Fabrication of 14 different RNA nanoparticles for specific tumor targeting without accumulation in normal organs

RNA

Volumn 19, Issue 6, 2013, Pages 767-777

  Shu, Yi ^a   Haque, Farzin ^a   Shu, Dan ^a   Li, Wei ^b   Zhu, Zhenqi ^c   Kotb, Malak ^c   Lyubchenko, Yuri ^d   Guo, Peixuan ^a  

^a University of Kentucky   (United States)

^b University of Cincinnati   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Bacteriophage phi29; Nanobiotechnology; RNA nanoparticle; RNA nanotechnology; RNA therapeutics; Target delivery

Indexed keywords

NANOPARTICLE; RIBONUCLEASE; RIBOZYME; RNA; RNA NANOPARTICLE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DIMERIZATION; DISSOCIATION; GENE SILENCING; HEPATITIS B VIRUS; MOLECULAR INTERACTION; MOLECULARLY TARGETED THERAPY; MOUSE; NANOFABRICATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; RNA CONFORMATION; RNA DEGRADATION; RNA FOLDING; RNA STABILITY; RNA STRUCTURE; RNA SYNTHESIS; STOICHIOMETRY;

BACTERIOPHAGE PHI29; NANOBIOTECHNOLOGY; RNA NANOPARTICLE; RNA NANOTECHNOLOGY; RNA THERAPEUTICS; TARGET DELIVERY;

ANIMALS; BASE SEQUENCE; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; GENE SILENCING; GENETIC THERAPY; INVERTED REPEAT SEQUENCES; MALE; MICE; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; NANOPARTICLES; NANOTECHNOLOGY; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NEOPLASMS, EXPERIMENTAL; NUCLEOTIDE MOTIFS; RNA; RNA FOLDING; RNA STABILITY; STRUCTURE-ACTIVITY RELATIONSHIP; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84878025754     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.037002.112     Document Type: Article

References (88)

