MS2 viruslike particles: A robust, semisynthetic targeted drug delivery platform

Molecular Pharmaceutics

Volumn 10, Issue 1, 2013, Pages 59-68

  Galaway, Francis A ^a,b   Stockley, Peter G ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

MS2; nanoparticle targeting; siRNA delivery; virus assembly

Indexed keywords

DOUBLE STRANDED RNA; NUCLEASE; SMALL INTERFERING RNA; TRANSFERRIN; VIRUS PROTEIN;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; COVALENT BOND; DRUG DELIVERY SYSTEM; ENDOCYTOSIS; FLUORESCENCE; HELA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LIPID TRANSPORT; MS2 VIRUS; NONHUMAN; PRIORITY JOURNAL; VIRION; VIRUS CAPSID;

CAPSID; CAPSID PROTEINS; CELL LINE, TUMOR; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; GENETIC VECTORS; HELA CELLS; HUMANS; LEVIVIRUS; RNA PHAGES; RNA, SMALL INTERFERING; TRANSFECTION; TRANSFERRIN; VIRION;

EID: 84872139457     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp3003368     Document Type: Article

References (44)

1. Ruiz-Garcia, A.; Bermejo, M.; Moss, A.; Casabo, V. G. Pharmacokinetics in Drug Discovery Development 2008, 97, 654-690
2. Voegtlin, C. The pharmacology of arsphenamine (salvarsan) and related arsenicals Physiol. Rev. 1925, 5, 63-94
3. Ehrlich, P.; Bertheim, A. Reduction products of arsanilic acid and its derivatives-First announcement: p-aminophenyl-arsenoxide Ber. Dtsch. Chem. Ges. 1910, 43, 917-927
4. Wagner, R. W. Gene inhibition using antisense oligodeoxynucleotides Nature 1994, 372, 333-335
5. Wagner, E.; Curiel, D.; Cotten, M. Delivery of drugs, proteins and genes into cells using using transferrin as a ligand for receptor-mediated endocytosis Adv. Drug Delivery Rev. 1994, 14, 113-135
6. Allen, T. M.; Cullis, P. R. Drug delivery systems: entering the mainstream Science 2004, 303, 1818-1822
7. Wu, M.; Brown, W. L.; Stockley, P. G. Cell-specific delivery of bacteriophage-encapsidated ricin A chain Bioconjugate Chem. 1995, 6, 587-595
8. Mastico, R. A.; Talbot, S. J.; Stockley, P. G. Multiple presentation of foreign peptides on the surface of an RNA-free spherical bacteriophage capsid J. Gen. Virol. 1993, 74, 541-548
9. ValegaÌŠrd, K.; Liljas, L.; Fridborg, K.; Unge, T. The three-dimensional structure of the bacterial virus MS2 Nature 1990, 345, 36-41
10. Caspar, D.; Klug, A. Physical principles in the construction of regular viruses Cold Spring Harbor Symp. Quant. Biol. 1962, 27, 1-24
11. Dykeman, E. C.; Twarock, R. All-atom normal-mode analysis reveals an RNA-induced allostery in a bacteriophage coat protein Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys. 2010, 81, 031908
12. Stockley, P. G. A simple, RNA-mediated allosteric switch controls the pathway to formation of a T=3 viral capsid J. Mol. Biol. 2007, 369, 541-552
13. Morton, V. L. The impact of viral RNA on assembly pathway selection J. Mol. Biol. 2010, 401, 298-308
14. Basnak, G. Viral genomic single-stranded RNA directs the pathway toward a T=3 capsid J. Mol. Biol. 2010, 395, 924-936
15. Borodavka, A.; Tuma, R.; Stockley, P. G. Evidence that viral RNAs have evolved for efficient, two-stage packaging Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 15769-15774
16. Sugiyama, T.; Nakada, D. Translational control of bacteriophage MS2 RNA cistrons by MS2 coat protein: affinity and specificity of the interaction of MS2 coat protein with MS2 RNA J. Mol. Biol. 1970, 48, 349-355
17. Wu, M.; Sherwin, T.; Brown, W. Delivery of antisense oligonucleotides to leukemia cells by RNA bacteriophage capsids Nanotechnol., Biol. Med. 2005, 1, 67-76
18. Brown, W. L. RNA bacteriophage capsid-mediated drug delivery and epitope presentation Intervirology 2002, 45, 371-380
