Delivery of macromolecules using arginine-rich cell-penetrating peptides: Ways to overcome endosomal entrapment

AAPS Journal

Volumn 11, Issue 1, 2009, Pages 13-22

  El Sayed, Ayman ^a,c   Futaki, Shiroh ^b   Harashima, Hideyoshi ^a,c  

^a HOKKAIDO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Arginine rich cell penetrating peptides; Endosomal escape; Membrane disruptive peptides; Oligoarginine; Protein transduction domains

Indexed keywords

ARGININE RICH CELL PENETRATING PEPTIDE; DRUG CARRIER; OLIGODEOXYNUCLEOTIDE; PENETRATIN; PLASMID DNA; POLYETHYLENEIMINE; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; VIRUS HEMAGGLUTININ;

BIOCOMPATIBILITY; BIODEGRADABILITY; CHEMICAL MODIFICATION; CYTOSOL; DRUG CYTOTOXICITY; ENDOCYTOSIS; ENDOSOME; INTERNALIZATION; LIPOSOMAL DELIVERY; MEMBRANE DAMAGE; NONVIRAL GENE DELIVERY SYSTEM; PHOTOCHEMICAL INTERNALIZATION; REVIEW;

ARGININE; CELL MEMBRANE; CYTOSOL; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; ENDOSOMES; HUMANS; INTRACELLULAR MEMBRANES; LIPOPEPTIDES; LIPOSOMES; LYSOSOMES; MACROMOLECULAR SUBSTANCES; MEMBRANE FUSION; PEPTIDES; PHOTOCHEMISTRY; PHOTOSENSITIZING AGENTS; POLYMERS;

EID: 65549133368     PISSN: 15507416     EISSN: None     Source Type: Journal    
DOI: 10.1208/s12248-008-9071-2     Document Type: Review

References (96)