1. Abdelmawla S, Guo S, Zhang L, Pulukuri S, Patankar P, Conley P, Trebley J, Guo P, Li QX. 2011. Pharmacological characterization of chemically synthesized monomeric pRNA nanoparticles for systemic delivery. Mol Ther 19: 1312-1322.
2. Afonin KA, Grabow WW, Walker FM, Bindewald E, Dobrovolskaia MA, Shapiro BA, Jaeger L. 2011. Design and self-assembly of siRNA-functionalized RNA nanoparticles for use in automated nanomedicine. Nat Protoc 6: 2022-2034.
3. Altinoglu EI, Russin TJ, Kaiser JM, Barth BM, Eklund PC, Kester M, Adair JH. 2008. Near-infrared emitting fluorophore-doped calcium phosphate nanoparticles for in vivo imaging of human breast cancer. ACS Nano 2: 2075-2084.
4. Balzani V, Credi A, Venturi M. 2002. The bottom-up approach to molecular-level devices and machines. Chemistry 8: 5524-5532.
5. Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
6. Barth BM, Sharma R, Altinoglu EI, Morgan TT, Shanmugavelandy SS, Kaiser JM, McGovern C, Matters GL, Smith JP, Kester M, et al. 2010. Bioconjugation of calcium phosphosilicate composite nanoparticles for selective targeting of human breast and pancreatic cancers in vivo. ACS Nano 4: 1279-1287.
7. Baugh C, Grate D, Wilson C. 2000. 2.8 Å crystal structure of the malachite green aptamer. J Mol Biol 301: 117-128.
8. Bindewald E, Hayes R, Yingling YG, Kasprzak W, Shapiro BA. 2008. RNAJunction: A database of RNA junctions and kissing loops for three-dimensional structural analysis and nanodesign. Nucleic Acids Res 36: D392-D397.
9. Brummelkamp TR, Bernards R, Agami R. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553. (Pubitemid 34408678)
10. Cairns J, Overbaugh J, Miller S. 1988. The origin of mutants. Nature 335: 142-145.
11. Carmichael GG. 2002. Medicine: Silencing viruses with RNA. Nature 418: 379-380.
12. Chang KY, Tinoco I Jr. 1994. Characterization of a "kissing" hairpin complex derived from the human immunodeficiency virus genome. Proc Natl Acad Sci 91: 8705-8709.
13. Chen C, Zhang C, Guo P. 1999. Sequence requirement for hand-in-hand interaction in formation of pRNA dimers and hexamers to gear φ29 DNA translocation motor. RNA 5: 805-818. (Pubitemid 29283782)
14. Chen C, Sheng S, Shao Z, Guo P. 2000. A dimer as a building block in assembling RNA: A hexamer that gears bacterial virus phi29 DNA-translocating machinery. J Biol Chem 275: 17510-17516. (Pubitemid 30430792)
15. Chowrira BM, Berzal-Herranz A, Burke JM. 1991. Novel guanosine requirement for catalysis by the hairpin ribozyme. Nature 354: 320-322. (Pubitemid 21896887)
16. Clever JL, Wong ML, Parslow TG. 1996. Requirements for kissing-loop-mediated dimerization of human immunodeficency virus RNA. J Virol 70: 5902-5908. (Pubitemid 26266802)
17. Coleman J, Hirashima A, Inocuchi Y, Green PJ, Inouye M. 1985. A novel immune system against bacteriophage infection using complementary RNA (micRNA). Nature 315: 601-603. (Pubitemid 15021203)
18. Duchaine TF, Slack FJ. 2009. RNA interference and micro-RNA-oriented therapy in cancer: Rationales, promises, and challenges. Curr Oncol 16: 265-270.
19. Ellington AD, Szostak JW. 1990. In vitro selection of RNA molecules that bind specific ligands. Nature 346: 818-822.
20. Fabian MR, Sonenberg N, Filipowicz W. 2010. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351-379.
21. Garver K, Guo P. 1997. Boundary of pRNA functional domains and minimum pRNA sequence requirement for specific connector binding and DNA packaging of phage φ29. RNA 3: 1068-1079.
22. Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: An expanding universe. Nat Rev Genet 10: 94-108.
