. and Brodin, Jeffrey D. and Millan, Jaime A. and Seo, Soyoung E. and Girard, Martin and Olvera de la Cruz, Monica and Lee, Byeongdu and Mirkin, Chad A.},
abstractNote = {Colloidal crystal engineering with DNA can be used to realize precise control over nanoparticle (NP) arrangement. Here, we investigate a case of DNA-based assembly where the properties of DNA as a polyelectrolyte brush are employed to alter a hybridization-driven NP crystallization pathway. Using the co-assembly of DNA-conjugated proteins and spherical gold 2 nanoparticles (AuNPs) as a model system, we explore how steric repulsion between non-complementary, neighboring DNA-NPs due to overlapping DNA shells can influence their ligand-directed behavior. Specifically, our experimental data coupled with coarse-grained molecular dynamics (MD) simulations reveal that by changing factors related to NP repulsion, two structurally distinct outcomes can be achieved. When steric repulsion between DNA-AuNPs is significantly greater than that between DNA-proteins, a lower packing density crystal lattice is favored over the structure that is predicted by design rules based on DNA-hybridization considerations alone. This is enabled by the large difference in DNA density on AuNPs versus proteins and can be tuned by modulating the flexibility, and thus conformational entropy, of the DNA on the constituent particles. At intermediate ligand flexibility, the crystallization pathways are energetically similar and the structural outcome can be adjusted using the density of DNA duplexes on DNA-AuNPs and by screening the Coulomb potential between them. Such lattices are shown to undergo dynamic reorganization upon changing salt concentration. These data help elucidate the structural considerations necessary for understanding repulsive forces in DNA-assembly and lay the groundwork for using them to increase architectural diversity in engineering colloidal crystals.},
doi = {10.1021/acs.nanolett.7b02502},
url = {https://www.osti.gov/biblio/1395868},
journal = {Nano Letters},
issn = {1530-6984},
number = 8,
volume = 17,
place = {United States},
year = {Fri Jul 21 00:00:00 EDT 2017},
month = {Fri Jul 21 00:00:00 EDT 2017}
}
Works referenced in this record:
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
Structural diversity in binary nanoparticle superlattices
journal, January 2006
- Shevchenko, Elena V.; Talapin, Dmitri V.; Kotov, Nicholas A.
- Nature, Vol. 439, Issue 7072, p. 55-59
The role of interparticle and external forces in nanoparticle assembly
journal, July 2008
- Min, Younjin; Akbulut, Mustafa; Kristiansen, Kai
- Nature Materials, Vol. 7, Issue 7
Nanoscale Forces and Their Uses in Self-Assembly
journal, July 2009
- Bishop, Kyle J. M.; Wilmer, Christopher E.; Soh, Siowling
- Small, Vol. 5, Issue 14
Templated Techniques for the Synthesis and Assembly of Plasmonic Nanostructures
journal, June 2011
- Jones, Matthew R.; Osberg, Kyle D.; Macfarlane, Robert J.
- Chemical Reviews, Vol. 111, Issue 6
From Artificial Atoms to Nanocrystal Molecules: Preparation and Properties of More Complex Nanostructures
journal, March 2010
- Choi, Charina L.; Alivisatos, A. Paul
- Annual Review of Physical Chemistry, Vol. 61, Issue 1
Self-Assembly of Colloidal Nanocrystals: From Intricate Structures to Functional Materials
journal, August 2016
- Boles, Michael A.; Engel, Michael; Talapin, Dmitri V.
- Chemical Reviews, Vol. 116, Issue 18
Modulating the Bond Strength of DNA–Nanoparticle Superlattices
journal, December 2015
- Seo, Soyoung E.; Wang, Mary X.; Shade, Chad M.
- ACS Nano, Vol. 10, Issue 2
Epitaxy: Programmable Atom Equivalents Versus Atoms
journal, December 2016
- Wang, Mary X.; Seo, Soyoung E.; Gabrys, Paul A.
- ACS Nano, Vol. 11, Issue 1
Nanoparticle Superlattice Engineering with DNA
journal, October 2011
- Macfarlane, R. J.; Lee, B.; Jones, M. R.
- Science, Vol. 334, Issue 6053, p. 204-208
DNA-programmable nanoparticle crystallization
journal, January 2008
- Park, Sung Yong; Lytton-Jean, Abigail K. R.; Lee, Byeongdu
- Nature, Vol. 451, Issue 7178, p. 553-556
DNA-guided crystallization of colloidal nanoparticles
journal, January 2008
- Nykypanchuk, Dmytro; Maye, Mathew M.; van der Lelie, Daniel
- Nature, Vol. 451, Issue 7178, p. 549-552
Programmable materials and the nature of the DNA bond
journal, February 2015
- Jones, M. R.; Seeman, N. C.; Mirkin, C. A.
- Science, Vol. 347, Issue 6224
A general approach to DNA-programmable atom equivalents
journal, May 2013
- Zhang, Chuan; Macfarlane, Robert J.; Young, Kaylie L.
