Programmable self-assembly of three-dimensional nanostructures from 10,000 unique components (original) (raw)
References
- Chen, J. & Seeman, N. C. The synthesis from DNA of a molecule with the connectivity of a cube. Nature 350, 631–633 (1991)
Article ADS CAS Google Scholar - Winfree, E., Liu, F., Wenzler, L. A. & Seeman, N. C. Design and self-assembly of two-dimensional DNA crystals. Nature 394, 539–544 (1998)
Article ADS CAS Google Scholar - Shih, W. M., Quispe, J. D. & Joyce, G. F. A. 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron. Nature 427, 618–621 (2004)
Article ADS CAS Google Scholar - Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 440, 297–302 (2006)
Article ADS CAS Google Scholar - Zheng, J. P. et al. From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal. Nature 461, 74–77 (2009)
Article ADS CAS Google Scholar - Douglas, S. M. et al. Self-assembly of DNA into nanoscale three-dimensional shapes. Nature 459, 414–418 (2009)
Article ADS CAS Google Scholar - Han, D. et al. DNA origami with complex curvatures in three-dimensional space. Science 332, 342–346 (2011)
Article ADS CAS Google Scholar - Wei, B., Dai, M. & Yin, P. Complex shapes self-assembled from single-stranded DNA tiles. Nature 485, 623–626 (2012)
Article ADS CAS Google Scholar - Ke, Y., Ong, L. L., Shih, W. M. & Yin, P. Three-dimensional structures self-assembled from DNA bricks. Science 338, 1177–1183 (2012)
Article ADS CAS Google Scholar - Han, D. et al. DNA gridiron nanostructures based on four-arm junctions. Science 339, 1412–1415 (2013)
Article ADS CAS Google Scholar - Iinuma, R. et al. Polyhedra self-assembled from DNA tripods and characterized with 3D DNA-PAINT. Science 344, 65–69 (2014)
Article ADS CAS Google Scholar - Gerling, T., Wagenbauer, K. F., Neuner, A. M. & Dietz, H. Dynamic DNA devices and assemblies formed by shape-complementary, non-base pairing 3D components. Science 347, 1446–1452 (2015)
Article ADS CAS Google Scholar - Benson, E. et al. DNA rendering of polyhedral meshes at the nanoscale. Nature 523, 441–444 (2015)
Article ADS CAS Google Scholar - Veneziano, R. et al. Designer nanoscale DNA assemblies programmed from the top down. Science 352, 1534 (2016)
Article ADS CAS Google Scholar - Marchi, A. N., Saaem, I., Vogen, B. N., Brown, S. & Labean, T. H. Towards larger DNA origami. Nano Lett. 14, 5740–5747 (2014)
Article ADS CAS Google Scholar - Nickels, P. C. et al. DNA origami structures directly assembled from intact bacteriophages. Small 10, 1765–1769 (2014)
Article CAS Google Scholar - Liu, Y., Ke, Y. & Yan, H. Self-assembly of symmetric finite-size DNA nanoarrays. J. Am. Chem. Soc. 127, 17140–17141 (2005)
Article CAS Google Scholar - Jungmann, R. et al. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat. Methods 11, 313–318 (2014)
Article CAS Google Scholar - Douglas, S. M. et al. Rapid prototyping of 3D DNA-origami shapes with caDNAno. Nucleic Acids Res. 37, 5001–5006 (2009)
Article CAS Google Scholar - Midgley, P. A. & Weyland, M. 3D electron microscopy in the physical sciences: the development of Z-contrast and EFTEM tomography. Ultramicroscopy 96, 413–431 (2003)
Article CAS Google Scholar - Myhrvold, C. et al. Barcode extension for analysis and reconstruction of structures (BEARS). Nat. Commun. 8, 14698 (2017)
Article ADS CAS Google Scholar - Jacobs, W. M., Reinhardt, A. & Frenkel, D. Rational design of self-assembled pathways for complex multicomponent structures. Proc. Natl Acad. Sci. USA 112, 6313–6318 (2015)
Article ADS CAS Google Scholar - Nickels, P. C. et al. Molecular force spectroscopy with a DNA origami-based nanoscopic force clamp. Science 354, 305–307 (2016)
