RNA self-assembly and RNA nanotechnology

Accounts of Chemical Research

Volumn 47, Issue 6, 2014, Pages 1871-1880

  Grabow, Wade W ^a   Jaeger, Luc ^b  

^a SEATTLE PACIFIC UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NANOSTRUCTURES; RIBOSWITCH; RNA;

CHEMISTRY; METHODS; NANOMEDICINE; NANOTECHNOLOGY; NUCLEIC ACID CONFORMATION; NUCLEOTIDE MOTIFS; RIBOSWITCH; THERMODYNAMICS;

NANOMEDICINE; NANOSTRUCTURES; NANOTECHNOLOGY; NUCLEIC ACID CONFORMATION; NUCLEOTIDE MOTIFS; RIBOSWITCH; RNA; THERMODYNAMICS;

EID: 84902593809     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar500076k     Document Type: Article

References (83)

1. Jaeger, L.; Calkins, E. R. Downward causation by information control in micro-organisms Interface Focus 2012, 2, 26-41
2. Collins, L. J.; Penny, D. The RNA infrastructure: Dark matter of the eukaryotic cell? Trends Genet. 2009, 25, 120-128
3. St Laurent, G.; Savva, Y. A.; Kapranov, P. Dark matter RNA: An intelligent scaffold for the dynamic regulation of the nuclear information landscape Front. Genet. 2012, 3, 57
4. Qu, H.; Fang, X. A brief review on the Human Encyclopedia of DNA Elements (ENCODE) project Genomics, Proteomics Bioinf. 2013, 11, 135-141
5. Afonin, K. A.; Lindsay, B.; Shapiro, B. A. Engineered RNA nanodesigns for applications in RNA nanotechnology DNA RNA Nanotechnol. 2013, 1, 1-15
6. Grabow, W.; Jaeger, L. RNA modularity for synthetic biology F1000Prime Rep. 2013, 5 46
7. Guo, P. The emerging field of RNA nanotechnology Nat. Nanotechnol 2010, 5, 833-842
8. Ishikawa, J.; Furuta, H.; Ikawa, Y. RNA tectonics (tectoRNA) for RNA nanostructure design and its application in synthetic biology Wiley Interdiscip Rev.: RNA 2013, 4, 651-664
9. Chakraborty, S.; Mehtab, S.; Krishnan, Y. The predictive power of synthetic nucleic acid technologies in RNA biology Acc. Chem. Res. 2014, 10.1021/ar400323d
10. Jaeger, L.; Leontis, N. B. Tecto-RNA: One-dimensional self-assembly through tertiary interactions Angew. Chem., Int. Ed. 2000, 14, 2521-2524
11. Chworos, A.; Severcan, I.; Koyfman, A. Y.; Weinkam, P.; Oroudjev, E.; Hansma, H. G.; Jaeger, L. Building programmable jigsaw puzzles with RNA Science 2004, 306, 2068-2072
12. Nasalean, L.; Baudrey, S.; Leontis, N. B.; Jaeger, L. Controlling RNA self-assembly to form filaments Nucleic Acids Res. 2006, 34, 1381-1392
13. Severcan, I.; Geary, C.; Verzemnieks, E.; Chworos, A.; Jaeger, L. Square-shaped RNA particles from different RNA folds Nano Lett. 2009, 9, 1270-1277
14. Severcan, I.; Geary, C.; Chworos, A.; Voss, N.; Jacovetty, E.; Jaeger, L. A polyhedron made of tRNAs Nat. Chem. 2010, 2, 772-779
15. Geary, C.; Chworos, A.; Jaeger, L. Promoting RNA helical stacking via A-minor junctions Nucleic Acids Res. 2011, 39, 1066-1080
16. Grabow, W. W.; Zakrevsky, P.; Afonin, K. A.; Chworos, A.; Shapiro, B. A.; Jaeger, L. Self-assembling RNA nanorings based on RNAI/II inverse kissing complexes Nano Lett. 2011, 11, 878-887