1. M. Belting, S. Sandgren, and A. Wittrup. Nuclear delivery of macromolecules: Barriers and carriers. Adv. Drug Deliv. Rev. 57(4):505-527 (2005).
2. H. Kamiya, H. Akita, and H. Harashima. Pharmacokinetic and pharmacodynamic considerations in gene therapy. Drug Discov. Today. 8(21):990-996 (2003).
3. M. Mae, and U. Langel. Cell-penetrating peptides as vectors for peptide, protein and oligonucleotide delivery. Curr. Opin. Pharmacol. 6(5):509-514 (2006).
4. 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):3544-3551 (2006).
5. H. Brooks, B. Lebleu, and E. Vives. Tat peptide-mediated cellular delivery: Back to basics. Adv. Drug Deliv. Rev. 57(4):559-577 (2005).
6. S. Futaki. Membrane-permeable arginine-rich peptides and the translocation mechanisms. Adv. Drug Deliv. Rev. 57(4):547-558 (2005).
7. V. P. Torchilin. Tat peptide-mediated intracellular delivery of pharmaceutical nanocarriers. Adv. Drug Deliv. Rev. 60(4-5):548-558 (2008).
8. I. Nakase, T. Takeuchi, G. Tanaka, and S. Futaki. Methodological and cellular aspects that govern the internalization mechanisms of arginine-rich cell-penetrating peptides. Adv. Drug Deliv. Rev. 60(4-5):598-607 (2008).
9. A. D. Frankel, and C. O. Pabo. Cellular uptake of the tat protein from human immunodeficiency virus. Cell. 55(6):1189-1193 (1988).
10. D. Derossi, A. H. Joliot, G. Chassaing, and A. Prochiantz. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269(14):10444-10450 (1994).
11. S. Futaki, T. Suzuki, W. Ohashi, T. Yagami, S. Tanaka, K. Ueda, and Y. Sugiura. Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem. 276(8):5836-5840 (2001).
12. T. Suzuki, S. Futaki, M. Niwa, S. Tanaka, K. Ueda, and Y. Sugiura. Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem. 277(4):2437-2443 (2002).
13. J. P. Richard, K. Melikov, E. Vives, C. Ramos, B. Verbeure, M. J. Gait, L. V. Chernomordik, and B. Lebleu. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 278(1):585-590 (2003).
14. S. M. Fuchs, and R. T. Raines. Pathway for polyarginine entry into mammalian cells. Biochemistry. 43(9):2438-2444 (2004).
15. S. Futaki. Oligoarginine vectors for intracellular delivery: Design and cellular-uptake mechanisms. Biopolymers. 84(3):241-249 (2006).
16. F. Duchardt, M. Fotin-Mleczek, H. Schwarz, R. Fischer, and R. Brock. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic. 8(7):848-866 (2007).
17. I. Nakase, M. Niwa, T. Takeuchi, K. Sonomura, N. Kawabata, Y. Koike, M. Takehashi, S. Tanaka, K. Ueda, J. C. Simpson, A. T. Jones, Y. Sugiura, and S. Futaki. Cellular uptake of arginine-rich peptides: Roles for macropinocytosis and actin rearrangement. Mol. Ther. 10(6):1011-1022 (2004).
18. J. S. Wadia, R. V. Stan, and S. F. Dowdy. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10(3):310-315 (2004).
19. I. Nakase, A. Tadokoro, N. Kawabata, T. Takeuchi, H. Katoh, K. Hiramoto, M. Negishi, M. Nomizu, Y. Sugiura, and S. Futaki. Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis. Biochemistry. 46(2):492-501 (2007).
20. K. Melikov, and L. V. Chernomordik. Arginine-rich cell penetrating peptides: From endosomal uptake to nuclear delivery. Cell. Mol. Life Sci. 62(23):2739-2749 (2005).
21. P. A. Wender, W. C. Galliher, E. A. Goun, L. R. Jones, and T. H. Pillow. The design of guanidinium-rich transporters and their internalization mechanisms. Adv. Drug Deliv. Rev. 60(4-5):452-472 (2008).
22. S. Al-Taei, N. A. Penning, J. C. Simpson, S. Futaki, T. Takeuchi, I. Nakase, and A. T. Jones. Intracellular traffic and fate of protein transduction domains HIV-1 TAT peptide and octaarginine. Implications for their utilization as drug delivery vectors. Bioconjug. Chem. 17(1):90-100 (2006).