- Nature Materials, Vol. 12, Issue 8
A general strategy for the DNA-mediated self-assembly of functional nanoparticles into heterogeneous systems
journal, October 2013
- Zhang, Yugang; Lu, Fang; Yager, Kevin G.
- Nature Nanotechnology, Vol. 8, Issue 11
Nucleic Acid-Modified Nanostructures as Programmable Atom Equivalents: Forging a New “Table of Elements”
journal, May 2013
- Macfarlane, Robert J.; O'Brien, Matthew N.; Petrosko, Sarah Hurst
- Angewandte Chemie International Edition, Vol. 52, Issue 22
Life as a Nanoscale Phenomenon
journal, July 2008
- Mann, Stephen
- Angewandte Chemie International Edition, Vol. 47, Issue 29
Self-Assembly of a Tetrahedral Lectin into Predesigned Diamondlike Protein Crystals
journal, August 1999
- Dotan, Nir; Arad, Dorit; Frolow, Felix
- Angewandte Chemie International Edition, Vol. 38, Issue 16
Nanohedra: Using symmetry to design self assembling protein cages, layers, crystals, and filaments
journal, February 2001
- Padilla, J. E.; Colovos, C.; Yeates, T. O.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 5
Self-Assembly of Proteins into Designed Networks
journal, October 2003
- Ringler, P.
- Science, Vol. 302, Issue 5642
In vitro self-assembly of tailorable nanotubes from a simple protein building block
journal, February 2008
- Ballister, E. R.; Lai, A. H.; Zuckermann, R. N.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 10
DNA-controlled assembly of a NaTl lattice structure from gold nanoparticles and protein nanoparticles
journal, October 2010
- Cigler, Petr; Lytton-Jean, Abigail K. R.; Anderson, Daniel G.
- Nature Materials, Vol. 9, Issue 11, p. 918-922
Generation of protein lattices by fusing proteins with matching rotational symmetry
journal, July 2011
- Sinclair, John C.; Davies, Karen M.; Vénien-Bryan, Catherine
- Nature Nanotechnology, Vol. 6, Issue 9
Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays
journal, March 2012
- Brodin, Jeffrey D.; Ambroggio, X. I.; Tang, Chunyan
- Nature Chemistry, Vol. 4, Issue 5
Computational design of a protein crystal
journal, April 2012
- Lanci, C. J.; MacDermaid, C. M.; Kang, S. -g.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 19
Design of ordered two-dimensional arrays mediated by noncovalent protein-protein interfaces
journal, June 2015
- Gonen, S.; DiMaio, F.; Gonen, T.
- Science, Vol. 348, Issue 6241
Electrostatic assembly of binary nanoparticle superlattices using protein cages
journal, December 2012
- Kostiainen, Mauri A.; Hiekkataipale, Panu; Laiho, Ari
- Nature Nanotechnology, Vol. 8, Issue 1
Protein crystalline frameworks with controllable interpenetration directed by dual supramolecular interactions
journal, August 2014
- Sakai, Fuji; Yang, Guang; Weiss, Manfred S.
- Nature Communications, Vol. 5, Issue 1
Designed, Helical Protein Nanotubes with Variable Diameters from a Single Building Block
journal, August 2015
- Brodin, Jeffrey D.; Smith, Sarah J.; Carr, Jessica R.
- Journal of the American Chemical Society, Vol. 137, Issue 33
Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals
journal, May 2016
- Suzuki, Yuta; Cardone, Giovanni; Restrepo, David
- Nature, Vol. 533, Issue 7603
DNA-mediated engineering of multicomponent enzyme crystals
journal, March 2015
- Brodin, Jeffrey D.; Auyeung, Evelyn; Mirkin, Chad A.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 15
Modulating Nanoparticle Superlattice Structure Using Proteins with Tunable Bond Distributions
journal, January 2017
- McMillan, Janet R.; Brodin, Jeffrey D.; Millan, Jaime A.
- Journal of the American Chemical Society, Vol. 139, Issue 5
Establishing the Design Rules for DNA-Mediated Programmable Colloidal Crystallization
journal, May 2010
- Macfarlane, Robert J.; Jones, Matthew R.; Senesi, Andrew J.
- Angewandte Chemie, Vol. 122, Issue 27, p. 4693-4696
Morphological Diversity of DNA-Colloidal Self-Assembly
journal, September 2002
- Tkachenko, Alexei V.
- Physical Review Letters, Vol. 89, Issue 14
The Significance of Multivalent Bonding Motifs and “Bond Order” in DNA-Directed Nanoparticle Crystallization
journal, May 2016
- Thaner, Ryan V.; Eryazici, Ibrahim; Macfarlane, Robert J.
- Journal of the American Chemical Society, Vol. 138, Issue 19
Electrostatic Self-Assembly of Binary Nanoparticle Crystals with a Diamond-Like Lattice
journal, February 2006
- Kalsin, A. M.; Fialkowski, M.; Paszewski, M.
