Nanoparticle delivery of antisense oligonucleotides and their application in the exon skipping strategy for duchenne muscular dystrophy

Nucleic Acid Therapeutics

Volumn 24, Issue 1, 2014, Pages 87-100

  Falzarano, Maria Sofia ^a   Passarelli, Chiara ^a,b   Ferlini, Alessandra ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CELL PENETRATING PEPTIDE; CHITOSAN; COPOLYMER; DYSTROPHIN; LIPID; MACROGOL; METHACRYLIC ACID; MORPHOLINO OLIGONUCLEOTIDE; NANOPARTICLE; PEPTIDE NUCLEIC ACID; POLOXAMER; POLY(METHYL METHACRYLATE); POLYGLACTIN; SILICON DIOXIDE; SILVER NANOPARTICLE; SMALL INTERFERING RNA; SMALL NUCLEAR RNA;

ACTIVE TRANSPORT; ANTISENSE THERAPY; CHEMICAL MODIFICATION; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DUCHENNE MUSCULAR DYSTROPHY; ENDOCYTOSIS; EXON SKIPPING; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; REVIEW; SPONTANEOUS MUTATION;

ANIMALS; DOGS; DRUG DELIVERY SYSTEMS; DYSTROPHIN; EXONS; HUMANS; MALE; MICE; MICE, INBRED MDX; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; NANOMEDICINE; NANOPARTICLES; OLIGONUCLEOTIDES, ANTISENSE; TARGETED GENE REPAIR;

EID: 84893610019     PISSN: 21593337     EISSN: None     Source Type: Journal    
DOI: 10.1089/nat.2013.0450     Document Type: Review

References (95)

1. AARTSMA-RUS, A. (2012). Overview on AON design. Methods Mol. Biol. 867,117-129.
2. AARTSMA-RUS, A., and VAN OMMEN, G.J. (2007). Antisense-mediated exon skipping: a versatile tool with therapeutic and research applications. RNA 13, 1609-1624.
3. AKINC, A., THOMAS, M., KLIBANOV, A.M., LANGER, R. (2005). Exploring polyethyleniminemediated DNA transfection and the proton sponge hypothesis. J. Gene Med. 7, 657-663.
4. AMANTANA, A., and IVERSEN, P.L. (2005). Pharmacokinetics and biodistribution of phosphorodiamidate morpholino antisense oligomers. Curr. Opin. Pharmacol. 5, 550-555.
5. BASSI, E., FALZARANO, S., FABRIS, M., GUALANDI, F., MERLINI, L., VATTEMI, G., PERRONE, D., MARCHESI, E., SABATELLI, P., SPARNACCI, K., et al. (2012). Persistent dystrophin protein restoration 90 days after a course of intraperitoneally administered naked 2'OMePS AON and ZM2 NP-AON complexes in mdx mice. J. Biomed. Biotechnol. 2012, 897076.
6. BEDI, D., GILLESPIE, J.W., PETRENKO, V.A. Jr., EBNER, A., LEITNER, M., HINTERDORFER, P., PETRENKO, V.A. (2013). Targeted delivery of siRNA into breast cancer cells via phage fusion proteins. Mol. Pharm. 10, 551-559.
7. BENNETT, C.F., and SWAYZE, E.E. (2010). RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Annu. Rev. Pharmacol. Toxicol. 50, 259-293.
8. BETTS, C., SALEH, A.F., ARZUMANOV, A.A., HAMMOND, S.M., GODFREY, C., COURSINDEL, T., GAIT, M.J., WOOD, M.J. (2012). Pip6-PMO, a new generation of peptide-oligonucleotide conjugates with improved cardiac exon skipping activity for DMD treatment. Mol. Ther. Nucleic Acids. 1, e38.
9. BROWN, P.K., QURESHI, A.T., MOLL, A.N., HAYES, D.J., MONROE, W.T. (2013). Silver nanoscale antisense drug delivery system for photoactivated gene silencing. ACS Nano 7, 2948-2959.