Article ADS CAS Google Scholar - Douglas, S. M., Chou, J. J. & Shih, W. M. DNA-nanotube-induced alignment of membrane proteins for NMR structure determination. Proc. Natl Acad. Sci. USA 104, 6644–6648 (2007)
Article ADS CAS Google Scholar - Fu, J. et al. Multi-enzyme complexes on DNA scaffolds capable of substrate channeling with an artificial swinging arm. Nat. Nanotechnol. 9, 531–536 (2014)
Article ADS CAS Google Scholar - Sun, W. et al. Casting inorganic structures with DNA molds. Science 346, 1258361 (2014)
Article Google Scholar - Knudsen, J. B. et al. Routing of individual polymers in designed patterns. Nat. Nanotechnol. 10, 892–898 (2015)
Article ADS CAS Google Scholar - Acuna, G. P. et al. Fluorescence enhancement at docking sites of DNA-directed self-assembled nanoantennas. Science 338, 506–510 (2012)
Article ADS CAS Google Scholar - Schmidt, T. L. et al. Scalable amplification of strand subsets from chip-synthesized oligonucleotide libraries. Nat. Commun. 6, 8634 (2015)
Article ADS CAS Google Scholar - Rajendran, A., Endo, M., Katsuda, Y., Hidaka, K. & Sugiyama, H. Programmed two-dimensional self-assembly of multiple DNA origami jigsaw pieces. ACS Nano 5, 665–671 (2011)
Article CAS Google Scholar - Sobczak, J.-P. J., Martin, T. G., Gerling, T. & Dietz, H. Rapid folding of DNA into nanoscale shapes at constant temperature. Science 338, 1458–1461 (2012)
Article ADS CAS Google Scholar - Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012)
Article CAS Google Scholar - Huang, B., Wang, W., Bates, M. & Zhuang, X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810–813 (2008)
Article ADS CAS Google Scholar - Lin, C. et al. Sub-micrometre geometrically encoded fluorescent barcodes self-assembled from DNA. Nat. Chem. 4, 832–839 (2012)
Article CAS Google Scholar - El Beheiry, M. & Dahan, M. ViSP: representing single-particle localizations in three dimensions. Nat. Methods 10, 689–690 (2013)
Article CAS Google Scholar - Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012)
Article CAS Google Scholar - Quail, M. A. et al. A large genome centre’s improvements to the Illumina sequencing system. Nat. Methods 5, 1005–1010 (2008)
Article CAS Google Scholar
Acknowledgements
We thank N. Ponnuswamy, R. Sørensen, J. Hahn, J. Lara, L. Chou, N. Garreau, S. Saka, H. Sasaki, J. B. Woehrstein and C. B. Marks for experimental help. We also thank B. Wei, W. Sun and W.M. Shih for discussions, M. Beatty and J. Cheng for help in developing the Nanobricks platform, and C. Chen for assistance with draft preparation. The work was funded by Office of Naval Research grants N000141010827, N000141310593, N000141410610, N000141612182 and N000141612410, an Army Research Office grant W911NF1210238, National Science Foundation grants CCF-1054898, CCF-1162459, CCF-1317291, CMMI-1333215, CMMI-1334109 and CMMI-1344915, an Air Force Office of Scientific Research grant AFA9550-15-1-0514, and National Institute of Health grants 1DP2OD007292 and 1R01EB018659, 167814 (P.Y.); an Emory Biomedical Engineering Department Startup Fund, an Emory Winship Cancer Institute Billi and Bernie Marcus Research Award, a Winship Cancer Institute grant number IRG-14-188-0 from the American Cancer Society, and a National Science Foundation CAREER Award DMR–1654485 (Y.K.); French National Research Agency grants ANR-16-CE09-0004-01 and ANR-15-CE09-0003-02 (G.B.); and a French National Research Agency grant ANR-10-INBS-05 (P.B.). L.L.O. was funded by an NSF graduate research fellowship. N.H. was funded by the German National Academic Foundation and German Academic Exchange Service. M.T.S. acknowledges support from the International Max Planck Research School for Molecular and Cellular Life Sciences (IMPRS-LS).