17. Ohno, H.; Kobayashi, T.; Kabata, R.; Endo, K.; Iwasa, T.; Yoshimura, S. H.; Takeyasu, K.; Inoue, T.; Saito, H. Synthetic RNA-protein complex shaped like an equilateral triangle Nat. Nanotechnol 2011, 6, 116-120
18. Shu, D.; Moll, W. D.; Deng, Z.; Mao, C.; Guo, P. Bottom-up assembly of RNA arrays and superstructures as potential parts in nanotechnology Nano Lett. 2004, 4, 1717-1723
19. Khaled, A.; Guo, S.; Li, F.; Guo, P. Controllable self-assembly of nanoparticles for specific delivery of multiple therapeutic molecules to cancer cells using RNA nanotechnology Nano Lett. 2005, 5, 1797-1808
20. Shu, Y.; Haque, F.; Shu, D.; Li, W.; Zhu, Z.; Kotb, M.; Lyubchenko, Y.; Guo, P. Fabrication of 14 different RNA nanoparticles for specific tumor targeting without accumulation in normal organs RNA 2013, 19, 767-777
21. Jaeger, L.; Chworos, A. The architectonics of programmable RNA and DNA nanostructures Curr. Opin. Struct. Biol. 2006, 16, 531-543
22. Butcher, S. E.; Pyle, A. M. The molecular interactions that stabilize RNA tertiary structure: RNA motifs, patterns, and networks Acc. Chem. Res. 2011, 44, 1302-1311
23. Leontis, N. B.; Lescoute, A.; Westhof, E. The building blocks and motifs of RNA architecture Curr. Opin. Struct. Biol. 2006, 16, 279-287
24. Lescoute, A.; Westhof, E. The interaction networks of structured RNAs Nucleic Acids Res. 2006, 34, 6587-6604
25. Jaeger, L.; Verzemnieks, E. J.; Geary, C. The UA-handle: A versatile submotif in stable RNA architectures Nucleic Acids Res. 2009, 37, 215-230
26. Grabow, W. W.; Zhuang, Z.; Shea, J. E.; Jaeger, L. The GA-minor submotif as a case study of RNA modularity, prediction, and design Wiley Interdiscip Rev.: RNA 2013, 4, 181-203
27. Draper, D. E. RNA folding: Thermodynamic and molecular descriptions of the roles of ions Biophys. J. 2008, 95, 5489-5495
28. Woodson, S. A. Compact intermediates in RNA folding Annu. Rev. Biophys. 2010, 39, 61-77
29. 2+ on the free energy landscape for folding a purine riboswitch RNA Biochemistry 2011, 50, 2790-2799
30. Ramakrishnan, V. Unraveling the structure of the ribosome (Nobel Lecture) Angew. Chem., Int. Ed. 2010, 49, 4355-4380
31. Yusupova, G.; Yusupov, M. High-resolution structure of the eukaryotic 80S ribosome Annu. Rev. Biochem. 2014, 10.1146/annurev-biochem-060713-035445
32. Massire, C.; Jaeger, L.; Westhof, E. Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis J. Mol. Biol. 1998, 279, 773-793
33. Torres-Larios, A.; Swinger, K. K.; Pan, T.; Mondragon, A. Structure of ribonuclease P - a universal ribozyme Curr. Opin. Struct. Biol. 2006, 16, 327-335
34. Lehnert, V.; Jaeger, L.; Michel, F.; Westhof, E. New loop-loop tertiary interactions in self-splicing introns of subgroup IC and ID: A complete 3D model of the Tetrahymena thermophila ribozyme Chem. Biol. 1996, 3, 993-1009
35. Stahley, M. R.; Strobel, S. A. RNA splicing: Group I intron crystal structures reveal the basis of splice site selection and metal ion catalysis Curr. Opin. Struct. Biol. 2006, 16, 319-326
