Efficient intracellular delivery of siRNA with a safe multitargeted lipid-based nanoplatform

Nanomedicine

Volumn 8, Issue 9, 2013, Pages 1397-1413

  Gomes Da Silva, Lígia C ^a,b   Fernández, Yolanda ^c   Abasolo, Ibane ^c   Schwartz, Simo ^c   Ramalho, José S ^d   Pedroso De Lima, Maria C ^a,e   Simões, Sérgio ^a,b   Moreira, João N ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^d UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

blood stability; cancer; dual targeted delivery; immunogenicity; intravenous administration; pH sensitive liposome; siRNA

Indexed keywords

LIPOSOME; SMALL INTERFERING RNA; GREEN FLUORESCENT PROTEIN; NANOPARTICLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DOWN REGULATION; EGFP GENE; FEMALE; FLOW CYTOMETRY; GENE; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOGENICITY; LIPOSOMAL GENE DELIVERY SYSTEM; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CHEMISTRY; ENDOTHELIUM CELL; GENE TRANSFER; GENETICS; METABOLISM; NEOPLASMS; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; ENDOTHELIAL CELLS; FLOW CYTOMETRY; GENE SILENCING; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; LIPOSOMES; MICE; NANOPARTICLES; NEOPLASMS; RNA, SMALL INTERFERING;

EID: 84893195240     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.12.174     Document Type: Article

References (60)