10. BULFIELD, G., SILLER, W.G., WIGHT, P.A., MOORE, K.J. (1984). Xchromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. U. S. A. 81, 1189-1192.
11. BUVOLI, M., BUVOLI, A., LEINWAND, L.A. (2007). Interplay between exonic splicingenhancers, mRNA processing, and mRNA surveillance in the dystrophic Mdx mouse. PLoS One 2, e427.
12. CAPUTO, A., BROCCA-COFANO, E., CASTALDELLO, A., DE MICHELE, R., ALTAVILLA, G., MARCHISIO, M., GAVIOLI, R., ROLEN, U., CHIARANTINI, L., CERASI, A., et al. (2004). Novel biocompatible anionic polymeric microspheres for the delivery of the HIV-1 Tat protein for vaccine application. Vaccine 22, 2910-2924.
13. CASTANOTTO, D., and ROSSI, J.J. (2009). The promises and pitfalls of RNA-interference-based therapeutics. Nature 457, 426-433.
14. CHAMBERLAIN, J.S., METZGER, J., REYES, M., TOWNSEND, D., FAULKNER, J.A. (2007). Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J. 21, 2195-2204.
15. CHEN, Y., CHEN, H., SHI, J. (2013). In Vivo Bio-Safety Evaluations and Diagnostic/Therapeutic Applications of Chemically Designed Mesoporous Silica Nanoparticles. Adv. Mater. 25, 3144-3176.
16. CHERIF, M.S., SHUAIBU, M.N., KUROSAKI, T., HELEGBE, G.K., KIKUCHI, M., YANAGI, T., TSUBOI, T., SASAKI, H., HIRAYAMA, K. (2011). Immunogenicity of novel nanoparticle-coated MSP-1 C-terminus malaria DNA vaccine using different routes of administration. Vaccine 29, 9038-9050.
17. CHIN, J.Y., and GLAZER, P.M. (2009). Repair of DNA lesions associated with triplex-forming oligonucleotides. Mol. Carcinog. 48, 389-399.
18. CIRAK, S., ARECHAVALA-GOMEZA, V., GUGLIERI, M., FENG, L., TORELLI, S., ANTHONY, K., ABBS, S., GARRALDA, M.E., BOURKE, J., WELLS, D.J., et al. (2011). Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study. Lancet 378, 595-605.
19. DANHIER, F., ANSORENA, E., SILVA, J.M., COCO, R., BRETON, A.L., PRÉ AT, V. (2012). PLGA-based nanoparticles: An overview of biomedical applications. J. Control. Release 161, 505-522.
20. DE DIESBACH, P., N'KULI, F., BERENS, C., SONVEAUX, E., MONSIGNY, M., ROCHE, A.C., COURTOY, P.J. (2002). Receptor-mediated endocytosis of phosphodiester oligonucleotides in the HepG2 cell line: evidence for nonconventional intracellular trafficking. Nucleic Acids Res. 30, 1512-1521.
21. DE MARTIMPREY, H., BERTRAND, J.R., MALVY, C., COUVREUR, P., VAUTHIER, C. (2010). New core-shell nanoparticules for the intravenous delivery of siRNA to experimental thyroid papillary carcinoma. Pharm. Res. 27, 498-509.
22. DELEAVEY, G.F., and DAMHA, M.J. (2012). Designing chemically modified oligonucleotides for targeted gene silencing. Chem. Biol. 19, 937-954.
23. DES RIEUX, A., FIEVEZ, V., GARINOT, M., SCHNEIDER, Y.J., PRÉAT, V. (2006). Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J. Control Release 116, 1-27.
24. DIAS, N., and STEIN, C.A. (2002). Antisense oligonucleotides: basic concepts and mechanisms.Mol. Cancer Ther. 1, 347-355.
25. DIEBOLD, Y., and CALONGE, M. (2010). Applications of nanoparticles in ophthalmology. Prog. Retin. Eye Res. 29, 596-609.