19. Tuthill, T. J.; Bubeck, D.; Rowlands, D. J.; Hogle, J. M. Characterization of early steps in the poliovirus infection process: Receptor-decorated liposomes induce conversion of the virus to membrane-anchored entry-intermediate particles J. Virol. 2006, 80, 172-180
20. Murray, J. B.; Collier, A. K.; Arnold, J. R. A general purification procedure for chemically synthesized oligoribonucleotides Anal. Biochem. 1994, 218, 177-184
21. McNamara, J. O. Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras Nat. Biotechnol. 2006, 24, 1005-1015
22. Stockley, P. G.; Stonehouse, N. J.; Murry, J. B. Probing sequence-specific RNA recognition by the bacteriophage MS2 coat protien Nucleic Acids 1995, 23, 2512-2518
23. Kim, D. H. Synthetic dsRNA Dicer substrates enhance RNAi potency and efficacy Nat. Biotechnol. 2004, 23, 222-226
24. ValegaÌŠrd, K.; Murray, J. B.; Stockley, P. G.; Stonehouse, N. J.; Liljas, L. Crystal structure of an RNA bacteriophage coat protein-operator complex Nature 1994, 371, 623-626
25. Valegaîrd, K. The three-dimensional structures of two complexes between recombinant MS2 capsids and RNA operator fragments reveal sequence-specific protein-RNA interactions J. Mol. Biol. 1997, 270, 724-38
26. Brown, R. S.; Hingerty, B. E.; Dewan, J. C.; Klug, A. Pb(II)-catalysed cleavage of the sugar-phosphate backbone of yeast tRNAPhe-implications for lead toxicity and self-splicing RNA Nature 1983, 303, 543-546
27. Gell, C. Single-molecule fluorescence resonance energy transfer assays reveal heterogeneous folding ensembles in a simple RNA stem-loop J. Mol. Biol. 2008, 384, 264-278
28. Aleku, M. Intracellular localization of lipoplexed siRNA in vascular endothelial cells of different mouse tissues Microvasc. Res. 2008, 76, 31-41
29. Aleku, M. Atu027, a liposomal small interfering RNA formulation targeting protein kinase N3, inhibits cancer progression Cancer Res. 2008, 68, 9788-9798
30. Strumberg, D. Phase I clinical development of Atu027, a siRNA formulation targeting PKN3 in patients with advanced solid tumors Int. J. Clin. Pharmacol. Ther. 2011, 50, 76-78
31. Hirsch, M.; Strand, D.; Helm, M. Dye selection for live cell imaging of intact siRNA Biol. Chem. 2011, 393, 23-35
32. Leong, H. S. Intravital imaging of embryonic and tumor neovasculature using viral nanoparticles Nat. Protoc. 2010, 5, 1406-1417
33. Brunel, F. M. Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting Nano Lett. 2010, 10, 1093-1097
34. Koudelka, K. J. Endothelial Targeting of Cowpea Mosaic Virus (CPMV) via Surface Vimentin PLoS Pathogens 2009, 5, 10
35. Keefe, A. D.; Pai, S.; Ellington, A. Aptamers as therapeutics Nat. Rev. Drug Discovery 2010, 9, 537-550
36. Davis, M. E. The First Targeted Delivery of siRNA in Humans via a Nanoparticle: From Concept to Clinic Mol. Pharmaceutics 2009, 6, 659-668
37. Pang, L. Modifying the surface charge of pathogen-sized microspheres for studying pathogen transport in groundwater J. Environ. Qual. 2009, 38, 2210-2217
38. Tong, G. J.; Hsiao, S. C.; Carrico, Z. M.; Francis, M. B. Viral capsid DNA aptamer conjugates as multivalent cell-targeting vehicles J. Am. Chem. Soc. 2009, 131, 11174-11178
39. Stephanopoulos, N.; Tong, G. J.; Hsiao, S. C.; Francis, M. B. Dual-surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells ACS Nano 2010, 4, 6014-6020
40. Rhee, J.-K. Colorful Virus-like Particles: Fluorescent Protein Packaging by the Qβ Capsid Biomacromolecules 2011, 135, 1-8
41. Pokorski, J. K.; Hovlid, M. L.; Finn, M. G. Cell targeting with hybrid Qβ virus-like particles displaying epidermal growth factor ChemBioChem 2011, 92037, 2441-2447
42. Ashley, C. E. Cell-Specific Delivery of Diverse Cargos by Bacteriophage MS2 Virus-like Particles ACS Nano 2011, 5, 5729-5745
43. Stockley, P. G. Protein-based drug delivery system. (1992). US Patent No.
44. Pan, Y. Development of a microRNA delivery system based on bacteriophage MS2 virus-like particles FEBS J. 2012, 279, 1198-1208