Modulating nanoparticle superlattice structure using proteins with tunable bond distributions

McMillan, Janet R.; Brodin, Jeffrey D.; Millan, Jaime A.; Lee, Byeongdu; Olvera de la Cruz, Monica; Mirkin, Chad A.

doi:10.1021/jacs.6b11893

Title: Modulating nanoparticle superlattice structure using proteins with tunable bond distributions

Journal Article · Wed Jan 25 00:00:00 EST 2017 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.6b11893· OSTI ID:1371916

McMillan, Janet R. ^[1]; Brodin, Jeffrey D. ^[1]; Millan, Jaime A. ^[1];

^[2]; Olvera de la Cruz, Monica ^[1];

^[1]

Northwestern Univ., Evanston, IL (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)

Here, we investigate the use of proteins with tunable DNA modification distributions to modulate nanoparticle superlattice structure. Using Beta-galactosidase (βgal) as a model system, we have employed the orthogonal chemical reactivities of surface amines and thiols to synthesize protein-DNA conjugates with 36 evenly distributed or 8 specifically positioned oligonucleotides. When assembled into crystalline superlattices with AuNPs, we find that the distribution of DNA modifications modulates the favored structure: βgal with uniformly distributed DNA bonding elements results in body-centered cubic crystals, whereas DNA functionalization of cysteines results in AB₂ packing. We probe the role of protein oligonucleotide number and conjugate size on this observation, which revealed the importance of oligonucleotide distribution and number in this observed assembly behavior. These results indicate that proteins with defined DNA-modification patterns are powerful tools to control the nanoparticle superlattices architecture, and establish the importance of oligonucleotide distribution in the assembly behavior of protein-DNA conjugates.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: U.S. Department of Defense (DOD); Air Force Research Laboratory (AFRL), Air Force Office of Scientific Research (AFOSR); USDOE Office of Science (SC); W.M. Keck Foundation; National Science Foundation (NSF)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1371916

Journal Information:: Journal of the American Chemical Society, Vol. 139, Issue 5; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 46 works

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References (36)