26. DOUGLAS, A.G., and WOOD, M.J. (2013). Splicing therapy for neuromuscular disease. Mol. Cell Neurosci. 56:169-185.
27. DUAN, D. (2011). Duchenne muscular dystrophy gene therapy: Lost in translation? Res. Rep. Biol. 2011, 31-42.
28. DUNCAN, R., and GASPAR, R. (2011). Nanomedicine(s) under the microscope. Mol. Pharm. 8, 2101-2141.
29. DUNN, S.S., TIAN, S., BLAKE, S., WANG, J., GALLOWAY, A.L., MURPHY, A., POHLHAUS, P.D., ROLLAND, J.P., NAPIER, M.E., DESIMONE, J.M. (2012). Reductively responsive siRNA-conjugated hydrogel nanoparticles for gene silencing. J. Am. Chem. Soc. 134, 7423-7430.
30. DUPONT, E., PROCHIANTZ, A., JOLIOT, A. (2011). Penetratin story: an overview. Methods Mol. Biol. 683, 21-29.
31. DURBEEJ, M., and CAMPBELL, K.P. (2002). Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr. Opin. Genet. Dev. 12, 349-361.
32. EMERY, A.E.H. (2002). The muscular dystrophies. Lancet 359, 687-695.
33. EZZAT, K., ZAGHLOUL, E.M., EL ANDALOUSSI, S., LEHTO, T., EL-SAYED, R., MAGDY, T., SMITH, C.I., LANGEL, U. (2012). Solid formulation of cell-penetrating peptide nanocomplexes with siRNA and their stability in simulated gastric conditions. J. Control. Release 162, 1-8.
34. FERLINI, A., SABATELLI, .P, FABRIS, M., BASSI, E., FALZARANO, S., VATTEMI, G., PERRONE, D., GUALANDI, F., MARALDI, N.M., MERLINI, L., et al. (2010). Dystrophin restoration in skeletal, heart and skin arrector pili smooth muscle of mdx mice by ZM2 NP-AON complexes. Gene Ther. 17, 432-438.
35. GEARY, R.S., HENRY, S.P., GRILLONE, L.R. (2002). Fomivirsen: clinical pharmacology and potential drug interactions. Clin. Pharmacokinet. 41, 255-260.
36. GEARY, R.S., WATANABE, T.A., TRUONG, L., FREIER, S., LESNIK, E.A., SIOUFI, N.B., SASMOR, H., MANOHARAN, M., LEVIN, A.A. (2001). Pharmacokinetic properties of 29-O-(2-methoxyethyl)-modified oligonucleotide analogs in rats. J. Pharmacol. Exp. Ther. 296, 890-897.
37. GEBSKI, B.L., MANN, C.J., FLETCHER, S., WILTON, S.D. (2003). Morpholino antisense oligonucleotide induced dystrophin exon 23 skipping in mdx mouse muscle. Hum. Mol. Genet. 12, 1801-1811.
38. GOYENVALLE, A., BABBS, A., POWELL, D., KOLE, R., FLETCHER, S., WILTON, S.D., DAVIES, K.E. (2010). Prevention of dystrophic pathology in severely affected dystrophin/utrophin-defcient mice by morpholino-oligomermediated exon-skipping. Mol. Ther. 18, 198-205.
39. GOYENVALLE, A., VULIN, A., FOUGEROUSSE, F., LETURCQ, F., KAPLAN, J.C., GARCIA, L., DANOS, O. (2004). Rescue of dystrophic muscle through U7 snRNAmediated exon skipping. Science 306, 1796-1799.
40. HENRY, S.P., JOHNSON, M., ZANARDI, T.A., FEY, R., AUYEUNG, D., LAPPIN, P.B., LEVIN, A.A. (2012). Renal uptake and tolerability of a 2'-O-methoxyethyl modified antisense oligonucleotide (ISIS 113715) in monkey. Toxicology 301, 13-20.