23. Gold L. 1995. The SELEX process: A surprising source of therapeutic and diagnostic compounds. Harvey Lect 91: 47-57.
24. Grabow WW, Zakrevsky P, Afonin KA, Chworos A, Shapiro BA, Jaeger L. 2011. Self-assembling RNA nanorings based on RNAI/II inverse kissing complexes. Nano Lett 11: 878-887.
25. Guo P. 2010. The emerging field of RNA nanotechnology. Nat Nanotechnol 5: 833-842.
26. Guo P, Erickson S, Anderson D. 1987. A small viral RNA is required for in vitro packaging of bacteriophage φ29 DNA. Science 236: 690-694. (Pubitemid 17076855)
27. Guo P, Zhang C, Chen C, Trottier M, Garver K. 1998. Inter-RNA interaction of phage φ29 pRNA to form a hexameric complex for viral DNA transportation. Mol Cell 2: 149-155. (Pubitemid 128378977)
28. Guo S, Tschammer N, Mohammed S, Guo P. 2005. Specific delivery of therapeutic RNAs to cancer cells via the dimerization mechanism of phi29 motor pRNA. Hum Gene Ther 16: 1097-1109. (Pubitemid 41324569)
29. Guo S, Huang F, Guo P. 2006. Construction of folate-conjugated pRNA of bacteriophage phi29 DNA packaging motor for delivery of chimeric siRNA to nasopharyngeal carcinoma cells. Gene Ther 13: 814-820.
30. Guo P, Coban O, Snead NM, Trebley J, Hoeprich S, Guo S, Shu Y. 2010. Engineering RNA for targeted siRNA delivery and medical application. Adv Drug Deliv Rev 62: 650-666.
31. Guo P, Haque F, Hallahan B, Reif R, Li H. 2012a. Uniqueness, advantages, challenges, solutions, and perspectives in therapeutics applying RNA nanotechnology. Nucleic Acid Ther 22: 226-245.
32. Guo P, Shu Y, Binzel D, Cinier M. 2012b. Synthesis, conjugation, and labeling of multifunctional pRNA nanoparticles for specific delivery of siRNA, drugs and other therapeutics to target cells. Methods Mol Biol 928: 197-219.
33. Hansma HG, Oroudjev E, Baudrey S, Jaeger L. 2003. TectoRNA and "kissing-loop " RNA: Atomic force microscopy of self-assembling RNA structures. J Microsc 212: 273-279. (Pubitemid 38028525)
34. Haque F, Shu D, Shu Y, Shlyakhtenko L, Rychahou P, Evers M, Guo P. 2012. Ultrastable synergistic tetravalent RNA nanoparticles for targeting to cancers. Nano Today 7: 245-257.
35. He L, Hannon GJ. 2004. MicroRNAs: Small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522-531. (Pubitemid 38868508)
36. Henkin TM. 2008. Riboswitch RNAs: Using RNA to sense cellular metabolism. Genes Dev 22: 3383-3390.
37. Hoeprich S, Zhou Q, Guo S, Qi G, Wang Y, Guo P. 2003. Bacterial virus phi29 pRNA as a hammerhead ribozyme escort to destroy hepatitis B virus. Gene Ther 10: 1258-1267. (Pubitemid 36934728)
38. Jacque JM, Triques K, Stevenson M. 2002. Modulation of HIV-1 replication by RNA interference. Nature 418: 435-438. (Pubitemid 34826845)
39. Jaeger L, Leontis NB. 2000. Tecto-RNA: One-dimensional self-assembly through tertiary interactions. Angew Chem Int Ed Engl 39: 2521-2524. (Pubitemid 30602533)
40. Khaled A, Guo S, Li F, Guo P. 2005. Controllable self-assembly of nanoparticles for specific delivery of multiple therapeutic molecules to cancer cells using RNA nanotechnology. Nano Letters 5: 1797-1808. (Pubitemid 41396168)
41. Knecht DA, Loomis WF. 1987. Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236: 1081-1086. (Pubitemid 17113249)
42. Lee RJ, Low PS. 1994. Delivery of liposomes into cultured KB cells via folate receptor-mediated endocytosis. J Biol Chem 269: 3198-3204. (Pubitemid 24237629)
43. Lee H, Lytton-Jean AK, Chen Y, Love KT, Park AI, Karagiannis ED, Sehgal A, Querbes W, Zurenko CS, Jayaraman M, et al. 2012a. Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery. Nat Nanotechnol 7: 389-393.
44. Lee JB, Hong J, Bonner DK, Poon Z, Hammond PT. 2012b. Self-assembled RNA interference microsponges for efficient siRNA delivery. Nat Mater 11: 316-322.