1. Elbashir SM, Lendeckel W, Tuschl T. RNA interference is mediated by 21-And 22-nucleotide RNAs. Genes Dev. 15(2), 188-200 (2001).
2. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411(6836), 494-498(2001).
3. Moreira JN, Santos A, Moura V, Pedroso DE Lima MC, Simoes S. Nonviral lipid-based nanoparticles for targeted cancer systemic gene silencing. J. Nanosci. Nanotechnol. 8(5), 2187-2204 (2008).
4. Whitehead KA, Langer R, Anderson DG. Knocking down barriers: Advances in siRNA delivery. Nat. Rev. Drug Discov. 8(2), 129-138 (2009).
5. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 144(5), 646-674 (2011).
6. Moura V, Lacerda M, Figueiredo P, et al.: Targeted and intracellular triggered delivery of therapeutics to cancer cells and the tumor microenvironment: Impact on the treatment of breast cancer. Breast Cancer Res. Treat. 133(1), 61-73 (2012).
7. Christian S, Pilch J, Akerman ME, Porkka K, Laakkonen P, Ruoslahti E. Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J. Cell. Biol. 163(4), 871-878 (2003).
8. Porkka K, Laakkonen P, Hoffman JA, Bernasconi M, Ruoslahti E. A fragment of the HMGN2 protein homes to the nuclei of tumor cells and tumor endothelial cells in vivo. Proc. Natl Acad. Sci. USA 99(11), 7444-7449 (2002).
9. Santos AO, Da Silva LC, Bimbo LM, De Lima MC, Simoes S, Moreira JN. Design of peptide-Targeted liposomes containing nucleic acids. Biochim. Biophys. Acta 1798(3), 433-441 (2010).
10. Mishra S, Webster P, Davis ME. PEGylation significantly affects cellular uptake and intracellular trafficking of nonviral gene delivery particles. Eur. J. Cell. Biol. 83(3), 97-111 (2004).
11. Song LY, Ahkong QF, Rong Q, et al.: Characterization of the inhibitory effect of PEG-lipid conjugates on the intracellular delivery of plasmid and antisense DNA mediated by cationic lipid liposomes. Biochim. Biophys. Acta 1558(1), 1-13 (2002).
12. Lai MZ, Duzgunes N, Szoka FC. Effects of replacement of the hydroxyl group of cholesterol and tocopherol on the thermotropic behavior of phospholipid membranes. Biochemistry 24(7), 1646-1653 (1985).
13. Hafez IM, Cullis PR. Cholesteryl hemisuccinate exhibits pH sensitive polymorphic phase behavior. Biochim. Biophys. Acta 1463(1), 107-114 (2000).
14. Li X, Schick M. Theory of tunable pH-sensitive vesicles of anionic and cationic lipids or anionic and neutral lipids. Biophys. J. 80(4), 1703-1711 (2001).
15. Simões S, Slepushkin V, Duzgunes N, Pedroso De Lima MC. On the mechanisms of internalization and intracellular delivery mediated by pH-sensitive liposomes. Biochim. Biophys. Acta 1515(1), 23-37 (2001).
16. Sledz CA, Holko M, De Veer MJ, Silverman RH, Williams BR. Activation of the interferon system by short-interfering RNAs. Nat. Cell Biol. 5(9), 834-839 (2003).
17. Hornung V, Guenthner-Biller M, Bourquin C, et al.: Sequence-specific potent induction of IFN-Alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat. Med. 11(3), 263-270 (2005).
18. Sioud M. Induction of inflammatory cytokines and interferon responses by double-stranded and single-stranded siRNAs is sequence-dependent and requires endosomal localization. J. Mol. Biol. 348(5), 1079-1090 (2005).
19. Judge AD, Sood V, Shaw JR, Fang D, Mcclintock K, Maclachlan I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 23(4), 457-462 (2005).
20. Judge A, Maclachlan I. Overcoming the innate immune response to small interfering RNA. Hum. Gene Ther. 19(2), 111-124 (2008).
21. Brignole C, Marimpietri D, Pagnan G, et al.: Neuroblastoma targeting by c-myb-selective antisense oligonucleotides entrapped in anti-GD2 immunoliposome: Immune cell-mediated anti-Tumor activities. Cancer Lett. 228(1-2), 181-186 (2005).
22. Tagami T, Nakamura K, Shimizu T, Yamazaki N, Ishida T, Kiwada H. CpG motifs in pDNA-sequences increase anti-PEG IgM production induced by PEG-coated pDNA-lipoplexes. J. Control. Release 142(2), 160-166 (2010).
23. Judge A, Mcclintock K, Phelps JR, Maclachlan I. Hypersensitivity and loss of disease site targeting caused by antibody responses to PEGylated liposomes. Mol. Ther. 13(2), 328-337 (2006).
24. Semple SC, Harasym TO, Clow KA, Ansell SM, Klimuk SK, Hope MJ. Immunogenicity and rapid blood clearance of liposomes containing polyethylene glycol-lipid conjugates and nucleic acid. J. Pharmacol. Exp. Ther. 312(3), 1020-1026 (2005).
25. Tagami T, Uehara Y, Moriyoshi N, Ishida T, Kiwada H. Anti-PEG IgM production by siRNA encapsulated in a PEGylated lipid nanocarrier is dependent on the sequence of the siRNA. J. Control. Release 151(2), 149-154 (2011).
26. Judge AD, Bola G, Lee AC, Maclachlan I. Design of noninflammatory synthetic siRNA mediating potent gene silencing in vivo. Mol. Ther. 13(3), 494-505 (2006).
27. Robbins M, Judge A, Liang L, Mcclintock K, Yaworski E, Maclachlan I. 2′-O-methyl-modified RNAs act as TLR7 antagonists. Mol. Ther. 15(9), 1663-1669 (2007).
28. Hamm S, Latz E, Hangel D, et al.: Alternating 2'-O-ribose methylation is a universal approach for generating nonstimulatory siRNA by acting as TLR7 antagonist. Immunobiology 215(7), 559-569 (2010).
29. Robbins M, Judge A, Ambegia E, et al.: Misinterpreting the therapeutic effects of small interfering RNA caused by immune stimulation. Hum. Gene Ther. 19(10), 991-999 (2008).
30. Semple SC, Klimuk SK, Harasym TO, et al.: Efficient encapsulation of antisense oligonucleotides in lipid vesicles using ionizable aminolipids: Formation of novel small multilamellar vesicle structures. Biochim. Biophys. Acta 1510(1-2), 152-166 (2001).