41. HOFFMAN, E.P., MORGAN, J.E., WATKINS, S.C., PARTRIDGE, T.A. (1990). Somatic reversion/suppression of the mouse mdx phenotype in vivo. J. Neurol. Sci. 99, 9-25.
42. HOU, S., MA, H., JI, Y., HOU, W., JIA, N. (2013). A calcium phosphate nanoparticle-based biocarrier for efficient cellular delivery of antisense oligodeoxynucleotides. ACS Appl. Mater. Interfaces 5, 1131-1136.
43. JÄ RVER, P., COURSINDEL, T., ANDALOUSSI, S.E., GODFREY, C., WOOD, M.J., GAIT, M.J. (2012). Peptidemediated Cell and In Vivo Delivery of Antisense Oligonucleotides and siRNA. Mol. Ther. Nucleic Acids 1, e27.
44. JÄ RVER, P., O'DONOVAN, L., GAIT, M.J. (2013). A Chemical View of Oligonucleotides for Exon Skipping and Related Drug Applications. Nucleic Acid Ther. Oct 30. [Epub ahead of print]
45. JAYARAMAN, M., ANSELL, S.M., MUI, B.L., TAM, Y.K., CHEN, J., DU, X., BUTLER, D., ELTEPU, L., MATSUDA, S., NARAYANANNAIR, J.K., et al. (2012). Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo. Angew Chem. Int. Ed. Engl. 51(34), 8529-8533.
46. JULIANO, R.L., MING, X., NAKAGAWA, O. (2012). Cellular uptake and intracellular trafficking of antisense and siRNA oligonucleotides. Bioconjug. Chem. 23, 147-157.
47. KERSEY, F.R., MERKEL, T.J., PERRY, J.L., NAPIER, M.E., DESIMONE, J.M. (2012). Effect of aspect ratio and deformability on nanoparticle extravasation through nanopores. Langmuir. 28, 8773-8781.
48. KIM, Y., TEWARI, M., PAJEROWSKI, J.D., CAI, S., SEN, S., WILLIAMS, J.H., SIRSI, S.R., LUTZ, G.J., DISCHER, D.E. (2009). Polymersome delivery of siRNA and antisense oligonucleotides. J. Control. Release 134, 132-140.
49. KINGSTON, H.M., HARPER, P.S., PEARSON, P.L., DAVIES, K.E., WILLIAMSON, R., PAGE, D. (1983). Localisation of gene for Becker muscular dystrophy. Lancet 322, 1200.
50. KORNEGAY, J.N., BOGAN, J.R., BOGAN, D.J., CHILDERS, M.K., LI, J., NGHIEM, P., DETWILER, D.A., LARSEN, C.A., GRANGE, R.W., BHAVARAJU-SANKA, R.K., et al. (2012). Canine models of Duchenne muscular dystrophy and their use in therapeutic strategies. Mamm. Genome 23, 85-108.
51. KRUTZFELDT, J., RAJEWSKY, N., BRAICH, R., RAJEEV, K.G., TUSCHL, T., MANOHARAN, M., STOFFEL, M. (2005). Silencing of microRNAs in vivo with 'antagomirs.' Nature 438, 85-89.
52. LAMPRECHT, A., YAMAMOTO, H., TAKEUCHI, H., KAWASHIMA, Y. (2005). Nanoparticles enhance therapeutic efficiency by selectively increased local drug dose in experimental colitis in rats. J. Pharmacol. Exp. Ther. 315, 196-202.
53. LI, J., WANG, Y., ZHU, Y., OUPICKÝ , D. (2013). Recent advances in delivery of drug-nucleic acid combinations for cancer treatment. J. Control. Release 172:589-600.
54. LIANG, Y., LIU, Z., SHUAI, X., WANG, W., LIU, J., BI, W., WANG, C., JING, X., LIU, Y., TAO, E. (2012). Delivery of cationic polymer-siRNA nanoparticles for gene therapies in neural regeneration. Biochem. Biophys. Res. Commun. 421, 690-695.