23. T. B. Potocky, A. K. Menon, and S. H. Gellman. Cytoplasmic and nuclear delivery of a TAT-derived peptide and a beta-peptide after endocytic uptake into HeLa cells. J. Biol. Chem. 278(50):50188-50194 (2003).
24. R. Fischer, K. Kohler, M. Fotin-Mleczek, and R. Brock. A stepwise dissection of the intracellular fate of cationic cell-penetrating peptides. J. Biol. Chem. 279(13):12625-12635 (2004).
25. J. B. Rothbard, T. C. Jessop, R. S. Lewis, B. A. Murray, and P. A. Wender. Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells. J. Am. Chem. Soc. 126(31):9506-9507 (2004).
26. J. B. Rothbard, T. C. Jessop, and P. A. Wender. Adaptive translocation: the role of hydrogen bonding and membrane potential in the uptake of guanidinium-rich transporters into cells. Adv. Drug Deliv. Rev. 57(4):495-504 (2005).
27. N. Sakai, T. Takeuchi, S. Futaki, and S. Matile. Direct observation of anion-mediated translocation of fluorescent oligoarginine carriers into and across bulk liquid and anionic bilayer membranes. Chembiochem. 6(1):114-122 (2005).
28. T. Hitz, R. Iten, J. Gardiner, K. Namoto, P. Walde, and D. Seebach. Interaction of alpha-and beta-oligoarginine-acids and amides with anionic lipid vesicles: A mechanistic and thermodynamic study. Biochemistry. 45(18):5817-5829 (2006).
29. J. Bjorklund, H. Biverstahl, A. Graslund, L. Maler, and P. Brzezinski. Real-time transmembrane translocation of penetratin driven by light-generated proton pumping. Biophys. J. 91(4):L29-L31 (2006).
30. M. Magzoub, A. Pramanik, and A. Graslund. Modeling the endosomal escape of cell-penetrating peptides: Transmembrane pH gradient driven translocation across phospholipid bilayers. Biochemistry. 44(45):14890-14897 (2005).
31. G. Ruan, A. Agrawal, A. I. Marcus, and S. Nie. Imaging and tracking of Tat peptide-conjugated quantum dots in living cells: New insights into nanoparticle uptake, intracellular transport, and vesicle shedding. J. Am. Chem. Soc. 129(47):14759-14766 (2007).
32. D. S. Youngblood, S. A. Hatlevig, J. N. Hassinger, P. L. Iversen, and H. M. Moulton. Stability of cell-penetrating peptide-morpholino oligomer conjugates in human serum and in cells. Bioconjug. Chem. 18(1):50-60 (2007).
33. R. E. Vandenbroucke, S. C. De Smedt, J. Demeester, and N. N. Sanders. Cellular entry pathway and gene transfer capacity of TAT-modified lipoplexes. Biochim. Biophys. Acta. 1768(3):571-579 (2007).
34. J. R. Maiolo, M. Ferrer, and E. A. Ottinger. Effects of cargo molecules on the cellular uptake of arginine-rich cell-penetrating peptides. Biochim. Biophys. Acta. 1712(2):161-172 (2005).
35. R. Fischer, D. Bachle, M. Fotin-Mleczek, G. Jung, H. Kalbacher, and R. Brock. A targeted protease substrate for a quantitative determination of protease activities in the endolysosomal pathway. Chembiochem. 7(9):1428-1434 (2006).
36. J. Rinne, B. Albarran, J. Jylhava, T. O. Ihalainen, P. Kankaanpaa, V. P. Hytonen, P. S. Stayton, M. S. Kulomaa, and M. Vihinen-Ranta. Internalization of novel non-viral vector TAT-streptavidin into human cells. BMC Biotechnol. 7:1 (2007).
37. P. L. Felgner, T. R. Gadek, M. Holm, R. Roman, H. W. Chan, M. Wenz, J. P. Northrop, G. M. Ringold, and M. Danielsen. Lipofection: A highly efficient, lipid-mediated DNA-transfection procedure. Proc. Natl. Acad. Sci. USA. 84(21):7413-7417 (1987).
38. H. Farhood, N. Serbina, and L. Huang. The role of dioleoyl phosphatidylethanolamine in cationic liposome mediated gene transfer. Biochim. Biophys. Acta. 1235(2):289-295 (1995).
39. X. Zhou, and L. Huang. DNA transfection mediated by cationic liposomes containing lipopolylysine: Characterization and mechanism of action. Biochim. Biophys. Acta. 1189(2):195-203 (1994).
