A single-stranded architecture for cotranscriptional folding of RNA nanostructures

The future of RNA origami writ large Researchers have long fabricated intricate nanostructures from carefully linked DNA strands. Now they can use RNA made by gene expression, which avoids the costly strand synthesis and lengthy annealing steps necessary with DNA origami. Geary et al. used molecular modeling to extend the size of folded RNA origami structures (see the Perspective by Leontis and Westhof). The modeling revealed assembly patterns for linking single-stranded RNA into A-form helices. The authors created two-dimensional structures as large as 660 nucleotides on mica surfaces. Science, this issue p. 799; see also p. 732 The size of RNA origami nanostructures has been increased with a distinct assembly pattern. [Also see Perspective by Leontis and Westhof] Artificial DNA and RNA structures have been used as scaffolds for a variety of nanoscale devices. In comparison to DNA structures, RNA structures have been limited in size, but they also have advantages: RNA can fold during transcription and thus can be genetically encoded and expressed in cells. We introduce an architecture for designing artificial RNA structures that fold from a single strand, in which arrays of antiparallel RNA helices are precisely organized by RNA tertiary motifs and a new type of crossover pattern. We constructed RNA tiles that assemble into hexagonal lattices and demonstrated that lattices can be made by annealing and/or cotranscriptional folding. Tiles can be scaled up to 660 nucleotides in length, reaching a size comparable to that of large natural ribozymes.

[1]  Juliane Junker,et al.  The Making Of A Fly The Genetics Of Animal Design , 2016 .

[2]  Luc Jaeger,et al.  RNA self-assembly and RNA nanotechnology. , 2014, Accounts of chemical research.

[3]  Minjae Lee,et al.  RNA design rules from a massive open laboratory , 2014, Proceedings of the National Academy of Sciences.

[4]  Peng Yin,et al.  Conditional Dicer Substrate Formation via Shape and Sequence Transduction with Small Conditional RNAs , 2013, Journal of the American Chemical Society.

[5]  Luc Jaeger,et al.  RNA modularity for synthetic biology , 2013, F1000prime reports.

[6]  T. G. Martin,et al.  Cryo-EM structure of a 3D DNA-origami object , 2012, Proceedings of the National Academy of Sciences.

[7]  P. Yin,et al.  Complex shapes self-assembled from single-stranded DNA tiles , 2012, Nature.

[8]  V. Isaeva.  Self-organization in biological systems , 2012, Biology Bulletin.

[9]  Wenjiao Song,et al.  Fluorescence Imaging of Cellular Metabolites with RNA , 2012, Science.

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

[11]  Faisal A. Aldaye,et al.  Organization of Intracellular Reactions with Rationally Designed RNA Assemblies , 2011, Science.

[12]  Tae-Jin Kim,et al.  Use of RNA structure flexibility data in nanostructure modeling. , 2011, Methods.

[13]  Wade W Grabow,et al.  Self-assembling RNA nanorings based on RNAI/II inverse kissing complexes. , 2011, Nano letters (Print).

[14]  S. Yoshimura,et al.  Synthetic RNA-protein complex shaped like an equilateral triangle. , 2011, Nature nanotechnology.

[15]  Conrad Steenberg,et al.  NUPACK: Analysis and design of nucleic acid systems , 2011, J. Comput. Chem..

[16]  Luc Jaeger,et al.  Promoting RNA helical stacking via A-minor junctions , 2010, Nucleic acids research.

[17]  L. Jaeger,et al.  In vitro Assembly of Cubic RNA-Based Scaffolds Designed in silico , 2010, Nature nanotechnology.

[18]  Eric Westhof,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2022 .

[19]  Cody W. Geary,et al.  A polyhedron made of tRNAs , 2010, Nature chemistry.

[20]  Hervé Isambert,et al.  The jerky and knotty dynamics of RNA. , 2009, Methods.

[21]  Hao Yan,et al.  A replicable tetrahedral nanostructure self-assembled from a single DNA strand. , 2009, Journal of the American Chemical Society.

[22]  S. Murata,et al.  Substrate-assisted assembly of interconnected single-duplex DNA nanostructures. , 2009, Angewandte Chemie.

[23]  C. Mao,et al.  Surface-mediated DNA self-assembly. , 2009, Journal of the American Chemical Society.

[24]  J. Kjems,et al.  Self-assembly of a nanoscale DNA box with a controllable lid , 2009, Nature.

[25]  Cody W. Geary,et al.  Square-shaped RNA particles from different RNA folds. , 2009, Nano letters.

[26]  Eric Westhof,et al.  The Dynamic Landscapes of RNA Architecture , 2009, Cell.

[27]  Hao Yan,et al.  In vivo cloning of artificial DNA nanostructures , 2008, Proceedings of the National Academy of Sciences.

[28]  L. Jaeger,et al.  The architectonics of programmable RNA and DNA nanostructures. , 2006, Current opinion in structural biology.

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

[30]  H. Hansma,et al.  Building Programmable Jigsaw Puzzles with RNA , 2004, Science.

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

[32]  Conrad C. Huang,et al.  UCSF Chimera—A visualization system for exploratory research and analysis , 2004, J. Comput. Chem..

[33]  William M. Shih,et al.  A 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron , 2004, Nature.

[34]  G. Kawai,et al.  RNA LEGO: magnesium-dependent formation of specific RNA assemblies through kissing interactions. , 2003, Chemistry & biology.

[35]  S. Woodson,et al.  Effect of transcription on folding of the Tetrahymena ribozyme. , 2003, RNA.

[36]  N. Seeman,et al.  A robust DNA mechanical device controlled by hybridization topology , 2002, Nature.

[37]  Philippe Dumas,et al.  Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site , 2001, Nature Structural Biology.

[38]  T. Steitz,et al.  The kink‐turn: a new RNA secondary structure motif , 2001, The EMBO journal.

[39]  Lucey Dr,et al.  Tecto-RNA: One-Dimensional Self-Assembly through Tertiary Interactions , 2000 .

[40]  A'-form RNA double helix in the single crystal structure of r(UGAGCUUCGGCUC). , 1998, Nucleic acids research.

[41]  D. Crothers,et al.  The solution structure of an RNA loop-loop complex: the ColE1 inverted loop sequence. , 1998, Structure.

[42]  N. Seeman,et al.  Design and self-assembly of two-dimensional DNA crystals , 1998, Nature.

[43]  C. Zhang,et al.  Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. , 1998, Molecular cell.

[44]  I. Tinoco,et al.  Use of ultra stable UNCG tetraloop hairpins to fold RNA structures: thermodynamic and spectroscopic applications. , 1995, Nucleic acids research.

[45]  N. Seeman,et al.  DNA double-crossover molecules. , 1993, Biochemistry.

[46]  N. Seeman,et al.  Synthesis from DNA of a molecule with the connectivity of a cube , 1991, Nature.

[47]  N. Seeman.  Nucleic acid junctions and lattices. , 1982, Journal of theoretical biology.

[48]  H R Drew,et al.  The anatomy of A-, B-, and Z-DNA. , 1982, Science.

[49]  D W Hukins,et al.  Structures of synthetic polynucleotides in the A-RNA and A'-RNA conformations: x-ray diffraction analyses of the molecular conformations of polyadenylic acid--polyuridylic acid and polyinosinic acid--polycytidylic acid. , 1973, Journal of molecular biology.