DNA-mediated engineering of multicomponent enzyme crystals

Brodin, Jeffrey D.; Auyeung, Evelyn; Mirkin, Chad A.

doi:10.1073/pnas.1503533112

Title: DNA-mediated engineering of multicomponent enzyme crystals

Journal Article · Mon Mar 23 00:00:00 EDT 2015 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1503533112· OSTI ID:1182330

Brodin, Jeffrey D. ^[1]; Auyeung, Evelyn ^[2]; Mirkin, Chad A. ^[3]

Northwestern Univ., Evanston, IL (United States). Dept. of Chemistry. International Inst. for Nanotechnology
Northwestern Univ., Evanston, IL (United States). International Inst. for Nanotechnology. Dept. of Materials Science and Engineering
Northwestern Univ., Evanston, IL (United States). Dept. of Chemistry. International Inst. for Nanotechnology. Dept. of Materials Science and Engineering

The ability to predictably control the coassembly of multiple nanoscale building blocks, especially those with disparate chemical and physical properties such as biomolecules and inorganic nanoparticles, has far-reaching implications in catalysis, sensing, and photonics, but a generalizable strategy for engineering specific contacts between these particles is an outstanding challenge. This is especially true in the case of proteins, where the types of possible interparticle interactions are numerous, diverse, and complex. In this paper, we explore the concept of trading protein–protein interactions for DNA–DNA interactions to direct the assembly of two nucleic-acid–functionalized proteins with distinct surface chemistries into six unique lattices composed of catalytically active proteins, or of a combination of proteins and DNA-modified gold nanoparticles. The programmable nature of DNA–DNA interactions used in this strategy allows us to control the lattice symmetries and unit cell constants, as well as the compositions and habit, of the resulting crystals. Finally, this study provides a potentially generalizable strategy for constructing a unique class of materials that take advantage of the diverse morphologies, surface chemistries, and functionalities of proteins for assembling functional crystalline materials.

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Research Organization:: Northwestern Univ., Evanston, IL (United States)

Sponsoring Organization:: USDOE; USDOD; US Air Force Office of Scientific Research (AFOSR)

Grant/Contract Number:: AC02-06CH11357; N00014-15-1-0043; FA9550-11-1-0275

OSTI ID:: 1182330

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 15; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 111 works

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References (50)