36. Toor, N.; Keating, K. S.; Fedorova, O.; Rajashankar, K.; Wang, J.; Pyle, A. M. Tertiary architecture of the Oceanobacillus iheyensis group II intron RNA 2010, 16, 57-69
37. Marcia, M.; Somarowthu, S.; Pyle, A. M. Now on display: A gallery of group II intron structures at different stages of catalysis Mobile DNA 2013, 4 14
38. Will, C. L.; Luhrmann, R. Spliceosome structure and function Cold Spring Harb Perspect Biol. 2011, 3 a003707
39. Bindewald, E.; Hayes, R.; Yingling, Y. G.; Kasprzak, W.; Shapiro, B. A. RNAJunction: A database of RNA junctions and kissing loops for three-dimensional structural analysis and nanodesign Nucleic Acids Res. 2008, 36, D392-D397
40. Grabow, W. W.; Zhuang, Z.; Swank, Z. N.; Shea, J. E.; Jaeger, L. The right angle (RA) motif: A prevalent ribosomal RNA structural pattern found in group I introns J. Mol. Biol. 2012, 424, 54-67
41. Zhang, H.; Endrizzi, J. A.; Shu, Y.; Haque, F.; Sauter, C.; Shlyakhtenko, L. S.; Lyubchenko, Y.; Guo, P.; Chi, Y. I. Crystal structure of 3WJ core revealing divalent ion-promoted thermostability and assembly of the Phi29 hexameric motor pRNA RNA 2013, 19, 1226-1237
42. Bindewald, E.; Grunewald, C.; Boyle, B.; O'Connor, M.; Shapiro, B. A. Computational strategies for the automated design of RNA nanoscale structures from building blocks using NanoTiler J. Mol. Graphics Modell. 2008, 27, 299-308
43. Bindewald, E.; Afonin, K.; Jaeger, L.; Shapiro, B. A. Multistrand RNA secondary structure prediction and nanostructure design including pseudoknots ACS Nano 2011, 5, 9542-9551
44. Kasprzak, W.; Bindewald, E.; Kim, T. J.; Jaeger, L.; Shapiro, B. A. Use of RNA structure flexibility data in nanostructure modeling Methods 2011, 54, 239-250
45. Lee, J.; Kladwang, W.; Lee, M.; Cantu, D.; Azizyan, M.; Kim, H.; Limpaecher, A.; Yoon, S.; Treuille, A.; Das, R. RNA design rules from a massive open laboratory Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 2122-2127
46. Afonin, K. A.; Kasprzak, W. K.; Bindewald, E.; Kireeva, M.; Viard, M.; Kashlev, M.; Shapiro, B. A. In silico design and enzymatic synthesis of functional RNA nanoparticles Acc. Chem. Res. 2014, 10.1021/ar400329z
47. Afonin, K. A.; Cieply, D. J.; Leontis, N. B. Specific RNA self-assembly with minimal paranemic motifs J. Am. Chem. Soc. 2008, 130, 93-102
48. Afonin, K. A.; Bindewald, E.; Yaghoubian, A. J.; Voss, N.; Jacovetty, E.; Shapiro, B. A.; Jaeger, L. In vitro assembly of cubic RNA-based scaffolds designed in silico Nat. Nanotechnol 2010, 5, 676-682
49. Dibrov, S. M.; McLean, J.; Parsons, J.; Hermann, T. Self-assembling RNA square Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 6405-6408
50. Khisamutdinov, E. F.; Jasinski, D. L.; Guo, P. RNA as a Boiling-Resistant Anionic Polymer Material To Build Robust Structures with Defined Shape and Stoichiometry ACS Nano 2014, 10.1021/nn5006254
51. Koyfman, A. Y.; Braun, G.; Magonov, S.; Chworos, A.; Reich, N. O.; Jaeger, L. Controlled spacing of cationic gold nanoparticles by nanocrown RNA J. Am. Chem. Soc. 2005, 127, 11886-11887