A DNA-based method for rationally assembling nanoparticles into macroscopic materials Mirkin, Chad A.; Letsinger, Robert L.; Mucic, Robert C. Nature, Vol. 382, Issue 6592, p. 607-609 https://doi.org/10.1038/382607a0	journal	August 1996
DNA in a material world Seeman, Nadrian C. Nature, Vol. 421, Issue 6921 https://doi.org/10.1038/nature01406	journal	January 2003
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
Programmable materials and the nature of the DNA bond Jones, M. R.; Seeman, N. C.; Mirkin, C. A. Science, Vol. 347, Issue 6224 https://doi.org/10.1126/science.1260901	journal	February 2015
DNA-guided crystallization of colloidal nanoparticles Nykypanchuk, Dmytro; Maye, Mathew M.; van der Lelie, Daniel Nature, Vol. 451, Issue 7178, p. 549-552 https://doi.org/10.1038/nature06560	journal	January 2008
DNA-programmable nanoparticle crystallization Park, Sung Yong; Lytton-Jean, Abigail K. R.; Lee, Byeongdu Nature, Vol. 451, Issue 7178, p. 553-556 https://doi.org/10.1038/nature06508	journal	January 2008
Nanoparticle Superlattice Engineering with DNA Macfarlane, R. J.; Lee, B.; Jones, M. R. Science, Vol. 334, Issue 6053, p. 204-208 https://doi.org/10.1126/science.1210493	journal	October 2011
Dynamic Tuning of DNA-Nanoparticle Superlattices by Molecular Intercalation of Double Helix Pal, Suchetan; Zhang, Yugang; Kumar, Sanat K. Journal of the American Chemical Society, Vol. 137, Issue 12 https://doi.org/10.1021/ja512799d	journal	March 2015
The Significance of Multivalent Bonding Motifs and “Bond Order” in DNA-Directed Nanoparticle Crystallization Thaner, Ryan V.; Eryazici, Ibrahim; Macfarlane, Robert J. Journal of the American Chemical Society, Vol. 138, Issue 19 https://doi.org/10.1021/jacs.6b02479	journal	May 2016
A general approach to DNA-programmable atom equivalents Zhang, Chuan; Macfarlane, Robert J.; Young, Kaylie L. Nature Materials, Vol. 12, Issue 8 https://doi.org/10.1038/nmat3647	journal	May 2013
DNA-mediated engineering of multicomponent enzyme crystals Brodin, Jeffrey D.; Auyeung, Evelyn; Mirkin, Chad A. Proceedings of the National Academy of Sciences, Vol. 112, Issue 15 https://doi.org/10.1073/pnas.1503533112	journal	March 2015
DNA-nanoparticle superlattices formed from anisotropic building blocks Jones, Matthew R.; Macfarlane, Robert J.; Lee, Byeongdu Nature Materials, Vol. 9, Issue 11, p. 913-917 https://doi.org/10.1038/nmat2870	journal	October 2010
Superlattices assembled through shape-induced directional binding Lu, Fang; Yager, Kevin G.; Zhang, Yugang Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7912	journal	April 2015
Modular and Chemically Responsive Oligonucleotide “Bonds” in Nanoparticle Superlattices Barnaby, Stacey N.; Thaner, Ryan V.; Ross, Michael B. Journal of the American Chemical Society, Vol. 137, Issue 42 https://doi.org/10.1021/jacs.5b07908	journal	October 2015
Transmutable nanoparticles with reconfigurable surface ligands Kim, Y.; Macfarlane, R. J.; Jones, M. R. Science, Vol. 351, Issue 6273 https://doi.org/10.1126/science.aad2212	journal	February 2016
Synthetically programmable nanoparticle superlattices using a hollow three-dimensional spacer approach Auyeung, Evelyn; Cutler, Joshua I.; Macfarlane, Robert J. Nature Nanotechnology, Vol. 7, Issue 1 https://doi.org/10.1038/nnano.2011.222	journal	December 2011
Diamond family of nanoparticle superlattices Liu, W.; Tagawa, M.; Xin, H. L. Science, Vol. 351, Issue 6273, p. 582-586 https://doi.org/10.1126/science.aad2080	journal	February 2016
Lattice engineering through nanoparticle–DNA frameworks Tian, Ye; Zhang, Yugang; Wang, Tong Nature Materials, Vol. 15, Issue 6, p. 654-661 https://doi.org/10.1038/nmat4571	journal	February 2016
Orthogonal Self-Assembly on Colloidal Gold-Platinum Nanorods Martin, Benjamin R.; Dermody, Daniel J.; Reiss, Brian D. Advanced Materials, Vol. 11, Issue 12, p. 1021-1025 https://doi.org/10.1002/(SICI)1521-4095(199908)11:12<1021::AID-ADMA1021>3.0.CO;2-S	journal	August 1999
Biphasic Janus particles with nanoscale anisotropy Roh, Kyung-Ho; Martin, David C.; Lahann, Joerg Nature Materials, Vol. 4, Issue 10, p. 759-763 https://doi.org/10.1038/nmat1486	journal	September 2005
Asymmetric Functionalization of Gold Nanoparticles with Oligonucleotides Xu, Xiaoyang; Rosi, Nathaniel L.; Wang, Yuhuang Journal of the American Chemical Society, Vol. 128, Issue 29 https://doi.org/10.1021/ja061980b	journal	July 2006
Guided hierarchical co-assembly of soft patchy nanoparticles Gröschel, André H.; Walther, Andreas; Löbling, Tina I. Nature, Vol. 503, Issue 7475 https://doi.org/10.1038/nature12610	journal	November 2013
Transfer of molecular recognition information from DNA nanostructures to gold nanoparticles Edwardson, Thomas G. W.; Lau, Kai Lin; Bousmail, Danny Nature Chemistry, Vol. 8, Issue 2 https://doi.org/10.1038/nchem.2420	journal	January 2016
Self-Assembly of a Tetrahedral Lectin into Predesigned Diamondlike Protein Crystals Dotan, Nir; Arad, Dorit; Frolow, Felix Angewandte Chemie International Edition, Vol. 38, Issue 16 https://doi.org/10.1002/(SICI)1521-3773(19990816)38:16<2363::AID-ANIE2363>3.3.CO;2-4	journal	August 1999
Computational design of a protein crystal Lanci, C. J.; MacDermaid, C. M.; Kang, S. -g. Proceedings of the National Academy of Sciences, Vol. 109, Issue 19 https://doi.org/10.1073/pnas.1112595109	journal	April 2012
Protein crystalline frameworks with controllable interpenetration directed by dual supramolecular interactions Sakai, Fuji; Yang, Guang; Weiss, Manfred S. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5634	journal	August 2014
A Metal Organic Framework with Spherical Protein Nodes: Rational Chemical Design of 3D Protein Crystals Sontz, Pamela A.; Bailey, Jake B.; Ahn, Sunhyung Journal of the American Chemical Society, Vol. 137, Issue 36 https://doi.org/10.1021/jacs.5b07463	journal	September 2015
Design of ordered two-dimensional arrays mediated by noncovalent protein-protein interfaces Gonen, S.; DiMaio, F.; Gonen, T. Science, Vol. 348, Issue 6241 https://doi.org/10.1126/science.aaa9897	journal	June 2015
Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals Suzuki, Yuta; Cardone, Giovanni; Restrepo, David Nature, Vol. 533, Issue 7603 https://doi.org/10.1038/nature17633	journal	May 2016
Electrostatic assembly of binary nanoparticle superlattices using protein cages Kostiainen, Mauri A.; Hiekkataipale, Panu; Laiho, Ari Nature Nanotechnology, Vol. 8, Issue 1 https://doi.org/10.1038/nnano.2012.220	journal	December 2012
Binary Protein Crystals for the Assembly of Inorganic Nanoparticle Superlattices Künzle, Matthias; Eckert, Thomas; Beck, Tobias Journal of the American Chemical Society, Vol. 138, Issue 39 https://doi.org/10.1021/jacs.6b07260	journal	September 2016
DNA-Mediated Cellular Delivery of Functional Enzymes Brodin, Jeffrey D.; Sprangers, Anthony J.; McMillan, Janet R. Journal of the American Chemical Society, Vol. 137, Issue 47 https://doi.org/10.1021/jacs.5b09711	journal	November 2015
A Strain-Promoted [3 + 2] Azide−Alkyne Cycloaddition for Covalent Modification of Biomolecules in Living Systems Agard, Nicholas J.; Prescher, Jennifer A.; Bertozzi, Carolyn R. Journal of the American Chemical Society, Vol. 126, Issue 46 https://doi.org/10.1021/ja044996f	journal	November 2004
DNA-mediated nanoparticle crystallization into Wulff polyhedra Auyeung, Evelyn; Li, Ting I. N. G.; Senesi, Andrew J. Nature, Vol. 505, Issue 7481 https://doi.org/10.1038/nature12739	journal	November 2013
Heterogeneous Ligand–Nanoparticle Distributions: A Major Obstacle to Scientific Understanding and Commercial Translation Mullen, Douglas G.; Banaszak Holl, Mark M. Accounts of Chemical Research, Vol. 44, Issue 11 https://doi.org/10.1021/ar1001389	journal	November 2011
Modeling the Crystallization of Spherical Nucleic Acid Nanoparticle Conjugates with Molecular Dynamics Simulations Li, Ting I. N. G.; Sknepnek, Rastko; Macfarlane, Robert J. Nano Letters, Vol. 12, Issue 5 https://doi.org/10.1021/nl300679e	journal	April 2012