55. LU, Q.L., MANN, C.J., LOU, F., BOU-GHARIOS, G., MORRIS, G.E., XUE, S.A., FLETCHER, S., PARTRIDGE, T.A., WILTON, S.D. (2003). Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse. Na.t Med. 9, 1009-1014.
56. LU, Q.L., YOKOTA, T., TAKEDA, S., GARCIA, L., MUNTONI, F., PARTRIDGE, T. (2011). The status of exon skipping as a therapeutic approach to duchenne muscular dystrophy. Mol Ther. 19, 9-15.
57. MENDELL, J.R., RODINO-KLAPAC, L., SAHENK, Z., MALIK, V., KASPAR, B.K., WALKER, C.M., CLARK, K.R. (2012). Gene therapy for muscular dystrophy: lessons learned and path forward. Neurosci. Lett. 527, 90-99.
58. MONACO, A.P., BERTELSON, C.J., LIECHTI-GALLATI, S., MOSR, H., KUNKEL, L.M. (1988). An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics 2, 90-95.
59. NA, H.K., KIM, M.H., PARK, K., RYOO, S.R., LEE, K.E., JEON, H., RYOO, R., HYEON, C., MIN, D.H. (2012). Efficient functional delivery of siRNA using mesoporous silica nanoparticles with ultralarge pores. Small. 8, 1752-1761.
60. NAKAGAKI, W.R., and CAMILLI, J.A. (2012). Bone tissue and muscle dystrophin deficiency in mdx mice. Joint Bone Spine 79, 129-133.
61. NEU, M., GERMERSHAUS, O., BEHE, M., KISSEL, T. (2007). Bioreversibly crosslinked polyplexes of PEI and high molecular weight PEG show extended circulation times in vivo. J. Control. Release 124, 69-80.
62. NGUYEN, D.N., MAHON, K.P., CHIKH, G., KIM, P., CHUNG, H., VICARI, A.P., LOVE, K.T., GOLDBERG, M., CHEN, S., KRIEG, A.M., et al. (2012). Lipid-derived nanoparticles for immunostimulatory RNA adjuvant delivery. Proc. Natl. Acad. Sci. U. S. A. 109, E797-803.
63. NIELSEN, P.E. (2010). Peptide nucleic acids (PNA) in chemical biology and drug discovery. Chem. Biodivers. 7, 786-804.
64. NIMESH, S., GUPTA, N., CHANDRA, R. (2011). Cationic polymer based nanocarriers for delivery of therapeutic nucleic acids. J. Biomed. Nanotechnol. 7, 504-520.
65. PAN, W.H. and CLAWSON, G.A. (2006). Antisense applications for biological control. J. Cell Biochem. 98, 14-35.
66. PATIL, Y., PANYAM, J. (2009). Polymeric Nanoparticles for siRNA Delivery and Gene Silencing. Int. J. Pharm. 367, 195-203.
67. PATIL, Y.B., SWAMINATHAN, S.K., SADHUKHA, T., MA, L., PANYAM, J. (2010). The use of nanoparticle-mediated targeted gene silencing and drug delivery to overcome tumor drug resistance. Biomaterials. 31, 358-365.
68. RAEMDONCK, K., MARTENS, T.F., BRAECKMANS, K., DEMEESTER, J., DE SMEDT, S.C. (2013). Polysaccharidebased nucleic acid nanoformulations. Adv. Drug. Deliv. Rev. 65:1123-1147.
69. RAGHUWANSHI, D., MISHRA, V., DAS, D., KAUR, K., SURESH, M.R. (2012). Dendritic cell targeted chitosan nanoparticles for nasal DNA immunization against SARS CoV nucleocapsid protein. Mol. Pharm. 9, 946-956.