- Science, Vol. 312, Issue 5772, p. 420-424
A Strain-Promoted [3 + 2] Azide−Alkyne Cycloaddition for Covalent Modification of Biomolecules in Living Systems
journal, November 2004
- Agard, Nicholas J.; Prescher, Jennifer A.; Bertozzi, Carolyn R.
- Journal of the American Chemical Society, Vol. 126, Issue 46
Visualizing Metabolically Labeled Glycoconjugates of Living Cells by Copper-Free and Fast Huisgen Cycloadditions
journal, March 2008
- Ning, Xinghai; Guo, Jun; Wolfert, Margreet A.
- Angewandte Chemie International Edition, Vol. 47, Issue 12
DNA-mediated nanoparticle crystallization into Wulff polyhedra
journal, November 2013
- Auyeung, Evelyn; Li, Ting I. N. G.; Senesi, Andrew J.
- Nature, Vol. 505, Issue 7481
Modeling the Crystallization of Spherical Nucleic Acid Nanoparticle Conjugates with Molecular Dynamics Simulations
journal, April 2012
- Li, Ting I. N. G.; Sknepnek, Rastko; Macfarlane, Robert J.
- Nano Letters, Vol. 12, Issue 5
Dynamics and Statics of DNA-Programmable Nanoparticle Self-Assembly and Crystallization
journal, May 2011
- Knorowski, C.; Burleigh, S.; Travesset, A.
- Physical Review Letters, Vol. 106, Issue 21
Entropy-Driven Crystallization Behavior in DNA-Mediated Nanoparticle Assembly
journal, June 2015
- Thaner, Ryan V.; Kim, Youngeun; Li, Ting I. N. G.
- Nano Letters, Vol. 15, Issue 8
Strong scaling of general-purpose molecular dynamics simulations on GPUs
journal, July 2015
- Glaser, Jens; Nguyen, Trung Dac; Anderson, Joshua A.
- Computer Physics Communications, Vol. 192
Exploring the zone of anisotropy and broken symmetries in DNA-mediated nanoparticle crystallization
journal, September 2016
- O’Brien, Matthew N.; Girard, Martin; Lin, Hai-Xin
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 38
DNA-Driven Assembly: From Polyhedral Nanoparticles to Proteins
journal, July 2017
- Girard, Martin; Millan, Jaime A.; Olvera de la Cruz, Monica
- Annual Review of Materials Research, Vol. 47, Issue 1
Small-angle scattering of particle assemblies
journal, July 2015
- Senesi, Andrew J.; Lee, Byeongdu
- Journal of Applied Crystallography, Vol. 48, Issue 4
Small Angle X-ray Scattering for Nanoparticle Research
journal, April 2016
- Li, Tao; Senesi, Andrew J.; Lee, Byeongdu
- Chemical Reviews, Vol. 116, Issue 18
Interactions of highly charged colloidal cylinders with applications to double-stranded DNA
journal, July 1977
- Stigter, Dirk
- Biopolymers, Vol. 16, Issue 7
Probability of DNA knotting and the effective diameter of the DNA double helix.
journal, June 1993
- Rybenkov, V. V.; Cozzarelli, N. R.; Vologodskii, A. V.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 11
Works referencing / citing this record:
Kernel Homology in Gold Nanoclusters
journal, October 2018
- Zhuang, Shengli; Liao, Lingwen; Yuan, Jinyun
- Angewandte Chemie International Edition, Vol. 57, Issue 47
Crystal engineering with DNA
journal, February 2019
- Laramy, Christine R.; O’Brien, Matthew N.; Mirkin, Chad A.
- Nature Reviews Materials, Vol. 4, Issue 3
Inverse design of simple pair potentials for the self-assembly of complex structures
journal, November 2018
- Adorf, Carl S.; Antonaglia, James; Dshemuchadse, Julia
- The Journal of Chemical Physics, Vol. 149, Issue 20
Kernel Homology in Gold Nanoclusters
journal, November 2018
- Zhuang, Shengli; Liao, Lingwen; Yuan, Jinyun
- Angewandte Chemie, Vol. 130, Issue 47
Inverse Design of Simple Pair Potentials for the Self-Assembly of Complex Structures
text, January 2017
- Adorf, Carl S.; Antonaglia, James; Dshemuchadse, Julia
- arXiv
Defining the Structure of a Protein–Spherical Nucleic Acid Conjugate and Its Counterionic Cloud
journal, March 2018
- Krishnamoorthy, Kurinji; Hoffmann, Kyle; Kewalramani, Sumit
- ACS Central Science, Vol. 4, Issue 3
Critical Assessment of the Interaction between DNA and Choline Amino Acid Ionic Liquids: Evidences of Multimodal Binding and Stability Enhancement
journal, December 2018
- Sahoo, Dipak Kumar; Jena, Subhrakant; Dutta, Juhi
- ACS Central Science, Vol. 4, Issue 12
The Importance of Salt-Enhanced Electrostatic Repulsion in Colloidal Crystal Engineering with DNA
journal, January 2019
- Seo, Soyoung E.; Girard, Martin; de la Cruz, Monica Olvera
- ACS Central Science, Vol. 5, Issue 1