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RNA Tectonics (tectoRNA) for RNA nanostructure design and its application in synthetic biology

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RNA molecules are versatile biomaterials that act not only as DNA‐like genetic materials but also have diverse functions in regulation of cellular biosystems. RNA is capable of regulating gene expression by sequence‐specific hybridization. This feature allows the design of RNA‐based artificial gene regulators (riboregulators). RNA can also build complex two‐dimensional (2D) and 3D nanostructures, which afford protein‐like functions and make RNA an attractive material for nanobiotechnology. RNA tectonics is a methodology in RNA nanobiotechnology for the design and construction of RNA nanostructures/nanoobjects through controlled self‐assembly of modular RNA units (tectoRNAs). RNA nanostructures designed according to the concept of RNA tectonics are also attractive as tools in synthetic biology, but in vivo RNA tectonics is still in the early stages. This review presents a summary of the achievements of RNA tectonics and its related researches in vitro, and also introduces recent developments that facilitated the use of RNA nanostructures in bacterial cells. WIREs RNA 2013, 4:651–664. doi: 10.1002/wrna.1185 This article is categorized under: RNA Structure and Dynamics > RNA Structure, Dynamics, and Chemistry RNA Methods > RNA Analyses In Vitro and In Silico

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2D RNA nanostructures designed for in vivo assembly. Schematic illustration of RNA strand (d1) and its self‐dimerization to form the RNA unit tile (d1‐1). Self‐assembly of the RNA unit tiles to form nanotubes and nanoarrays. Schematic illustration of the protile that forms by self‐dimerization of the RNA strand (d2a) and the RNA strand (d2-2) that decorates the protile to form the mature tile. Self‐assembly of the mature unit tiles organizes 2D nanostructures. (Reprinted with permission from Ref . Copyright 2011 AAAS).
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Polyhedral RNA 3D structures. (a) TectoRNA 3D antiprism. Step‐1: Schematic of formation of the tectoRNA antiprism by assembling a pair of tRNA squares via four tail–tail interactions. Step‐2: Oligomerization of the tectoRNA 3D antiprisms through biotin–streptavidin interactions. (Reprinted with permission from Ref . Copyright 2010 Macmillan Publishers Ltd). (b) RNA nanocubes. Development views of RNA nanocubes composed of 6 (left) and 10 (right) RNA strands. Each edge of the nanocube is made up of an RNA duplex. RNA nanocubes have 6 (left) or 10 (right) dangling ends, into which functional modifications can be introduced. Each broken line indicates Watson–Crick base pairs between two RNA regions forming one edge in the cube structure. (Reprinted with permission from Ref . Copyright 2010 Macmillan Publishers Ltd).
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RNA polygons assembled with tail–tail interactions. (a) Schematic illustration of the self‐assembling RNA square composed of four copies of the L‐shaped unit consisting of two RNA strands. (b) 3D crystal structure of the RNA square. Four L‐shaped unit RNAs are shown in different colors. (c) Schematic illustration of the equilateral RNA triangle, each corner of which is composed of the K‐turn motif recognized by the L7Ae protein.
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RNA nanoring assembled with the angled kissing loop (KL) complex. (a) Schematic of the angled KL complex (RNAI/IIi KL complex). (b) 3D nuclear magnetic resonance (NMR) structure of the angled KL complex (RNAI/IIi KL complex). (c) Schematic illustration of the hexameric RNA nanoring appending six siRNAs. Selective hexamerization was guided by six orthogonal KL complexes. (d) Schematic of the prohead RNA (pRNA) monomer unit. Nucleotides shown in red are responsible for inter‐unit base pairs (KL‐like interactions). The region shown without sequence is dispensable for oligomer formation and so it was deleted in pRNAmini for crystallization and was also modified with functional RNA modules. (e) 3D crystal structure of a closed tetramer of a shortened derivative of pRNA (pRNAmini). Four pRNAmini unit RNAs are shown in different colors.
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LRtectoRNAs. (a) Schematic representation of the association and dissociation of the tectoRNA possessing a GNRA loop and its receptor motif in a monomer RNA. (b) Association between the tectoRNA monomer with two GNRA receptors and a monomer with two GNRA tetraloops. (c) (top) Schematic of two alternative conformers of H‐shaped tectoRNA (molecule 1) due to alternative stacking of the 4WJ. (bottom left) Conformer B selectively oligomerizes in the anti‐parallel conformation. (bottom right) Conformer A forms oligomers with two different (parallel and anti‐parallel) association modes. It should be noted that the two assembly modes are able to coexist in a single oligomer filament. (Reprinted with permission from Ref . Copyright 2006 Oxford University Press). (d) Restriction of the oligomerization‐proficient conformer (A or B) by modulation of the lengths of the four stems (stem i to stem iv). (Reprinted with permission from Ref . Copyright 2006 Oxford University Press). (e) Restriction of the assembly mode in Conformer A using two orthogonal pairs of GNRA loops and their receptor motifs. (Reprinted with permission from Ref . Copyright 2006 Oxford University Press). (f) The H‐shaped tectoRNA (molecule 2) that selectively oligomerizes through Conformer B. (Reprinted with permission from Ref . Copyright 2006 Oxford University Press). (g) The H‐shaped tectoRNA (molecule 3) that selectively oligomerizes through the anti‐parallel mode of Conformer A. (h) The H‐shaped tectoRNAs (molecules 4, 5, and 6) that preferentially form closed ring oligomers through the parallel mode of Conformer A.
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KLtectoRNAs. (a) A basic KLtectoRNA monomer designed by Harada and coworkers. Two terminal loops in the unit RNA form a kissing loop (KL) interaction with the loops in another unit RNA resulting in homooligomer formation. (b) Schematic illustration of open linear (top) and closed ring (bottom) assemblies of KLtectoRNAs. (c) Thermo‐induced structural rearrangement of a KLtectoRNA dimer (top) to an extended duplex with a peptide recognition motif (bottom). (d) Schematic illustration of the RNA square composed of four KLtectoRNA monomers with 90° corner motifs. (e) KLtectoRNA units with three classes of 90° corner motifs. (f) Examples of controlled assemblies of tectoRNA squares. Assemblies were controlled by programmed duplex formation of the single‐stranded connector tails. (Reprinted with permission from Ref . Copyright 2004 AAAS).
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Synthetic TRtectoRNA biochemistry. Conversion of tectoRNA to functional RNA that promotes chemical bond‐forming reactions by installing functional modules. (top line) Step‐1: Conversion of homodimeric tectoRNA to heterodimeric tectoRNA to differentiate the substrate unit and catalytic unit. Step‐2: Installation of a substrate unit (a break in the RNA strand to be joined by ligase activity) and a catalytic module that promotes RNA–RNA joining reaction. Step‐3: Conversion of a modular ligase ribozyme (transDSL ribozyme) and its substrate to a pair of cross‐ligation/replication ribozymes, in which a fragmented ribozyme served as a substrate to be joined by the partner ribozyme. (bottom line) Step‐a: Installation of two peptide recognition motifs (PRM‐1 and PRM‐2) to the homodimeric tectoRNA. Step‐b: Recognition of a pair of substrate peptides (peptide‐1 and peptide‐2) by PRM‐1 and PRM‐2 to organize two peptide ligation modules, in which the two reactive termini of substrate peptides were fixed in close proximity to facilitate chemical ligation.
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