40. I. M. Hafez, and P. R. Cullis. Roles of lipid polymorphism in intracellular delivery. Adv. Drug Deliv. Rev. 47(2-3):139-148 (2001).
41. L. Hyndman, J. L. Lemoine, L. Huang, D. J. Porteous, A. C. Boyd, and X. Nan. HIV-1 Tat protein transduction domain peptide facilitates gene transfer in combination with cationic liposomes. J. Control. Release. 99(3):435-444 (2004).
42. K. Kogure, H. Akita, and H. Harashima. Multifunctional envelope-type nano device for non-viral gene delivery: Concept and application of Programmed Packaging. J. Control. Release. 122(3):246-251 (2007).
43. K. Kogure, H. Akita, Y. Yamada, and H. Harashima. Multifunctional envelope-type nano device (MEND) as a non-viral gene delivery system. Adv. Drug Deliv. Rev. 60(4-5):559-571 (2008).
44. 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):317-323 (2004).
45. I. A. Khalil, K. Kogure, S. Futaki, S. Hama, H. Akita, M. Ueno, H. Kishida, M. Kudoh, Y. Mishina, K. Kataoka, M. Yamada, and H. Harashima. Octaarginine-modified multifunctional envelope-type nanoparticles for gene delivery. Gene. Ther. 14(8):682-689 (2007).
46. R. Moriguchi, K. Kogure, H. Akita, S. Futaki, M. Miyagishi, K. Taira, and H. Harashima. A multifunctional envelope-type nano device for novel gene delivery of siRNA plasmids. Int. J. Pharm. 301(1-2):277-285 (2005).
47. R. Suzuki, Y. Yamada, and H. Harashima. Development of small, homogeneous pDNA particles condensed with mono-cationic detergents and encapsulated in a multifunctional envelope-type nano device. Biol. Pharm. Bull. 31(6):1237-1243 (2008).
48. Y. Nakamura, K. Kogure, Y. Yamada, S. Futaki, and H. Harashima. Significant and prolonged antisense effect of a multifunctional envelope-type nano device encapsulating antisense oligodeoxynucleotide. J. Pharm. Pharmacol. 58(4):431-437 (2006).
49. Y. Nakamura, K. Kogure, S. Futaki, and H. Harashima. Octaarginine-modified multifunctional envelope-type nano device for siRNA. J. Control. Release. 119(3):360-367 (2007).
50. 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):758-762 (2007).
51. Y. Yamada, H. Akita, H. Kamiya, K. Kogure, T. Yamamoto, Y. Shinohara, K. Yamashita, H. Kobayashi, H. Kikuchi, and H. Harashima. MITO-Porter: A liposome-based carrier system for delivery of macromolecules into mitochondria via membrane fusion. Biochim. Biophys. Acta. 1778(2):423-432 (2008).
52. T. Nakamura, R. Moriguchi, K. Kogure, N. Shastri, and H. Harashima. Efficient MHC class I presentation by controlled intracellular trafficking of antigens in octaarginine-modified liposomes. Mol. Ther. 16(8):1507-1514 (2008).
53. 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):164-173 (2008).
54. J. W. Holland, C. Hui, P. R. Cullis, and T. D. Madden. Poly(ethylene glycol)-lipid conjugates regulate the calcium-induced fusion of liposomes composed of phosphatidylethanolamine and phosphatidylserine. Biochemistry. 35(8):2618-2624 (1996).
55. R. M. Sawant, J. P. Hurley, S. Salmaso, A. Kale, E. Tolcheva, T. S. Levchenko, and V. P. Torchilin. "SMART" drug delivery systems: double-targeted pH-responsive pharmaceutical nanocarriers. Bioconjug. Chem. 17(4):943-949 (2006).
56. A. A. Kale, and V. P. Torchilin. "Smart" drug carriers: PEGylated TATp-modified pH-sensitive liposomes. J. Liposome. Res. 17(3-4):197-203 (2007).
57. A. A. Kale, and V. P. Torchilin. Enhanced transfection of tumor cells in vivo using "Smart" pH-sensitive TAT-modified pegylated liposomes. J. Drug Target. 15(7-8):538-545 (2007).
58. A. El-Sayed, I. A. Khalil, K. Kogure, S. Futaki, and H. Harashima. Octaarginine- and octalysine-modified nanoparticles have different modes of endosomal escape. J. Biol. Chem. 283(34):23450-23461 (2008).
