Self-Assembly of Hierarchical DNA Nanotube Architectures with Well-Defined Geometries.

An essential motif for the assembly of biological materials such as actin at the scale of hundreds of nanometers and beyond is a network of one-dimensional fibers with well-defined geometry. Here, we demonstrate the programmed organization of DNA filaments into micron-scale architectures where component filaments are oriented at preprogrammed angles. We assemble L-, T-, and Y-shaped DNA origami junctions that nucleate two or three micron length DNA nanotubes at high yields. The angles between the nanotubes mirror the angles between the templates on the junctions, demonstrating that nanoscale structures can control precisely how micron-scale architectures form. The ability to precisely program filament orientation could allow the assembly of complex filament architectures in two and three dimensions, including circuit structures, bundles, and extended materials.

[1]  Hao Yan,et al.  Complex wireframe DNA origami nanostructures with multi-arm junction vertices. , 2015, Nature nanotechnology.

[2]  Rodney Andrews,et al.  Aligned Multiwalled Carbon Nanotube Membranes , 2004, Science.

[3]  Manuel Théry,et al.  Directed cytoskeleton self-organization. , 2012, Trends in cell biology.

[4]  E. Winfree,et al.  Design and characterization of programmable DNA nanotubes. , 2004, Journal of the American Chemical Society.

[5]  Erik Winfree,et al.  Integrating DNA strand-displacement circuitry with DNA tile self-assembly , 2013, Nature Communications.

[6]  Friedrich C Simmel,et al.  DNA-based assembly lines and nanofactories. , 2012, Current opinion in biotechnology.

[7]  J. Schwarzbauer,et al.  Assembly of fibronectin extracellular matrix. , 2010, Annual review of cell and developmental biology.

[8]  G. Seelig,et al.  Dynamic DNA nanotechnology using strand-displacement reactions. , 2011, Nature chemistry.

[9]  Erik Winfree,et al.  Determining hydrodynamic forces in bursting bubbles using DNA nanotube mechanics , 2015, Proceedings of the National Academy of Sciences.

[10]  Hao Yan,et al.  Challenges and opportunities for structural DNA nanotechnology. , 2011, Nature nanotechnology.

[11]  Tim Liedl,et al.  DNA Origami Nanopores , 2013 .

[12]  T. Stearns,et al.  Microtubule-organizing centres: a re-evaluation , 2007, Nature Reviews Molecular Cell Biology.

[13]  W. B. Knowlton,et al.  Programmable Periodicity of Quantum Dot Arrays with DNA Origami Nanotubes , 2010, Nano letters.

[14]  S. Howorka,et al.  A biomimetic DNA-based channel for the ligand-controlled transport of charged molecular cargo across a biological membrane. , 2016, Nature nanotechnology.

[15]  Hao Yan,et al.  Organizing DNA origami tiles into larger structures using preformed scaffold frames. , 2011, Nano letters.

[16]  Hao Yan,et al.  DNA-origami-directed self-assembly of discrete silver-nanoparticle architectures. , 2010, Angewandte Chemie.

[17]  Johannes B. Woehrstein,et al.  Polyhedra Self-Assembled from DNA Tripods and Characterized with 3D DNA-PAINT , 2014, Science.

[18]  Shawn M. Douglas,et al.  Folding DNA into Twisted and Curved Nanoscale Shapes , 2009, Science.

[19]  Hao Yan,et al.  Folding and cutting DNA into reconfigurable topological nanostructures. , 2010, Nature nanotechnology.

[20]  N. Hirokawa,et al.  Kinesin and dynein superfamily proteins and the mechanism of organelle transport. , 1998, Science.

[21]  James J. De Yoreo,et al.  Principles of crystal nucleation and growth , 2003 .

[22]  Rebecca Schulman,et al.  Directing self-assembly of DNA nanotubes using programmable seeds. , 2013, Nano letters.

[23]  Daniel A. Fletcher,et al.  Cell mechanics and the cytoskeleton , 2010, Nature.

[24]  Michael Mertig,et al.  Self-assembly of DNA nanotubes with controllable diameters. , 2011, Nature communications.

[25]  Jiahai Wang,et al.  Template-synthesized DNA nanotubes. , 2005, Journal of the American Chemical Society.

[26]  Rebecca Schulman,et al.  Self-assembling DNA nanotubes to connect molecular landmarks. , 2017, Nature nanotechnology.

[27]  Axel Ekani-Nkodo,et al.  Joining and scission in the self-assembly of nanotubes from DNA tiles. , 2004, Physical review letters.

[28]  Melinda Larsen,et al.  Extracellular matrix dynamics in development and regenerative medicine , 2008, Journal of Cell Science.

[29]  T. Endo,et al.  ATP as building blocks for the self-assembly of excitonic nanowires. , 2005, Journal of the American Chemical Society.

[30]  E. Nogales,et al.  Structure of the alpha beta tubulin dimer by electron crystallography. , 1998, Nature.