45. Lee SJ, Huh MS, Lee SY, Min S, Lee S, Koo H, Chu JU, Lee KE, Jeon H, Choi Y, et al. 2012c. Tumor-homing poly-siRNA/glycol chitosan self-cross-linked nanoparticles for systemic siRNA delivery in cancer treatment. Angew Chem Int Ed Engl 51: 7203-7207.
46. Leontis NB, Lescoute A, Westhof E. 2006. The building blocks and motifs of RNA architecture. Curr Opin Struct Biol 16: 279-287. (Pubitemid 43831653)
47. Li H, Li WX, Ding SW. 2002. Induction and suppression of RNA silencing by an animal virus. Science 296: 1319-1321. (Pubitemid 34522787)
48. Lilley DM. 2000. Structures of helical junctions in nucleic acids. Q Rev Biophys 33: 109-159.
49. Liu J, Guo S, Cinier M, Shlyakhtenko L, Shu Y, Chen C, Shen G, Guo P. 2010. Fabrication of stable and RNase-resistant RNA nanoparticles active in gearing the nanomotors for viral DNA packaging. ACS Nano 5: 237-246.
50. Lu Y, Low PS. 2002. Folate-mediated delivery of macromolecular anticancer therapeutic agents. Adv Drug Deliv Rev 54: 675-693. (Pubitemid 35247522)
51. Lyubchenko YL, Shlyakhtenko LS. 2009. AFM for analysis of structure and dynamics of DNA and protein-DNA complexes. Methods 47: 206-213.
52. Ma Y, Sadoqi M, Shao J. 2012. Biodistribution of indocyanine green-loaded nanoparticles with surface modifications of PEG and folic acid. Int J Pharm 436: 25-31.
53. Mujeeb A, Clever JL, Billeci TM, James TL, Parslow TG. 1998. Structure of the dimer initiation complex of HIV-1 genomic RNA. Nat Struct Biol 5: 432-436. (Pubitemid 28265024)
54. Nakashima Y, Abe H, Abe N, Aikawa K, Ito Y. 2011. Branched RNA nanostructures for RNA interference. Chem Commun (Camb) 47: 8367-8369.
55. Nilsen TW. 2007. RNA 1997-2007: A remarkable decade of discovery. Mol Cell 28: 715-720. (Pubitemid 350217065)
56. Ogawa A, Maeda M. 2008. An artificial aptazyme-based riboswitch and its cascading system in E. coli. Chembiochem 9: 206-209. (Pubitemid 351196787)
57. Ohno H, Kobayashi T, Kabata R, Endo K, Iwasa T, Yoshimura SH, Takeyasu K, Inoue T, Saito H. 2011. Synthetic RNA-protein complex shaped like an equilateral triangle. Nat Nanotechnol 6: 116-120.
58. Prats AC, Roy C, Wang PA, Erard M, Housset V, Gabus C, Paoletti C, Darlix JL. 1990. cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J Virol 64: 774-783. (Pubitemid 20032694)
59. Reid RJD, Bodley JW, Anderson D. 1994a. Characterization of the prohead-pRNA interaction of bacteriophage phi29. J Biol Chem 269: 5157-5162. (Pubitemid 24239507)
60. Reid RJD, Bodley JW, Anderson D. 1994b. Identification of bacteriophage phi29 prohead RNA (pRNA) domains necessary for in vitro DNA-gp3 packaging. J Biol Chem 269: 9084-9089.
61. Reid RJD, Zhang F, Benson S, Anderson D. 1994c. Probing the structure of bacteriophage phi29 prohead RNA with specific mutations. J Biol Chem 269: 18656-18661. (Pubitemid 24224108)
62. Reif R, Haque F, Guo P. 2013. Fluorogenic RNA nanoparticles for monitoring RNA folding and degradation in real time in living cells. Nucleic Acid Ther 22: 428-437.
63. Sarver N, Cantin EM, Chang PS, Zaia JA, Ladne PA, Stephens DA, Rossi JJ. 1990. Ribozymes as potential anti-HIV-1 therapeutic agents. Science 247: 1222-1225.
64. Schmidt OG, Eberl K. 2001. Nanotechnology: Thin solid films roll up into nanotubes. Nature 410: 168. (Pubitemid 32216580)
65. Schroeder KT, McPhee SA, Ouellet J, Lilley DM. 2010. A structural database for k-turn motifs in RNA. RNA 16: 1463-1468.
66. Seeman NC, Belcher AM. 2002. Emulating biology: Building nanostructures from the bottom up. Proc Natl Acad Sci 99 (Suppl 2): 6451-6455. (Pubitemid 34492349)
