Dual-ligand modification of PEGylated liposomes shows better cell selectivity and efficient gene delivery

Journal of Controlled Release

Volumn 153, Issue 2, 2011, Pages 141-148

  Kibria, Golam ^a   Hatakeyama, Hiroto ^a   Ohga, Noritaka ^a   Hida, Kyoko ^a   Harashima, Hideyoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Cell penetrating peptide; Dual ligand; Gene expression; PEGylated liposome; RGD motif; Targeted delivery

Indexed keywords

CELL-PENETRATING PEPTIDE; DUAL-LIGAND; PEGYLATED LIPOSOMES; RGD MOTIF; TARGETED DELIVERY;

CELLS; DRUG DELIVERY; GENE THERAPY; GENE TRANSFER; GLYCOLS; LIGANDS; LIPOSOMES; MOLECULAR BIOLOGY; PEPTIDES; PHOSPHOLIPIDS; POLYETHYLENE GLYCOLS;

GENE EXPRESSION;

ARGININE DERIVATIVE; ARGINYLGLYCYLASPARTIC ACID; CELL PENETRATING PEPTIDE; CLATHRIN; DISTEAROYLPHOSPHOETHANOLAMINE; LIPOSOME; MACROGOL 2000; PHOSPHOETHANOLAMINE; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ANIMAL CELL; ARTICLE; CAVEOLA; CONTROLLED STUDY; ENDOCYTOSIS; FEMALE; GENE DELIVERY SYSTEM; GENE EXPRESSION; HUMAN; HUMAN CELL; INTERNALIZATION; LIPID MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL LINE; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; DNA; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION; HUMANS; INTEGRIN ALPHAVBETA3; LIGANDS; LIPOSOMES; MICE; OLIGOPEPTIDES; PHOSPHATIDYLETHANOLAMINES; POLYETHYLENE GLYCOLS; TRANSFECTION;

EID: 79960100272     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2011.03.012     Document Type: Article

References (44)