31. Maurer N, Wong KF, Stark H, et al.: Spontaneous entrapment of polynucleotides upon electrostatic interaction with ethanol-destabilized cationic liposomes. Biophys. J. 80(5), 2310-2326 (2001).
32. Moreira JN, Gaspar R, Allen TM. Targeting stealth liposomes in a murine model of human small cell lung cancer. Biochim. Biophys. Acta 1515(2), 167-176 (2001).
33. Moreira JN, Ishida T, Gaspar R, Allen TM. Use of the postinsertion technique to insert peptide ligands into preformed stealth liposomes with retention of binding activity and cytotoxicity. Pharm. Res. 19(3), 265-269 (2002).
34. Mendonca LS, Firmino F, Moreira JN, Pedroso De Lima MC, Simoes S. Transferrin receptor-Targeted liposomes encapsulating anti-BCR-ABL siRNA or as ODN for chronic myeloid leukemia treatment. Bioconjug. Chem. 21(1), 157-168 (2010).
35. Zhang YP, Sekirov L, Saravolac EG, et al.: Stabilized plasmid-lipid particles for regional gene therapy: Formulation and transfection properties. Gene Ther. 6(8), 1438-1447 (1999).
36. Marchio S, Lahdenranta J, Schlingemann RO, et al.: Aminopeptidase A is a functional target in angiogenic blood vessels. Cancer Cell 5(2), 151-162 (2004).
37. Jackson AL, Bartz SR, Schelter J, et al.: Expression profiling reveals off-Target gene regulation by RNAi. Nat. Biotechnol. 21(6), 635-637 (2003).
38. Tschuch C, Schulz A, Pscherer A, et al.: Off-Target effects of siRNA specific for GFP. BMC Mol. Biol. 9, 60 (2008).
39. Milla P, Dosio F, Cattel L. PEGylation of proteins and liposomes: A powerful and flexible strategy to improve the drug delivery. Curr. Drug Metab. 13(1), 105-119 (2011).
40. Zimmermann TS, Lee AC, Akinc A, et al.: RNAi-mediated gene silencing in nonhuman primates. Nature 441(7089), 111-114 (2006).
41. Judge AD, Robbins M, Tavakoli I, et al.: Confirming the RNAi-mediated mechanism of action of siRNA-based cancer therapeutics in mice. J. Clin. Invest. 119(3), 661-673 (2009).
42. Geisbert TW, Lee AC, Robbins M, et al.: Postexposure protection of nonhuman primates against a lethal Ebola virus challenge with RNA interference: A proof-of-concept study. Lancet 375(9729), 1896-1905 (2010).
43. Geisbert TW, Hensley LE, Kagan E, et al.: Postexposure protection of guinea pigs against a lethal ebola virus challenge is conferred by RNA interference. J. Infect. Dis. 193(12), 1650-1657 (2006).
44. Morrissey DV, Lockridge JA, Shaw L, et al.: Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs. Nat. Biotechnol. 23(8), 1002-1007 (2005).
45. Morrissey DV, Blanchard K, Shaw L, et al.: Activity of stabilized short interfering RNA in a mouse model of hepatitis B virus replication. Hepatology 41(6), 1349-1356 (2005).
46. Orringer DA, Koo YE, Chen T, et al.: In vitro characterization of a targeted, dye-loaded nanodevice for intraoperative tumor delineation. Neurosurgery 64(5), 965-971; discussion 971-972 (2009).
47. Reddy GR, Bhojani MS, Mcconville P, et al.: Vascular targeted nanoparticles for imaging and treatment of brain tumors. Clin. Cancer Res. 12(22), 6677-6686 (2006).
48. Winer I, Wang S, Lee YE, et al.: F3-Targeted cisplatin-hydrogel nanoparticles as an effective therapeutic that targets both murine and human ovarian tumor endothelial cells in vivo. Cancer Res. 70(21), 8674-8683 (2010).
49. Heyes J, Hall K, Tailor V, Lenz R, Maclachlan I. Synthesis and characterization of novel poly(ethylene glycol)-lipid conjugates suitable for use in drug delivery. J. Control. Release 112(2), 280-290 (2006).
50. Ishida T, Iden DL, Allen TM. A combinatorial approach to producing sterically stabilized (stealth) immunoliposomal drugs. FEBS Lett. 460(1), 129-133 (1999).
51. Uster PS, Allen TM, Daniel BE, Mendez CJ, Newman MS, Zhu GZ. Insertion of poly(ethylene glycol) derivatized phospholipid into preformed liposomes results in prolonged in vivo circulation time. FEBS Lett. 386(2-3), 243-246 (1996).
52. Cullis PR, De Kruijff B. The polymorphic phase behavior of phosphatidylethanolamines of natural and synthetic origin. A 31P NMR study. Biochim. Biophys. Acta 513(1), 31-42 (1978).
53. Slepushkin VA, Simoes S, Dazin P, et al.: Sterically stabilized pH-sensitive liposomes. Intracellular delivery of aqueous contents and prolonged circulation in vivo. J. Biol. Chem. 272(4), 2382-2388 (1997).
54. Mendonca LS, Moreira JN, De Lima MC, Simoes S. Coencapsulation of anti-BCR-ABL siRNA and imatinib mesylate in transferrin receptor-Targeted sterically stabilized liposomes for chronic myeloid leukemia treatment. Biotechnol. Bioeng. 107(5), 884-893 (2010).
55. Di Paolo D, Brignole C, Pastorino F, et al.: Neuroblastoma-Targeted nanoparticles entrapping siRNA specifically knockdown ALK. Mol. Ther. 19(6), 1131-1140 (2011).
56. Ambegia E, Ansell S, Cullis P, Heyes J, Palmer L, Maclachlan I. Stabilized plasmid-lipid particles containing PEG-diacylglycerols exhibit extended circulation lifetimes and tumor selective gene expression. Biochim. Biophys. Acta 1669(2), 155-163 (2005).
57. Sioud M. Deciphering the code of innate immunity recognition of siRNAs. Methods Mol. Biol. 487, 41-59 (2009).
58. Ge Q, Filip L, Bai A, Nguyen T, Eisen HN, Chen J. Inhibition of influenza virus production in virus-infected mice by RNA interference. Proc. Natl Acad. Sci. USA 101(23), 8676-8681 (2004).
59. Tompkins SM, Lo CY, Tumpey TM, Epstein SI. Protection against lethal influenza virus challenge by RNA interference in vivo. Proc. Natl Acad. Sci. USA 101(23), 8682-8686 (2004).
60. Webb MS, Saxon D, Wong FM, et al.: Comparison of different hydrophobic anchors conjugated to poly(ethylene glycol): Effects on the pharmacokinetics of liposomal vincristine. Biochim. Biophys. Acta 1372(2), 272-282 (1998).