67. Shu D, Huang L, Hoeprich S, Guo P. 2003. Construction of phi29 DNA-packaging RNA (pRNA) monomers, dimers, and trimers with variable sizes and shapes as potential parts for nanodevices. J Nanosci Nanotechnol 3: 295-302. (Pubitemid 38597291)
68. Shu D, Moll WD, Deng Z, Mao C, Guo P. 2004. Bottom-up assembly of RNA arrays and superstructures as potential parts in nanotechnology. Nano Lett 4: 1717-1723. (Pubitemid 39297452)
69. Shu D, Zhang H, Jin J, Guo P. 2007. Counting of six pRNAs of phi29 DNA-packaging motor with customized single molecule dual-view system. EMBO J 26: 527-537. (Pubitemid 46160952)
70. Shu D, Shu Y, Haque F, Abdelmawla S, Guo P. 2011a. Thermodynamically stable RNA three-way junctions for constructing multifuntional nanoparticles for delivery of therapeutics. Nat Nanotechnol 6: 658-667.
71. Shu Y, Cinier M, Fox SR, Ben-Johnathan N, Guo P. 2011b. Assembly of therapeutic pRNA-siRNA nanoparticles using bipartite approach. Mol Ther 19: 1304-1311.
72. Shu Y, Cinier M, Shu D, Guo P. 2011c. Assembly of multifunctional phi29 pRNA nanoparticles for specific delivery of siRNA and other therapeutics to targeted cells. Methods 54: 204-214.
73. Shukla GC, Haque F, Tor Y, Wilhelmsson LM, Toulme JJ, Isambert H, Guo P, Rossi JJ, Tenenbaum SA, Shapiro BA. 2011. A boost for the emerging field of RNA nanotechnology. ACS Nano 5: 3405-3418.
74. Srisawat C, Engelke DR. 2001. Streptavidin aptamers: Affinity tags for the study of RNAs and ribonucleoproteins. RNA 7: 632-641. (Pubitemid 32416820)
75. Strobel SA, Cochrane JC. 2007. RNA catalysis: Ribozymes, ribosomes, and riboswitches. Curr Opin Chem Biol 11: 636-643. (Pubitemid 350180571)
76. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411-413. (Pubitemid 352029978)
77. Tuerk C, Gold L. 1990. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249: 505-510.
78. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, et al. 2002. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419: 624-629.
79. Wagner C, Ehresmann C, Ehresmann B, Brunel C. 2004. Mechanism of dimerization of bicoid mRNA: Initiation and stabilization. J Biol Chem 279: 4560-4569. (Pubitemid 38199047)
80. Westhof E. 2012. Ribozymes, catalytically active RNA molecules. Introduction. Methods Mol Biol 848: 1-4.
81. Wiedenheft B, Sternberg SH, Doudna JA. 2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482: 331-338.
82. Wilcox CL, Crnic LS, Pizer LI. 1992. Replication, latent infection and reactivation in neuronal culture with a herpes simplex virus thymidine kinase-negative mutant. Virology 187: 348-352.
83. Xiao F, Sun J, Coban O, Schoen P, Wang JC, Cheng RH, Guo P. 2009a. Fabrication of massive sheets of single layer patterned arrays using lipid directed reengineered phi29 motor dodecamer. ACS Nano 3: 100-107.
84. Xiao F, Cai Y, Wang JC, Green D, Cheng RH, Demeler B, Guo P. 2009b. Adjustable ellipsoid nanoparticles assembled from re-engineered connectors of the bacteriophage phi29 DNA packaging motor. ACS Nano 3: 2163-2170.
85. Xiao F, Demeler B, Guo P. 2010. Assembly mechanism of the sixty-subunit nanoparticles via interaction of RNA with the reengineered protein connector of phi29 DNA-packaging motor. ACS Nano 4: 3293-3301.
86. Yingling YG, Shapiro BA. 2007. Computational design of an RNA hexagonal nanoring and an RNA nanotube. Nano Lett 7: 2328-2334. (Pubitemid 47310128)
87. Zhang CL, Lee C-S, Guo P. 1994. The proximate 5′ and 3′ ends of the 120-base viral RNA (pRNA) are crucial for the packaging of bacteriophage f29 DNA. Virology 201: 77-85.
88. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415. (Pubitemid 37442169)