Nucleic Acid-Modified Nanostructures as Programmable Atom Equivalents: Forging a New “Table of Elements”* Macfarlane, Robert J.; O’Brien, Matthew N.; Petrosko, Sarah Hurst Spherical Nucleic Acids https://doi.org/10.4324/9780429200151-6	book	August 2020
Maximizing DNA Loading on a Range of Gold Nanoparticle Sizes Hurst, Sarah J.; Lytton-Jean, Abigail K. R.; Mirkin, Chad A. Analytical Chemistry, Vol. 78, Issue 24 https://doi.org/10.1021/ac0613582	journal	December 2006
Accurate design of co-assembling multi-component protein nanomaterials King, Neil P.; Bale, Jacob B.; Sheffler, William Nature, Vol. 510, Issue 7503 https://doi.org/10.1038/nature13404	journal	May 2014
Generation of protein lattices by fusing proteins with matching rotational symmetry Sinclair, John C.; Davies, Karen M.; Vénien-Bryan, Catherine Nature Nanotechnology, Vol. 6, Issue 9 https://doi.org/10.1038/nnano.2011.122	journal	July 2011
Nanohedra: Using symmetry to design self assembling protein cages, layers, crystals, and filaments Padilla, J. E.; Colovos, C.; Yeates, T. O. Proceedings of the National Academy of Sciences, Vol. 98, Issue 5 https://doi.org/10.1073/pnas.041614998	journal	February 2001
Design and self-assembly of two-dimensional DNA crystals Winfree, Erik; Liu, Furong; Wenzler, Lisa A. Nature, Vol. 394, Issue 6693 https://doi.org/10.1038/28998	journal	August 1998
Enzyme cascades activated on topologically programmed DNA scaffolds Wilner, Ofer I.; Weizmann, Yossi; Gill, Ron Nature Nanotechnology, Vol. 4, Issue 4 https://doi.org/10.1038/nnano.2009.50	journal	March 2009
Computational Design of Self-Assembling Protein Nanomaterials with Atomic Level Accuracy King, N. P.; Sheffler, W.; Sawaya, M. R. Science, Vol. 336, Issue 6085 https://doi.org/10.1126/science.1219364	journal	May 2012
A comparison of successful and failed protein interface designs highlights the challenges of designing buried hydrogen bonds Brian, Kuhlman,; Benjamin, Stranges, P. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/wv99-pw07	text	January 2013
Life as a Nanoscale Phenomenon Mann, Stephen Angewandte Chemie International Edition, Vol. 47, Issue 29 https://doi.org/10.1002/anie.200705538	journal	July 2008
A general strategy for the DNA-mediated self-assembly of functional nanoparticles into heterogeneous systems Zhang, Yugang; Lu, Fang; Yager, Kevin G. Nature Nanotechnology, Vol. 8, Issue 11 https://doi.org/10.1038/nnano.2013.209	journal	October 2013
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
Establishing the Design Rules for DNA-Mediated Programmable Colloidal Crystallization Macfarlane, Robert J.; Jones, Matthew R.; Senesi, Andrew J. Angewandte Chemie International Edition, Vol. 49, Issue 27 https://doi.org/10.1002/anie.201000633	journal	May 2010
An Overview of Structural DNA Nanotechnology Seeman, Nadrian C. Molecular Biotechnology, Vol. 37, Issue 3 https://doi.org/10.1007/s12033-007-0059-4	journal	July 2007
DNA-controlled assembly of a NaTl lattice structure from gold nanoparticles and protein nanoparticles Cigler, Petr; Lytton-Jean, Abigail K. R.; Anderson, Daniel G. Nature Materials, Vol. 9, Issue 11, p. 918-922 https://doi.org/10.1038/nmat2877	journal	October 2010
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
Controlling the Lattice Parameters of Gold Nanoparticle FCC Crystals with Duplex DNA Linkers Hill, Haley D.; Macfarlane, Robert J.; Senesi, Andrew J. Nano Letters, Vol. 8, Issue 8 https://doi.org/10.1021/nl8011787	journal	August 2008
Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays Brodin, Jeffrey D.; Ambroggio, X. I.; Tang, Chunyan Nature Chemistry, Vol. 4, Issue 5 https://doi.org/10.1038/nchem.1290	journal	March 2012
DNA-Mediated Assembly of Protein Heterodimers on Membrane Surfaces Coyle, Michael P.; Xu, Qian; Chiang, Samantha Journal of the American Chemical Society, Vol. 135, Issue 13 https://doi.org/10.1021/ja3101215	journal	March 2013
DNA-Templated Self-Assembly of Protein Arrays and Highly Conductive Nanowires Yan, H. Science, Vol. 301, Issue 5641 https://doi.org/10.1126/science.1089389	journal	September 2003
From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal Zheng, Jianping; Birktoft, Jens J.; Chen, Yi Nature, Vol. 461, Issue 7260 https://doi.org/10.1038/nature08274	journal	September 2009
Self-assembly and modular functionalization of three-dimensional crystals from oppositely charged proteins Liljeström, Ville; Mikkilä, Joona; Kostiainen, Mauri A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5445	journal	July 2014
Synthetically Programmable Nanoparticle Superlattices Using a Hollow Three-Dimensional Spacer Approach Auyeung, Evelyn; Cutler, Joshua I.; Macfarlane, Robert J. Spherical Nucleic Acids https://doi.org/10.1201/9781003056690-29	book	March 2020
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
Synthetically Programmable Nanoparticle Superlattices Using a Hollow Three-Dimensional Spacer Approach* Auyeung, Evelyn; Cutler, Joshua I.; Macfarlane, Robert J. Spherical Nucleic Acids https://doi.org/10.1201/9781003056690-8	book	March 2020
Hierarchical Assembly of Plasmonic Nanostructures Using Virus Capsid Scaffolds on DNA Origami Templates Wang, Debin; Capehart, Stacy L.; Pal, Suchetan ACS Nano, Vol. 8, Issue 8 https://doi.org/10.1021/nn5015819	journal	July 2014
Protein Function in the Crystal Mozzarelli, A.; Rossi, G. L. Annual Review of Biophysics and Biomolecular Structure, Vol. 25, Issue 1 https://doi.org/10.1146/annurev.bb.25.060196.002015	journal	June 1996
Functionalizing Designer DNA Crystals with a Triple-Helical Veneer Rusling, David A.; Chandrasekaran, Arun Richard; Ohayon, Yoel P. Angewandte Chemie International Edition, Vol. 53, Issue 15 https://doi.org/10.1002/anie.201309914	journal	March 2014
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
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
Self-Assembly of Proteins into Designed Networks Ringler, P. Science, Vol. 302, Issue 5642 https://doi.org/10.1126/science.1088074	journal	October 2003
DNA-Directed Three-Dimensional Protein Organization Zhang, Chuan; Tian, Cheng; Guo, Fei Angewandte Chemie International Edition, Vol. 51, Issue 14 https://doi.org/10.1002/anie.201108710	journal	February 2012
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
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>3.0.CO;2-D	journal	August 1999
Nucleic Acid-Modified Nanostructures as Programmable Atom Equivalents: Forging a New “Table of Elements” Macfarlane, Robert J.; O'Brien, Matthew N.; Petrosko, Sarah Hurst Angewandte Chemie International Edition, Vol. 52, Issue 22 https://doi.org/10.1002/anie.201209336	journal	May 2013
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
Transitioning DNA-Engineered Nanoparticle Superlattices from Solution to the Solid State Auyeung, Evelyn; Macfarlane, Robert J.; Choi, Chung Hang J. Advanced Materials, Vol. 24, Issue 38 https://doi.org/10.1002/adma.201202069	journal	July 2012
A comparison of successful and failed protein interface designs highlights the challenges of designing buried hydrogen bonds Stranges, P. Benjamin; Kuhlman, Brian Protein Science, Vol. 22, Issue 1 https://doi.org/10.1002/pro.2187	journal	November 2012
Functionalizing Designer DNA Crystals with a Triple-Helical Veneer Rusling, David A.; Chandrasekaran, Arun Richard; Ohayon, Yoel P. Angewandte Chemie, Vol. 126, Issue 15 https://doi.org/10.1002/ange.201309914	journal	March 2014
Supramolecular assembling systems formed by heme–heme pocket interactions in hemoproteins Oohora, Koji; Onoda, Akira; Hayashi, Takashi Chemical Communications, Vol. 48, Issue 96 https://doi.org/10.1039/c2cc36376c	journal	January 2012
Natural Nanochemical Building Blocks: Icosahedral Virus Particles Organized by Attached Oligonucleotides Strable, Erica; Johnson, John E.; Finn, M. G. Nano Letters, Vol. 4, Issue 8 https://doi.org/10.1021/nl0493850	journal	August 2004
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
DNA-Directed Three-Dimensional Protein Organization Zhang, Chuan; Tian, Cheng; Guo, Fei Angewandte Chemie, Vol. 124, Issue 14 https://doi.org/10.1002/ange.201108710	journal	February 2012
Phase Behavior of Nanoparticles Assembled by DNA Linkers Xiong, Huiming; van der Lelie, Daniel; Gang, Oleg Physical Review Letters, Vol. 102, Issue 1 https://doi.org/10.1103/PhysRevLett.102.015504	journal	January 2009
Nucleic Acid-Modified Nanostructures as Programmable Atom Equivalents: Forging a New “Table of Elements”* Macfarlane, Robert J.; O’Brien, Matthew N.; Petrosko, Sarah Hurst Spherical Nucleic Acids https://doi.org/10.1201/9781003056676-6	book	March 2020
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
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
A Spectrophotometric Method for Measuring the Breakdown of Hydrogen Peroxide by Catalase Beers, Roland F.; Sizer, Irwin W. Journal of Biological Chemistry, Vol. 195, Issue 1 https://doi.org/10.1016/S0021-9258(19)50881-X	journal	March 1952
Reconstitution of Acid-denatured Catalase Samejima, Tatsuya; Yang, Jen Tsi Journal of Biological Chemistry, Vol. 238, Issue 10 https://doi.org/10.1016/S0021-9258(18)48655-3	journal	October 1963
Establishing the Design Rules for DNA-Mediated Programmable Colloidal Crystallization Macfarlane, Robert J.; Jones, Matthew R.; Senesi, Andrew J. Angewandte Chemie, Vol. 122, Issue 27, p. 4693-4696 https://doi.org/10.1002/ange.201000633	journal	May 2010