1. L. Zhang, F.X. Gu, J.M. Chan, A.Z. Wang, R.S. Langer, and O.C. Farokhzad Nanoparticles in medicine: therapeutic applications and developments Clin. Pharmacol. Ther. 83 5 2008 761 769 (Pubitemid 351556021)
2. E.A. Forssen, D.M. Coulter, and R.T. Proffitt Selective in vivo localization of daunorubicin small unilamellar vesicles in solid tumors Cancer Res. 52 1992 3255 3261
3. H. Hatakeyama, H. Akita, K. Kogure, M. Oishi, Y. Nagasaki, Y. Kihira, M. Ueno, H. Kobayashi, H. Kikuchi, and H. Harashima Development of a novel systemic gene delivery system for cancer therapy with a tumor-specific cleavable PEG-lipid Gene Ther. 14 1 2007 68 77 (Pubitemid 44942867)
4. H. Hatakeyama, H. Akita, and H. Harashima A multifunctional envelope type nano device (MEND) for gene delivery to tumours based on the EPR effect: a strategy for overcoming the PEG dilemma Adv. Drug. Deliv. Rev. 63 3 2011 152 160
5. R. Suzuki, T. Takizawa, Y. Kuwata, M. Mutoh, N. Ishiguro, N. Utoguchi, A. Shinohara, M. Eriguchi, H. Yanagie, and K. Maruyama Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome Int. J. Pharm. 346 1-2 2008 143 150 (Pubitemid 350101994)
6. A. Yamada, Y. Taniguchi, K. Kawano, T. Honda, Y. Hattori, and Y. Maitani Design of folate-linked liposomal doxorubicin to its antitumor effect in mice Clin. Cancer Res. 14 24 2008 8161 8168
7. Y. Chen, J.J. Wu, and L. Huang Nanoparticles targeted with NGR motif deliver c-myc siRNA and doxorubicin for anticancer therapy Mol. Ther. 18 4 2010 828 834
8. M. Oba, S. Fukushima, N. Kanayama, K. Aoyagi, N. Nishiyama, H. Koyama, and K. Kataoka Cyclic RGD peptide-conjugated polyplex micelles as a targetable gene delivery system directed to cells possessing alphavbeta3 and alphavbeta5 integrins Bioconjug. Chem. 18 5 2007 1415 1423 (Pubitemid 47464048)
9. H. Hatakeyama, H. Akita, E. Ishida, K. Hashimoto, H. Kobayashi, T. Aoki, J. Yasuda, K. Obata, H. Kikuchi, T. Ishida, H. Kiwada, and H. Harashima Tumor targeting of doxorubicin by anti-MT1-MMP antibody-modified PEG liposomes Int. J. Pharm. 342 1-2 2007 194 200 (Pubitemid 47259319)
10. J.W. Park, D.B. Kirpotin, K. Hong, R. Shalaby, Y. Shao, U.B. Nielsen, J.D. Marks, D. Papahadjopoulos, and C.C. Benz Tumor targeting using anti-her2 immunoliposomes J. Control. Release 74 1-3 2001 95 113 (Pubitemid 32727613)
11. S.M. Stephenson, P.S. Low, and R.J. Lee Folate receptor-mediated targeting of liposomal drugs to cancer cells Methods Enzymol. 387 2004 33 50
12. I.A. Khalil, K. Kogure, H. Akita, and H. Harashima Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery Pharmacol. Rev. 58 1 2006 32 45
13. A. El-Sayed, S. Futaki, and H. Harashima Delivery of macromolecules using arginine-rich cell-penetrating peptides: ways to overcome endosomal entrapment AAPS J. 11 1 2009 13 22
14. K. Kogure, R. Moriguchi, K. Sasaki, M. Ueno, S. Futaki, and H. Harashima Development of a non-viral multifunctional envelope-type nano device by a novel lipid film hydration method J. Control. Release 98 2 2004 317 323 (Pubitemid 38950740)
15. Y. Nakamura, K. Kogure, S. Futaki, and H. Harashima Octaarginine-modified multifunctional envelope-type nano device for siRNA J. Control. Release 119 3 2007 360 367 (Pubitemid 46770881)
16. R. Suzuki, Y. Yamada, and H. Harashima Efficient cytoplasmic protein delivery by means of a multifunctional envelope-type nano device Biol. Pharm. Bull. 30 4 2007 758 762 (Pubitemid 46571006)
17. M.D. Pierschbacher, and E. Ruoslahti Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule Nature 309 1984 30 33 (Pubitemid 14134132)
18. M.D. Pierschbacher, and E. Ruoslahti Variants of the cell recognition site of fibronectin that retain attachment-promoting activity Proc. Natl. Acad. Sci. U. S. A. 81 1984 5985 5988 (Pubitemid 15219582)
19. C.L. Gladson, and D.A. Cheresh Glioblastoma expression of vitronectin and the alpha v beta 3 integrin. Adhesion mechanism for transformed glial cells J. Clin. Invest. 88 1991 1924 1932
20. S.M. Albelda, S.A. Mette, D.E. Elder, R. Stewart, L. Damjanovich, M. Herlyn, and C.A. Buck Integrin distribution in malignant melanoma: association of the beta 3 subunit with tumor progression Cancer Res. 50 1990 6757 6764 (Pubitemid 20348810)
21. H. Liapis, L.M. Adler, M.R. Wick, and J.S. Rader Expression of alpha(v)beta3 integrin is less frequent in ovarian epithelial tumors of low malignant potential in contrast to ovarian carcinomas Hum. Pathol. 28 1997 443 449 (Pubitemid 27175085)
22. P.C. Brooks, R.A.F. Clark, and D.A. Cheresh Requirement of vascular integrin avB3 for angiogenesis Science 264 1994 569 571 (Pubitemid 24185862)