52. Busi, F.; Cayrol, B.; Lavelle, C.; LeDerout, J.; Pietrement, O.; Le Cam, E.; Geinguenaud, F.; Lacoste, J.; Regnier, P.; Arluison, V. Auto-assembly as a new regulatory mechanism of noncoding RNA Cell Cycle 2009, 8, 952-954
53. Cayrol, B.; Nogues, C.; Dawid, A.; Sagi, I.; Silberzan, P.; Isambert, H. A nanostructure made of a bacterial noncoding RNA J. Am. Chem. Soc. 2009, 131, 17270-17276
54. Delebecque, C. J.; Lindner, A. B.; Silver, P. A.; Aldaye, F. A. Organization of intracellular reactions with rationally designed RNA assemblies Science 2011, 333, 470-474
55. Ke, Y.; Ong, L. L.; Shih, W. M.; Yin, P. Three-dimensional structures self-assembled from DNA bricks Science 2012, 338, 1177-1183
56. Afonin, K. A.; Desai, R.; Viard, M.; Kireeva, M. L.; Bindewald, E.; Case, C. L.; Maciag, A. E.; Kasprzak, W. K.; Kim, T.; Sappe, A.; Stepler, M.; Kewalramani, V. N.; Kashlev, M.; Blumenthal, R.; Shapiro, B. A. Co-transcriptional production of RNA-DNA hybrids for simultaneous release of multiple split functionalities Nucleic Acids Res. 2014, 42, 2085-2097
57. Afonin, K. A.; Viard, M.; Martins, A. N.; Lockett, S. J.; Maciag, A. E.; Freed, E. O.; Heldman, E.; Jaeger, L.; Blumenthal, R.; Shapiro, B. A. Activation of different split functionalities on re-association of RNA-DNA hybrids Nat. Nanotechnol 2013, 8, 296-304
58. Lee, H.; Lytton-Jean, A. K.; Chen, Y.; Love, K. T.; Park, A. I.; Karagiannis, E. D.; Sehgal, A.; Querbes, W.; Zurenko, C. S.; Jayaraman, M.; Peng, C. G.; Charisse, K.; Borodovsky, A.; Manoharan, M.; Donahoe, J. S.; Truelove, J.; Nahrendorf, M.; Langer, R.; Anderson, D. G. Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery Nat. Nanotechnol 2012, 7, 389-393
59. Ko, S. H.; Su, M.; Zhang, C.; Ribbe, A. E.; Jiang, W.; Mao, C. Synergistic self-assembly of RNA and DNA molecules Nat. Chem. 2010, 2, 1050-1055
60. Endo, M.; Yamamoto, S.; Tatsumi, K.; Emura, T.; Hidaka, K.; Sugiyama, H. RNA-templated DNA origami structures Chem. Commun. 2013, 49, 2879-2881
61. Wang, P.; Ko, S. H.; Tian, C.; Hao, C.; Mao, C. RNA-DNA hybrid origami: folding of a long RNA single strand into complex nanostructures using short DNA helper strands Chem. Commun. 2013, 49, 5462-5464
62. Zheng, H. N.; Ma, Y. Z.; Xiao, S. J. Periodical assembly of repetitive RNA sequences synthesized by rolling circle transcription with short DNA staple strands to RNA-DNA hybrid nanowires Chem. Commun. 2014, 50, 2100-2103
63. Afonin, K. A.; Kireeva, M.; Grabow, W. W.; Kashlev, M.; Jaeger, L.; Shapiro, B. A. Co-transcriptional assembly of chemically modified RNA nanoparticles functionalized with siRNAs Nano Lett. 2012, 12, 5192-5195
64. Lee, J. B.; Hong, J.; Bonner, D. K.; Poon, Z.; Hammond, P. T. Self-assembled RNA interference microsponges for efficient siRNA delivery Nat. Mater. 2012, 11, 316-322
65. Ban, N.; Nissen, P.; Hansen, J.; Moore, P. B.; Steitz, T. A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution Science 2000, 289, 905-920