59. P. Meers, J. Bentz, D. Alford, S. Nir, D. Papahadjopoulos, and K. Hong. Synexin enhances the aggregation rate but not the fusion rate of liposomes. Biochemistry. 27(12):4430-4439 (1988).
60. T. Maeda, K. Kawasaki, and S. Ohnishi. Interaction of influenza virus hemagglutinin with target membrane lipids is a key step in virus-induced hemolysis and fusion at pH 5.2. Proc. Natl. Acad. Sci. USA. 78(7):4133-4137 (1981).
61. P. A. Bullough, F. M. Hughson, J. J. Skehel, and D. C. Wiley. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature. 371(6492):37-43 (1994).
62. I. M. Kaplan, J. S. Wadia, and S. F. Dowdy. Cationic TAT peptide transduction domain enters cells by macropinocytosis. J. Control. Release. 102(1):247-253 (2005).
63. S. El-Andaloussi, H. J. Johansson, P. Lundberg, and U. Langel. Induction of splice correction by cell-penetrating peptide nucleic acids. J. Gene Med. 8(10):1262-1273 (2006).
64. P. Lundberg, S. El-Andaloussi, T. Sutlu, H. Johansson, and U. Langel. Delivery of short interfering RNA using endosomolytic cell-penetrating peptides. Faseb J. 21(11):2664-2671 (2007).
65. C. Plank, B. Oberhauser, K. Mechtler, C. Koch, and E. Wagner. The influence of endosome-disruptive peptides on gene transfer using synthetic virus-like gene transfer systems. J. Biol. Chem. 269(17):12918-12924 (1994).
66. E. K. Esbjorner, K. Oglecka, P. Lincoln, A. Graslund, and B. Norden. Membrane binding of pH-sensitive influenza fusion peptides. Positioning, configuration, and induced leakage in a lipid vesicle model. Biochemistry. 46(47):13490-13504 (2007).
67. T. Sugita, T. Yoshikawa, Y. Mukai, N. Yamanada, S. Imai, K. Nagano, Y. Yoshida, H. Shibata, Y. Yoshioka, S. Nakagawa, H. Kamada, S. Tsunoda, and Y. Tsutsumi. Comparative study on transduction and toxicity of protein transduction domains. Br. J. Pharmacol. 153(6):1143-1152 (2008).
68. T. Sugita, T. Yoshikawa, Y. Mukai, N. Yamanada, S. Imai, K. Nagano, Y. Yoshida, H. Shibata, Y. Yoshioka, S. Nakagawa, H. Kamada, S. Tsunoda, and Y. Tsutsumi. Improved cytosolic translocation and tumor-killing activity of Tat-shepherdin conjugates mediated by co-treatment with Tat-fused endosome-disruptive HA2 peptide. Biochem. Biophys. Res. Commun. 363(4):1027-1032 (2007).
69. T. Yoshikawa, T. Sugita, Y. Mukai, N. Yamanada, K. Nagano, H. Nabeshi, Y. Yoshioka, S. Nakagawa, Y. Abe, H. Kamada, S. Tsunoda, and Y. Tsutsumi. Organelle-targeted delivery of biological macromolecules using the protein transduction domain: Potential applications for Peptide aptamer delivery into the nucleus. J. Mol. Biol. 380(5):777-782 (2008).
70. H. Michiue, K. Tomizawa, F. Y. Wei, M. Matsushita, Y. F. Lu, T. Ichikawa, T. Tamiya, I. Date, and H. Matsui. The NH2 terminus of influenza virus hemagglutinin-2 subunit peptides enhances the antitumor potency of polyarginine-mediated p53 protein transduction. J. Biol. Chem. 280(9):8285-8289 (2005).
71. N. Ohmori, T. Niidome, A. Wada, T. Hirayama, T. Hatakeyama, and H. Aoyagi. The enhancing effect of anionic alpha-helical peptide on cationic peptide-mediating transfection systems. Biochem. Biophys. Res. Commun. 235(3):726-729 (1997).
72. S. L. Lo, and S. Wang. An endosomolytic Tat peptide produced by incorporation of histidine and cysteine residues as a nonviral vector for DNA transfection. Biomaterials. 29(15):2408-2414 (2008).
73. P. Midoux, and M. Monsigny. Efficient gene transfer by histidylated polylysine/pDNA complexes. Bioconjug. Chem. 10(3):406-411 (1999).
74. O. Boussif, F. Lezoualc'h, M. A. Zanta, M. D. Mergny, D. Scherman, B. Demeneix, and J. P. Behr. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. USA. 92(16):7297-7301 (1995).