70. RIMESSI, P., SABATELLI, P., FABRIS, M., BRAGHETTA, P., BASSI, E., SPITALI, P., VATTEMI, G., TOMELLERI, G., MARI, L., PERRONE, D., et al. (2009). Cationic PMMA nanoparticles bind and deliver antisense oligoribonucleotides allowing restoration of dystrophin expression in the mdx mouse. Mol. Ther. 17, 820-827.
71. SAH, H., THOMA, L.A., DESU, H.R., SAH, E., WOOD, G.C. (2013). Concepts and practices used to develop functional PLGA-based nanoparticulate systems. Int. J. Nanomedicine. 8, 747-765.
72. SAZANI, P., KOLE, R. (2003). Therapeutic potential of antisense oligonucleotides as modulators of alternative splicing. J. Clin. Invest. 112, 481-486.
73. SCHAIRER, D., MARTINEZ, L.R., BLECHER, K., CHOUAKE, J., NACHARAJU, P., GIALANELLA, P., FRIEDMAN, J.M., NOSANCHUK, J.D., FRIEDMAN, A. (2012). Nitric oxide nanoparticles: pre-clinical utility as a therapeutic for intramuscular abscesses. Virulence 3, 62-67.
74. SHENG, Y., YUAN, Y., LIU, C., TAO, X., SHAN, X., XU, F (2009). In vitro macrophage uptake and in vivo biodistribution of PLA-PEG naoparticles loaded with hemoglobin as blood substitutes: effect of PEG content. J. Mater. Sci. Mater. Med. 20, 1881-1891.
75. SICINSKI, P., GENG, Y., RYDER-COOK, A.S., BARNARD, E.A., DARLISON, M.G., BARNARD, P.J. (1989). The molecular basis of muscular dystrophy in the mdx mouse. A point mutation. Science 244, 1578-1580.
76. SIRSI, S.R., SCHRAY, R.C., GUAN, X., LYKENS, N.M., WILLIAMS, J.H., ERNEY, M.L., LUTZ, G.J. (2008). Functionalized PEG-PEI copolymers complexed to exonskipping oligonucleotides improve dystrophin expression in mdx mice. Hum. Gene Ther. 19, 795-806.
77. SMITH, B.F., KORNEGAY, J.N., DUAN, D. (2007). Independent canine models of Duchenne muscular dystrophy due to intronic insertions of repetitive DNA. Presented at 10th Annual Meeting of the American Society of Gene Therapy, Seattle, WA, May 30-Jun 3, 2007.;
78. SOLDATI, C., BITHELL, A., CONFORTI, P., CATTANEO, E., BUCKLEY, N.J. (2011). Rescue of gene expression by modified REST decoy oligonucleotides in a cellular model of Huntington's disease. J. Neurochem. 116, 415-425.
79. TAO, W., DAVIDE, J.P., CAI, M., ZHANG, G.J., SOUTH, V.J., MATTER, A., NG, B., ZHANG, Y., SEPP-LORENZINO, L. (2010). Noninvasive imaging of lipid nanoparticle-mediated systemic delivery of small-interfering RNA to the liver. Mol. Ther. 18, 1657-1666.
80. VAINZOF, M., AYUB-GUERRIERI, D., ONOFRE, P.C., MARTINS, P.C., LOPES, V.F., ZILBERZTAJN, D., MAIA, L.S., SELL, K., YAMAMOTO, L.U. (2008). Animal models for genetic neuromuscular diseases. J. Mol. Neurosci. 34, 241-248.
81. VAN DEUTEKOM, J.C., JANSON, A.A., GINJAAR, I.B., FRANKHUIZEN, W.S., AARTSMA-RUS, A., BREMMERBOUT, M., DEN DUNNEN, J.T., KOOP, K., VAN DER KOOI, A.J., GOEMANS, N.M., et al. (2007). Local dystrophin restoration with antisense oligonucleotide PRO051. N. Engl. J. Med. 357, 2677-2686.