Author information
Authors and Affiliations
- Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, 02115, Massachusetts, USA
Luvena L. Ong, Nikita Hanikel, Omar K. Yaghi, Casey Grun, Maximilian T. Strauss, Florian Schueder, Bei Wang, Jocelyn Y. Kishi, Cameron Myhrvold, Allen Zhu & Peng Yin - Harvard–MIT Program in Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, 02139, Massachusetts, USA
Luvena L. Ong - Max Planck Institute of Biochemistry, Martinsried Munich, 82152, Germany
Maximilian T. Strauss, Florian Schueder & Ralf Jungmann - Department of Physics and Center for Nanoscience, Ludwig Maximilian University, Munich, 80539, Germany
Maximilian T. Strauss, Florian Schueder & Ralf Jungmann - Centre de Biochimie Structurale, CNRS UMR 5048, INSERM U1054, Montpellier, F-34000, France
Patrick Bron & Josephine Lai-Kee-Him - Department of Polymer Science and Engineering, University of Science and Technology of China, Hefei, 230026, Anhui, China
Bei Wang - Department of Biomedical Engineering, Emory University and Georgia Institute of Technology, Atlanta, 30322, Georgia, USA
Pengfei Wang & Yonggang Ke - Department of Systems Biology, Harvard Medical School, Boston, 02115, Massachusetts, USA
Jocelyn Y. Kishi, Cameron Myhrvold & Peng Yin - Institut de Génomique Fonctionnelle, CNRS UMR 5203, INSERM U1191, Montpellier, F-34000, France
Gaetan Bellot - Department of Chemistry, Emory University, Atlanta, 30322, Georgia, USA
Yonggang Ke
Authors
- Luvena L. Ong
You can also search for this author inPubMed Google Scholar - Nikita Hanikel
You can also search for this author inPubMed Google Scholar - Omar K. Yaghi
You can also search for this author inPubMed Google Scholar - Casey Grun
You can also search for this author inPubMed Google Scholar - Maximilian T. Strauss
You can also search for this author inPubMed Google Scholar - Patrick Bron
You can also search for this author inPubMed Google Scholar - Josephine Lai-Kee-Him
You can also search for this author inPubMed Google Scholar - Florian Schueder
You can also search for this author inPubMed Google Scholar - Bei Wang
You can also search for this author inPubMed Google Scholar - Pengfei Wang
You can also search for this author inPubMed Google Scholar - Jocelyn Y. Kishi
You can also search for this author inPubMed Google Scholar - Cameron Myhrvold
You can also search for this author inPubMed Google Scholar - Allen Zhu
You can also search for this author inPubMed Google Scholar - Ralf Jungmann
You can also search for this author inPubMed Google Scholar - Gaetan Bellot
You can also search for this author inPubMed Google Scholar - Yonggang Ke
You can also search for this author inPubMed Google Scholar - Peng Yin
You can also search for this author inPubMed Google Scholar
Contributions
L.L.O. conceived the project, designed and performed the experiments, analysed the data and wrote the paper. N.H. designed and performed the experiments, analysed the data and wrote the paper. O.K.Y., B.W. and P.W. performed the experiments and analysed the data. M.T.S. and F.S. performed the 3D DNA-PAINT experiments, analysed the data and wrote the paper. C.G. and J.Y.K. developed the Nanobricks software and wrote the paper. P.B. and J.L.-K.-H. performed the electron tomography experiments. C.M. designed and analysed the sequencing experiments and wrote the paper. A.Z. performed the experiments. R.J. supervised the DNA-PAINT experiments, interpreted data and wrote the paper. G.B. designed and supervised the electron tomography study, interpreted data and wrote the paper. Y.K. and P.Y. conceived, designed and supervised the study, interpreted the data and wrote the paper.
Corresponding authors
Correspondence toGaetan Bellot, Yonggang Ke or Peng Yin.
Ethics declarations
Competing interests
A patent has been filed based on this work. P.Y. is co-founder of Ultivue Inc. and NuProbe Global.
Additional information
Reviewer Information Nature thanks C. Lin and the other anonymous reviewer(s) for their contribution to the peer review of this work.
Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
Extended Data Figure 1 Gel electrophoresis analysis of DNA brick cuboids.
a–h, Structures of varying size (see schematics on the left) were assembled isothermally for 5–7 days at the temperatures indicated above each gel lane, with strand concentrations of 30 nM (a–d), 5 nM (e, g), 3 nM (f) and 20 nM (h). The number below each lane indicates the formation yield of the target structure. Lane ‘M’ contains a 1-kilobase ladder.
Extended Data Figure 2 Characterization of 30H × 30H × 260B cavity shapes.
a, Schematic of the 30H × 30H × 260B molecular canvas (grey) compared with a DNA-origami-sized structure (blue). b, For each structure (numbered 1–7), the top panels show 3D models of the designed structure, the bottom left panels show expected TEM projections and the bottom right panels show the TEM averages from at least six particles. c, The structures were folded with 5 nM per strand by isothermal annealing or by using a narrow ramp from 52.5 °C to 51 °C. Products were analysed on a 0.5% agarose gel in the presence of 10 mM MgCl2. The percentage listed below a target band indicates the gel yield; labels correspond to those in b or in Fig. 3.
Supplementary information
Supplementary Information
This file contains Supplementary Methods and Data, Supplementary Tables 1-3, Supplementary Figures 1-113 and Supplementary References – see contents pages for details. (PDF 30485 kb)
Supplementary Data 1
This file contains the sequences used for each structure on separate tabs. (XLSX 4706 kb)
Bear structure
Tomography video of the bear structure (AVI 11680 kb)
GEB structure
Tomography video of the GEB structure (AVI 12801 kb)
Helix structure
Tomography video of the helix structure (AVI 7636 kb)
PowerPoint slides
Rights and permissions
About this article
Cite this article
Ong, L., Hanikel, N., Yaghi, O. et al. Programmable self-assembly of three-dimensional nanostructures from 10,000 unique components.Nature 552, 72–77 (2017). https://doi.org/10.1038/nature24648
- Received: 18 February 2017
- Accepted: 15 October 2017
- Published: 07 December 2017
- Issue Date: 07 December 2017
- DOI: https://doi.org/10.1038/nature24648