23. T.J. Hieken, M. Farolan, S.G. Ronan, A. Shilkaitis, L. Wild, and T.K. Das Gupta Beta3 integrin expression in melanoma predicts subsequent metastasis J. Surg. Res. 63 1996 169 173 (Pubitemid 26197726)
24. J.M. Albert, C. Cao, L. Geng, L. Leavitt, D.E. Hallahan, and B. Lu Integrin alpha v beta 3 antagonist Cilengitide enhances efficacy of radiotherapy in endothelial cell and non-small-cell lung cancer models Int. J. Radiat. Oncol. Biol. Phys. 65 2006 1536 1543 (Pubitemid 44425239)
25. 3 integrin antagonists J. Med. Chem. 42 1999 3033 3040 (Pubitemid 29384038)
26. L.B. Jeffs, L.R. Palmer, E.G. Ambegia, C. Giesbrecht, S. Ewanick, and I. MacLachlan A scalable, extrusion-free method for efficient liposomal encapsulation of plasmid DNA Pharm. Res. 22 3 2005 362 372 (Pubitemid 40558494)
27. K. Hida, Y. Hida, D.N. Amin, A.F. Flint, D. Panigrahy, C.C. Morton, and M. Klagsbrun Tumor-associated endothelial cells with cytogenetic abnormalities Cancer Res. 64 2004 8249 8255 (Pubitemid 39491762)
28. I.A. Khalil, S. Futaki, M. Niwa, Y. Baba, N. Kaji, H. Kamiya, and H. Harashima Mechanism of improved gene transfer by the N-terminal stearylation of octaarginine: enhanced cellular association by hydrophobic core formation Gene Ther. 11 7 2004 636 644 (Pubitemid 38455982)
29. D. Mudhakir, H. Akita, E. Tan, and H. Harashima A novel IRQ ligand-modified nano-carrier targeted to a unique pathway of caveolar endocytic pathway J. Control. Release 125 2 2008 164 173 (Pubitemid 350299613)
30. S.H. Hansen, K. Sandvig, and B. van Deurs Clathrin and HA2 adaptors: effects of potassium depletion, hypertonic medium, and cytosol acidification J. Cell Biol. 121 1 1993 61 72 (Pubitemid 23097362)
31. T.M. Allen, and P.R. Cullis Drug delivery systems: entering the mainstream Science 303 2004 1818 1822 (Pubitemid 38374867)
32. A.J. Schraa, R.J. Kok, A.D. Berendsen, H.E. Moorlag, E.J. Bos, D.K. Meijer, L.F. de Leij, and G. Molema Endothelial cells internalize and degrade RGD-modified proteins developed for tumor vasculature targeting J. Control. Release 83 2 2002 241 251 (Pubitemid 35279469)
33. J. Folkman Angiogenesis in cancer, vascular, rheumatoid and other disease Nat. Med. 1 1995 27 31
34. E.F. Plow, T.A. Haas, L. Zhang, J. Loftus, and J.W. Smith Ligands binding to integrins J. Biol. Chem. 275 2000 21785 21788
35. S. Cressman, I. Dobson, J.B. Lee, Y.Y. Tam, and P.R. Cullis Synthesis of a labeled RGD-lipid, its incorporation into liposomal nanoparticles, and their trafficking in cultured endothelial cells Bioconjug. Chem. 20 7 2009 1404 1411
36. M. Oba, K. Aoyagi, K. Miyata, Y. Matsumoto, K. Itaka, N. Nishiyama, Y. Yamasaki, H. Koyama, and K. Kataoka Polyplex micelles with cyclic RGD peptide ligands and disulfide cross-links directing to the enhanced transfection via controlled intracellular trafficking Mol. Pharm. 5 6 2008 1080 1092
37. 3-targeted radiotracers: maximizing binding affinity via bivalency Bioconjug. Chem. 20 12 2009 2199 2213
38. S.L. Du, H. Pan, W.Y. Lu, J. Wang, J. Wu, and J.Y. Wang Cyclic Arg-Gly-Asp peptide-labeled liposomes for targeting drug therapy of hepatic fibrosis in rats J. Pharmacol. Exp. Ther. 322 2 2007 560 568 (Pubitemid 47105790)
39. J.M. Saul, A.V. Annapragada, and R.V. Bellamkonda A dual-ligand approach for enhancing targeting selectivity of therapeutic nanocarriers J. Control. Release 114 3 2006 277 287 (Pubitemid 44310813)
40. Y. Murase, T. Asai, Y. Katanasaka, T. Sugiyama, K. Shimizu, N. Maeda, and N. Oku A novel DDS strategy, "dual-targeting", and its application for antineovascular therapy Cancer Lett. 287 2 2010 165 171
41. K. Takara, H. Hatakeyama, N. Ohga, K. Hida, and H. Harashima Design of a dual-ligand system using a specific ligand and cell penetrating peptide, resulting in a synergistic effect on selectivity and cellular uptake Int. J. Pharm. 396 1-2 2010 143 148
42. I.A. Khalil, K. Kogure, S. Futaki, and H. Harashima High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene expression J. Biol. Chem. 281 6 2006 3544 3551 (Pubitemid 43845971)
43. D. Mudhakir, H. Akita, and H. Harashima Topology of octaarginines (R8) or IRQ ligand on liposomes affects the contribution of macropinocytosis- and caveolae-mediated cellular uptake Reactive and Functional Polymers 71 2011 340 343
44. M.R. Alam, V. Dixit, H. Kang, Z.B. Li, X. Chen, J. Trejo, M. Fisher, and R.L. Juliano Intracellular delivery of an anionic antisense oligonucleotide via receptor-mediated endocytosis Nucleic Acids Res. 36 8 2008 2764 2776 (Pubitemid 351659588)