82. VAN OMMEN, G.J., VAN DEUTEKOM, J., AARTSMARUS, A. (2008). The therapeutic potential of antisensemediated exon skipping. Curr. Opin. Mol. Ther. 10, 140-149.
83. VAN ROON-MOM, W.M. and AARTSMA-RUS, A. (2012). Overview on applications of antisense-mediated exon skipping. Methods Mol. Biol. 867, 79-96.
84. VOLLMER, J., KRIEG, A.M. (2009). Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists. Adv. Drug Deliv. Rev. 61, 195-204.
85. WANAKULE, P., LIU, G.W., FLEURY, A.T., ROY, K. (2012). Nano-inside-Micro: Disease-responsive Microgels with Encapsulated Nanoparticles for Intracellular Drug Delivery to the Deep Lung. J. Control. Release. 162, 429-437.
86. WANG, Y.J., WU, Y.T., LIN, J.Y., CHU, C.H., HUANG, H.Y., WANG, Y.C,. CHEN, J.K., YANG, C.S. (2012). Rapid quantitative analysis of clarithromycin in rat plasma by UPLCMS/MS after intravenous injection of the clarithromycinloaded ultrafine PLGA nanoparticles. J.Chromatogr. B Analyt. Technol. Biomed. Life Sci. 895-896, 178-181.
87. WILLIAMS, J.H., SCHRAY, R.C., SIRSI, S.R., LUTZ, G.J. (2008). Nanopolymers improve delivery of exon skipping oligonucleotides and concomitant dystrophin expression in skeletal muscle of mdx mice. BMC Biotechnol. 2, 8-35.
88. WILTON, S.D., FLETCHER, S. (2008). Exon skipping and Duchenne muscular dystrophy: hope, hype and how feasible? Neurol. India. 56, 254-262.
89. WOODROW, K.A., CU, Y., BOOTH, C.J., SAUCIER-SAWYER, J.K., WOOD, M.J., SALTZMAN, W.M. (2009). Intravaginal gene silencing using biodegradable polymer nanoparticles densely loaded with small-interfering RNA. Nat. Mater. 8, 526-533.
90. WU, B., LI, Y., MORCOS, P.A., DORAN, T.J., LU, P., LU, Q.L. (2009). Octa-guanidine morpholino restores dystrophin expression in cardiac and skeletal muscles and ameliorates pathology in dystrophic mdx mice. Mol. Ther. 17, 864-871.
91. YANG, L., NIU, H., GAO, X., WANG, Q., HAN, G., CAO, L., CAI, C., WEILER, J., YIN, H. (2013). Effective exon skipping and dystrophin restoration by 2'-o-methoxyethyl antisense oligonucleotide in dystrophin-deficient mice. PLoS One 8, e61584.
92. YANG, X.Z., DOU, S., SUN, T.M., MAO, C.Q., WANG, H.X., WANG, J. (2011). Systemic delivery of siRNA with cationic lipid assisted PEG-PLA nanoparticles for cancer therapy. J. Control. Release 156, 203-211.
93. YIN, H, SALEH, A.F., BETTS, C., CAMELLITI, P., SEOW, Y., ASHRAF, S., ARZUMANOV, A., HAMMOND, S., MERRITT, T., GAIT, M.J., WOOD, M.J. (2011). Pip5 transduction peptides direct high efficiency oligonucleotidemediated dystrophin exon skipping in heart and phenotypic correction in mdx mice. Mol. Ther. 19, 1295-1303.
94. ZANDANEL, C., VAUTHIER, C. (2012). Characterization of fluorescent poly(isobutylcyanoacrylate) nanoparticles obtained by copolymerization of a fluorescent probe during Redox Radical Emulsion Polymerization (RREP). Eur. J. Pharm. Biopharm. 82, 66-75.
95. ZHAO, J., CASTRANOVA, V. (2011). Toxicology of nanomaterials used in nanomedicine. J. Toxicol. Environ. Health B Crit. Rev. 14, 593-632.