Vectorization of morpholino oligomers by the (R-Ahx-R)4 peptide allows efficient splicing correction in the absence of endosomolytic agents

Journal of Controlled Release

Volumn 116, Issue 3, 2006, Pages 304-313

  Abes, Saïd ^a   Moulton, Hong M ^b   Clair, Philippe ^a   Prevot, Paul ^a   Youngblood, Derek S ^b   Wu, Rebecca P ^b   Iversen, Patrick L ^b   Lebleu, Bernard ^a  

^a UNIV MONTPELLIER   (France)

^b AVI BIOPHARMA INC   (United States)

Author keywords

(R Ahx R) 4; CPPs; Endosomolytic agents; PMO antisens; Splice correction

Indexed keywords

CONTROLLED DRUG DELIVERY; DEGRADATION; POLYPEPTIDES; POSITIVE IONS; VECTORS;

ENDOSOMOLYTIC AGENTS; PMO ANTIGENS; SPLICE CORRECTION;

OLIGOMERS;

6 AMINOHEXANOIC OLIGOARGININE PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER 705; ANTISENSE OLIGONUCLEOTIDE; BETA GLOBIN; CELL PENETRATING PEPTIDE; MESSENGER RNA PRECURSOR; OLIGOARGININE PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER 705; PEPTIDE; TAT 48-60 PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER 705;

ARTICLE; CELL NUCLEUS; CONJUGATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACTIVITY; DRUG CONJUGATION; DRUG METABOLISM; DRUG UPTAKE; ENDOCYTOSIS; ENDOSOME; FEMALE; GENE MUTATION; HELA CELL; HUMAN; HUMAN CELL; LYSOSOME; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; RNA SPLICING;

ANIMALS; CELL CULTURE TECHNIQUES; CELL NUCLEUS; CHO CELLS; CRICETINAE; CRICETULUS; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; ENDOSOMES; HELA CELLS; HUMANS; MORPHOLINES; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDE NUCLEIC ACIDS; PEPTIDES; RNA SPLICE SITES; RNA SPLICING;

EID: 33847036106     PISSN: 01683659     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jconrel.2006.09.011     Document Type: Article

References (35)