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DNA‐ and Field‐Mediated Assembly of Magnetic Nanoparticles into High‐Aspect Ratio Crystals Park, Sarah S.; Urbach, Zachary J.; Brisbois, Chase A. Advanced Materials, Vol. 32, Issue 4 https://doi.org/10.1002/adma.201906626	journal	December 2019
Efficient bioactive oligonucleotide‐protein conjugation for cell‐targeted cancer therapy Aviñó, Anna; Unzueta, Ugutz; Virtudes Céspedes, María ChemistryOpen, Vol. 8, Issue 3 https://doi.org/10.1002/open.201900038	journal	March 2019
Programmable Atom Equivalents: Atomic Crystallization as a Framework for Synthesizing Nanoparticle Superlattices Gabrys, Paul A.; Zornberg, Leonardo Z.; Macfarlane, Robert J. Small, Vol. 15, Issue 26 https://doi.org/10.1002/smll.201805424	journal	February 2019
Crystallizing protein assemblies via free and grafted linkers Dahal, Yuba Raj; Olvera de la Cruz, Monica Soft Matter, Vol. 15, Issue 21 https://doi.org/10.1039/c9sm00693a	journal	January 2019
Hamilton Receptor‐Mediated Self‐Assembly of Orthogonally Functionalized Au and TiO ₂ Nanoparticles Ali, Muhammad; Hasenöhrl, Dominik H.; Zeininger, Lukas Helvetica Chimica Acta, Vol. 102, Issue 4 https://doi.org/10.1002/hlca.201900015	journal	March 2019
Crystal engineering with DNA Laramy, Christine R.; O’Brien, Matthew N.; Mirkin, Chad A. Nature Reviews Materials, Vol. 4, Issue 3 https://doi.org/10.1038/s41578-019-0087-2	journal	February 2019
Significance of DNA bond strength in programmable nanoparticle thermodynamics and dynamics Yu, Qiuyan; Hu, Jinglei; Hu, Yi Soft Matter, Vol. 14, Issue 14 https://doi.org/10.1039/c7sm02456h	journal	January 2018
Particle analogs of electrons in colloidal crystals Girard, Martin; Wang, Shunzhi; Du, Jingshan S. Science, Vol. 364, Issue 6446 https://doi.org/10.1126/science.aaw8237	journal	June 2019
Assembling Ordered Crystals with Disperse Building Blocks Santos, Peter J.; Cheung, Tung Chun; Macfarlane, Robert J. Nano Letters, Vol. 19, Issue 8 https://doi.org/10.1021/acs.nanolett.9b02508	journal	July 2019
Defining the Structure of a Protein–Spherical Nucleic Acid Conjugate and Its Counterionic Cloud Krishnamoorthy, Kurinji; Hoffmann, Kyle; Kewalramani, Sumit ACS Central Science, Vol. 4, Issue 3 https://doi.org/10.1021/acscentsci.7b00577	journal	March 2018

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