66. Cate, J. H.; Gooding, A. R.; Podell, E.; Zhou, K.; Golden, B. L.; Kundrot, C. E.; Cech, T. R.; Doudna, J. A. Crystal structure of a group I ribozyme domain: principles of RNA packing Science 1996, 273, 1678-1685
67. Yingling, Y. G.; Shapiro, B. A. Computational design of an RNA hexagonal nanoring and an RNA nanotube Nano Lett. 2007, 7, 2328-2334
68. Guo, P.; Zhang, C.; Chen, C.; Garver, K.; Trottier, M. Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation Mol. Cell 1998, 2, 149-155
69. Jaeger, L.; Westhof, E.; Leontis, N. B. TectoRNA: Modular assembly units for the construction of RNA nano-objects Nucleic Acids Res. 2001, 29, 455-463
70. Geary, C.; Baudrey, S.; Jaeger, L. Comprehensive features of natural and in vitro selected GNRA tetraloop-binding receptors Nucleic Acids Res. 2008, 36, 1138-1152
71. Klein, D. J.; Schmeing, T. M.; Moore, P. B.; Steitz, T. A. The kink-turn: A new RNA secondary structure motif EMBO J. 2001, 20, 4214-4221
72. Liu, J.; Guo, S.; Cinier, M.; Shlyakhtenko, L. S.; Shu, Y.; Chen, C.; Shen, G.; Guo, P. Fabrication of stable and RNase-resistant RNA nanoparticles active in gearing the nanomotors for viral DNA packaging ACS Nano 2011, 5, 237-246
73. Wittmann, A.; Suess, B. Engineered riboswitches: Expanding researchers' toolbox with synthetic RNA regulators FEBS Lett. 2012, 586, 2076-2083
74. Ceres, P.; Garst, A. D.; Marcano-Velazquez, J. G.; Batey, R. T. Modularity of select riboswitch expression platforms enables facile engineering of novel genetic regulatory devices ACS Synth. Biol. 2013, 2, 463-472
75. Hall, B.; Micheletti, J. M.; Satya, P.; Ogle, K.; Pollard, J.; Ellington, A. D. Design, synthesis, and amplification of DNA pools for in vitro selection. Current Protocols in Nucleic Acid Chemistry 2009, 39, 9.2.1 - 9.2.28.
76. Chen, X.; Li, N.; Ellington, A. D. Ribozyme catalysis of metabolism in the RNA world Chem. Biodivers. 2007, 4, 633-655
77. Jaeger, L. The new world of ribozymes Curr. Opin. Struct. Biol. 1997, 7, 324-35
78. Zimmermann, B.; Bilusic, I.; Lorenz, C.; Schroeder, R. Genomic SELEX: A discovery tool for genomic aptamers Methods 2010, 52, 125-132
79. Ishikawa, J.; Furuta, H.; Ikawa, Y. An in vitro-selected RNA receptor for the GAAC loop: modular receptor for non-GNRA-type tetraloop Nucleic Acids Res. 2013, 41, 3748-3759
80. Goler, J. A.; Carothers, J. M.; Keasling, J. D. Dual-selection for evolution of in vivo functional aptazymes as riboswitch parts Methods Mol. Biol. 2014, 1111, 221-235
81. Behrouzi, R.; Roh, J. H.; Kilburn, D.; Briber, R. M.; Woodson, S. A. Cooperative tertiary interaction network guides RNA folding Cell 2012, 149, 348-357
82. Stern, S. T.; McNeil, S. E. Nanotechnology safety concerns revisited Toxicol. Sci. 2008, 101, 4-21
83. Singh, S.; Sharma, A.; Robertson, G. P. Realizing the clinical potential of cancer nanotechnology by minimizing toxicologic and targeted delivery concerns Cancer Res. 2012, 72, 5663-5668