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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
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Self-Assembly of a 3D DNA Crystal Structure with Rationally Designed Six-Fold Symmetry Zhang, Fei; Simmons, Chad R.; Gates, Jade Angewandte Chemie, Vol. 130, Issue 38 https://doi.org/10.1002/ange.201807223	journal	August 2018
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
DNA-Based Enzyme Reactors and Systems Linko, Veikko; Nummelin, Sami; Aarnos, Laura Nanomaterials, Vol. 6, Issue 8 https://doi.org/10.3390/nano6080139	journal	July 2016
Recent progress in live cell mRNA/microRNA imaging probes based on smart and versatile nanomaterials He, Dinggeng; Wong, Ka-Wang; Dong, Zhenzhen Journal of Materials Chemistry B, Vol. 6, Issue 47 https://doi.org/10.1039/c8tb02285b	journal	January 2018
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
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Building expanded structures from tetrahedral DNA branching elements, RNA and TMV protein Wenz, Nana L.; Piasecka, Sylwia; Kalinowski, Matthäus Nanoscale, Vol. 10, Issue 14 https://doi.org/10.1039/c7nr07743b	journal	January 2018
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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59 BASIC BIOLOGICAL SCIENCES
nanoscience
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self-assembly
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DNA-programmable assembly

Title: DNA-mediated engineering of multicomponent enzyme crystals

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