[31]  Michael J. Campolongo,et al.  Building plasmonic nanostructures with DNA. , 2011, Nature nanotechnology.

[32]  Rebecca Schulman,et al.  Kinetics and Thermodynamics of Watson-Crick Base Pairing Driven DNA Origami Dimerization. , 2016, Journal of the American Chemical Society.

[33]  Erik Winfree,et al.  An information-bearing seed for nucleating algorithmic self-assembly , 2009, Proceedings of the National Academy of Sciences.

[34]  Kenneth H. Downing,et al.  Structure of the αβ tubulin dimer by electron crystallography , 1998, Nature.

[35]  S. Stupp,et al.  Self-Assembly and Mineralization of Peptide-Amphiphile Nanofibers , 2001, Science.

[36]  Shawn M. Douglas,et al.  DNA-nanotube-induced alignment of membrane proteins for NMR structure determination , 2007, Proceedings of the National Academy of Sciences.

[37]  Faisal A. Aldaye,et al.  Modular construction of DNA nanotubes of tunable geometry and single- or double-stranded character. , 2009, Nature nanotechnology.

[38]  A. Ravve,et al.  Principles of Polymer Chemistry , 1995 .

[39]  S. Howorka Rationally engineering natural protein assemblies in nanobiotechnology. , 2011, Current opinion in biotechnology.

[40]  E. Winfree,et al.  Robust self-replication of combinatorial information via crystal growth and scission , 2012, Proceedings of the National Academy of Sciences.

[41]  H. Matsui,et al.  Peptide‐Based Nanotubes and Their Applications in Bionanotechnology , 2005, Advanced materials.

[42]  D. Fygenson,et al.  Self-assembly of precisely defined DNA nanotube superstructures using DNA origami seeds. , 2017, Nanoscale.

[43]  Jonathan Bath,et al.  A DNA-based molecular motor that can navigate a network of tracks. , 2012, Nature nanotechnology.

[44]  J. McIntosh,et al.  The Molecular Architecture of Axonemes Revealed by Cryoelectron Tomography , 2006, Science.

[45]  Harry M. T. Choi,et al.  Programming DNA Tube Circumferences , 2008, Science.

[46]  P. Rothemund Folding DNA to create nanoscale shapes and patterns , 2006, Nature.

[47]  Faisal A. Aldaye,et al.  A structurally tunable DNA-based extracellular matrix. , 2010, Journal of the American Chemical Society.

[48]  Rebecca Schulman,et al.  The Energy Landscape for the Self-Assembly of a Two-Dimensional DNA Origami Complex. , 2016, ACS nano.

[49]  Shuguang Zhang Fabrication of novel biomaterials through molecular self-assembly , 2003, Nature Biotechnology.

[50]  H. Dietz,et al.  Placing molecules with Bohr radius resolution using DNA origami. , 2016, Nature nanotechnology.

[51]  T. G. Martin,et al.  Rapid Folding of DNA into Nanoscale Shapes at Constant Temperature , 2012, Science.

[52]  K. Inaba,et al.  Tubulin-dynein system in flagellar and ciliary movement , 2012, Proceedings of the Japan Academy. Series B, Physical and biological sciences.

[53]  Bernard Yurke,et al.  Elongational-flow-induced scission of DNA nanotubes in laminar flow. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[54]  S. Stupp,et al.  Bioactive DNA-Peptide Nanotubes Enhance the Differentiation of Neural Stem Cells Into Neurons , 2014, Nano letters.

[55]  Cody W. Geary,et al.  A single-stranded architecture for cotranscriptional folding of RNA nanostructures , 2014, Science.

[56]  Luvena L. Ong,et al.  Three-Dimensional Structures Self-Assembled from DNA Bricks , 2012, Science.

[57]  M. Bathe,et al.  Quantitative prediction of 3D solution shape and flexibility of nucleic acid nanostructures , 2011, Nucleic acids research.

[58]  Adam H. Marblestone,et al.  Rapid prototyping of 3D DNA-origami shapes with caDNAno , 2009, Nucleic acids research.

[59]  Huang-Hao Yang,et al.  Template synthesized molecularly imprinted polymer nanotube membranes for chemical separations. , 2006, Journal of the American Chemical Society.

[60]  Kai Lin Lau,et al.  Minimalist Approach to Complexity: Templating the Assembly of DNA Tile Structures with Sequentially Grown Input Strands. , 2016, ACS nano.

[61]  Hai-Jun Su,et al.  Programmable motion of DNA origami mechanisms , 2015, Proceedings of the National Academy of Sciences.

[62]  Matthew D. Welch,et al.  A nucleator arms race: cellular control of actin assembly , 2010, Nature Reviews Molecular Cell Biology.

[63]  David R. Liu,et al.  DNA-templated organic synthesis: nature's strategy for controlling chemical reactivity applied to synthetic molecules. , 2004, Angewandte Chemie.

[64]  Lulu Qian,et al.  Programmable disorder in random DNA tilings. , 2017, Nature nanotechnology.