1. Thierry A.R., Vives E., Richard J.P., Prevot P., Martinand-Mari C., Robbins I., and Lebleu B. Cellular uptake and intracellular fate of antisense oligonucleotides. Curr. Opin. Mol. Ther. 5 2 (2003) 133-138
2. Zelphati O., Uyechi L.S., Barron L.G., and Szoka Jr. F.C. Effect of serum components on the physico-chemical properties of cationic lipid/oligonucleotide complexes and on their interactions with cells. Biochim. Biophys. Acta 1390 2 (1998) 119-133
3. Moghimi S.M., Symonds P., Murray J.C., Hunter A.C., Debska G., and Szewczyk A. A two-stage poly(ethylenimine)-mediated cytotoxicity: implications for gene transfer/therapy. Molec. Ther. 11 6 (2005) 990-995
4. Kaihatsu K., Huffman K.E., and Corey D.R. Intracellular uptake and inhibition of gene expression by PNAs and PNA-peptide conjugates. Biochemistry 43 45 (2004) 14340-14347
5. Gebski B.L., Mann C.J., Fletcher S., and Wilton S.D. Morpholino antisense oligonucleotide induced dystrophin exon 23 skipping in mdx mouse muscle. Hum. Mol. Genet. 12 15 (2003) 1801-1811
6. Pujals S., Fernandez-Carneado J., Lopez-Iglesias C., Kogan M.J., and Giralt E. Mechanistic aspects of CPP-mediated intracellular drug delivery: Relevance of CPP self-assembly. Biochim. Biophys. Acta. 1758 3 (2006) 264-279
7. Snyder E.L., and Dowdy S.F. Recent advances in the use of protein transduction domains for the delivery of peptides, proteins and nucleic acids in vivo. Expert Opin. Drug Deliv. 2 1 (2005) 43-51
8. Thierry A.R., Abes S., Resina S., Travo A., Richard J.P., Prevot P., and Lebleu B. Comparison of basic peptides-and lipid-based strategies for the delivery of splice correcting oligonucleotides. Biochim. Biophys. Acta 1758 3 (2006) 364-374
9. Abes S., Williams D., Prevot P., Thierry A.R., Gait M.J., and Lebleu B. Endosome trapping limits the efficiency of splicing correction by PNA-oligolysine conjugates. J. Control. Release 110 3 (2006) 595-604
10. Turner J.J., Ivanova G.D., Verbeure B., Williams D., Arzumanov A.A., Abes S., Lebleu B., and Gait M.J. Cell-penetrating peptide conjugates of peptide nucleic acids (PNA) as inhibitors of HIV-1 Tat-dependent trans-activation in cells. Nucleic Acids Res. 33 21 (2005) 6837-6849
11. Shiraishi T., Pankratova S., and Nielsen P.E. Calcium ions effectively enhance the effect of antisense peptide nucleic acids conjugated to cationic tat and oligoarginine peptides. Chem. Biol. 12 8 (2005) 923-929
12. Richard J.P., Melikov K., Vives E., Ramos C., Verbeure B., Gait M.J., Chernomordik L.V., and Lebleu B. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 278 1 (2003) 585-590
13. Kang S.H., Cho M.J., and Kole R. Up-regulation of luciferase gene expression with antisense oligonucleotides: implications and applications in functional assay development. Biochemistry 37 18 (1998) 6235-6239
14. Shiraishi T., and Nielsen P.E. Photochemically enhanced cellular delivery of cell penetrating peptide-PNA conjugates. FEBS Lett. 580 5 (2006) 1451-1456
15. Wadia J.S., Stan R.V., and Dowdy S.F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10 3 (2004) 310-315
16. Rothbard J.B., Kreider E., VanDeusen C.L., Wright L., Wylie B.L., and Wender P.A. Arginine-rich molecular transporters for drug delivery: role of backbone spacing in cellular uptake. J. Med. Chem. 45 17 (2002) 3612-3618
17. Draper B.W., Morcos P.A., and Kimmel C.B. Inhibition of zebrafish fgf8 pre-mRNA splicing with morpholino oligos: a quantifiable method for gene knockdo. Genesis 30 3 (2001) 154-156
18. Lacerra G., Sierakowska H., Carestia C., Fucharoen S., Summerton J., Weller D., and Kole R. Restoration of hemoglobin A synthesis in erythroid cells from peripheral blood of thalassemic patients. Proc. Natl. Acad. Sci. U. S. A. 97 17 (2000) 9591-9596
19. Alter J., Lou F., Rabinowitz A., Yin H., Rosenfeld J., Wilton S.D., Partridge T.A., and Lu Q. Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat. Med. 12 2 (2006) 175-177
20. Neuman B.W., Stein D.A., Kroeker A.D., Churchill M.J., Kim A.M., Kuhn P., Dawson P., Moulton H.M., Bestwick R.K., Iversen P.L., and Buchmeier M.J. Inhibition, escape, and attenuated growth of severe acute respiratory syndrome coronavirus treated with antisense morpholino oligomers. J. Virol. 79 15 (2005) 9665-9676
21. Neuman B.W., Stein D.A., Kroeker A.D., Paulino A.D., Moulton H.M., Iversen P.L., and Buchmeier M.J. Antisense morpholino-oligomers directed against the 5′ end of the genome inhibit coronavirus proliferation and growth. J. Virol. 78 11 (2004) 5891-5899
22. Deas T.S., Binduga-Gajewska I., Tilgner M., Ren P., Stein D.A., Moulton H.M., Iversen P.L., Kauffman E.B., Kramer L.D., and Shi P.Y. Inhibition of flavivirus infections by antisense oligomers specifically suppressing viral translation and RNA replication. J. Virol. 79 8 (2005) 4599-4609
23. Kinney R.M., Huang C.Y., Rose B.C., Kroeker A.D., Dreher T.W., Iversen P.L., and Stein D.A. Inhibition of dengue virus serotypes 1 to 4 in vero cell cultures with morpholino oligomers. J. Virol. 79 8 (2005) 5116-5128
24. J. Summerton, D. Weller, US Patent: (1993) 5185444.
25. Summerton J., and Weller D. Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 7 3 (1997) 187-195
26. Moulton H.M., Hase M.C., Smith K.M., and Iversen P.L. HIV Tat peptide enhances cellular delivery of antisense morpholino oligomers. Antisense Nucleic Acid Drug Dev. 13 1 (2003) 31-43
27. Moulton H.M., Nelson M.H., Hatlevig S.A., Reddy M.T., and Iversen P.L. Cellular uptake of antisense morpholino oligomers conjugated to arginine-rich peptides. Bioconjug. Chem. 15 2 (2004) 290-299
28. Sazani P., Kang S.H., Maier M.A., Wei C., Dillman J., Summerton J., Manoharan M., and Kole R. Nuclear antisense effects of neutral, anionic and cationic oligonucleotide analogs. Nucleic Acids Res. 29 19 (2001) 3965-3974
29. Richard J.P., Melikov K., Brooks H., Prevot P., Lebleu B., and Chernomordik L.V. Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J. Biol. Chem. 280 15 (2005) 15300-15306
30. Belting M. Heparan sulfate proteoglycan as a plasma membrane carrier. Trends Biochem. Sci. 28 3 (2003) 145-151
31. Enterlein S., Warfield K.L., Swenson D.L., Stein D.A., Smith J.L., Gamble C.S., Kroeker A.D., Iversen P.L., Bavari S., and Muhlberger E. VP35 knockdown inhibits Ebola virus amplification and protects against lethal infection in mice. Antimicrob. Agents Chemother. 50 3 (2006) 984-993
32. Holden K.L., Stein D.A., Pierson T.C., Ahmed A.A., Clyde K., Iversen P.L., and Harris E. Inhibition of dengue virus translation and RNA synthesis by a morpholino oligomer targeted to the top of the terminal 3′ stem-loop structure. Virology 344 2 (2006) 439-452
33. Joliot A., and Prochiantz A. Transduction peptides: from technology to physiology. Nat. Cell Biol. 6 (2004) 189-196
34. Nelson M.H., Stein D.A., Kroeker A.D., Hatlevig S.A., Iversen P.L., and Moulton H.M. Arginine-rich peptide conjugation to morpholino oligomers: effects on antisense activity and specificity. Bioconjug. Chem. 16 4 (2005) 959-966
35. McClorey G., Moulton H.M., Iversen P.L., Fletcher F., and Wilton S.D. Antisense oligonucleotide-induced exon skipping restores dystrophin ex- pression in vitro in a canine model of DMD. Gene Therapy. 13 19 (2006) 1373-1381