75. D. W. Pack, A. S. Hoffman, S. Pun, and P. S. Stayton. Design and development of polymers for gene delivery. Nat. Rev. Drug Discov. 4(7):581-593 (2005).
76. C. Rudolph, C. Plank, J. Lausier, U. Schillinger, R. H. Muller, and J. Rosenecker. Oligomers of the arginine-rich motif of the HIV-1 TAT protein are capable of transferring plasmid DNA into cells. J. Biol. Chem. 278(13):11411-11418 (2003).
77. R. Q. Huang, Y. Y. Pei, and C. Jiang. Enhanced gene transfer into brain capillary endothelial cells using Antp-modified DNA-loaded nanoparticles. J. Biomed. Sci. 14(5):595-605 (2007).
78. E. Kleemann, M. Neu, N. Jekel, L. Fink, T. Schmehl, T. Gessler, W. Seeger, and T. Kissel. Nano-carriers for DNA delivery to the lung based upon a TAT-derived peptide covalently coupled to PEG-PEI. J. Control. Release. 109(1-3):299-316 (2005).
79. S. R. Sirsi, R. C. Schray, X. Guan, J. H. Williams, M. L. Erney, and G. J. Lutz. Functionalized PEG-PEI copolymers complexed to exon-skipping oligonucleotides improve dystrophin expression in mdx mice. Hum. Gene Ther. 19(8):795-806 (2008).
80. F. Alexis, S. L. Lo, and S. Wang. Covalent attachment of low molecular weight Poly(ethylene imine) improves Tat peptide mediated gene delivery. Adv. Mater. 18(16):2174-2178 (2006).
81. J. S. Suk, J. Suh, K. Choy, S. K. Lai, J. Fu, and J. Hanes. Gene delivery to differentiated neurotypic cells with RGD and HIV Tat peptide functionalized polymeric nanoparticles. Biomaterials. 27(29):5143-5150 (2006).
82. S. R. Doyle, and C. K. Chan. Differential intracellular distribution of DNA complexed with polyethylenimine (PEI) and PEI-polyarginine PTD influences exogenous gene expression within live COS-7 cells. Genet. Vaccines Ther. 5:11 (2007).
83. P. Erbacher, A. C. Roche, M. Monsigny, and P. Midoux. Putative role of chloroquine in gene transfer into a human hepatoma cell line by DNA/ lactosylated polylysine complexes. Exp. Cell. Res. 225(1):186-194 (1996).
84. K. Ciftci, and R. J. Levy. Enhanced plasmid DNA transfection with lysosomotropic agents in cultured fibroblasts. Int. J. Pharm. 218(1-2):81-92 (2001).
85. M. S. Wadhwa, D. L. Knoell, A. P. Young, and K. G. Rice. Targeted gene delivery with a low molecular weight glycopeptide carrier. Bioconjug. Chem. 6(3):283-291 (1995).
86. E. Jeon, H. D. Kim, and J. S. Kim. Pluronic-grafted poly-(L)-lysine as a new synthetic gene carrier. J. Biomed. Mater. Res. A. 66(4):854-859 (2003).
87. T. Katav, L. Liu, T. Traitel, R. Goldbart, M. Wolfson, and J. Kost. Modified pectin-based carrier for gene delivery: Cellular barriers in gene delivery course. J. Control. Release. 130(20):183-191 (2008).
88. N. J. Caron, S. P. Quenneville, and J. P. Tremblay. Endosome disruption enhances the functional nuclear delivery of Tat-fusion proteins. Biochem. Biophys. Res. Commun. 319(1):12-20 (2004).
89. T. Shiraishi, S. Pankratova, and P. E. Nielsen. Calcium ions effectively enhance the effect of antisense peptide nucleic acids conjugated to cationic tat and oligoarginine peptides. Chem. Biol. 12(8):923-929 (2005).
90. T. Shiraishi, and P. E. Nielsen. Enhanced delivery of cell-penetrating peptide-peptide nucleic acid conjugates by endosomal disruption. Nat. Protoc. 1(2):633-636 (2006).
91. S. Abes, J. J. Turner, G. D. Ivanova, D. Owen, D. Williams, A. Arzumanov, P. Clair, M. J. Gait, and B. Lebleu. Efficient splicing correction by PNA conjugation to an R6-Penetratin delivery peptide. Nucleic Acids Res. 35(13):4495-4502 (2007).
92. A. Hogset, L. Prasmickaite, P. K. Selbo, M. Hellum, B. O. Engesaeter, A. Bonsted, and K. Berg. Photochemical internalisation in drug and gene delivery. Adv. Drug Deliv. Rev. 56(1):95-115 (2004).
93. M. Matsushita, H. Noguchi, Y. F. Lu, K. Tomizawa, H. Michiue, S. T. Li, K. Hirose, S. Bonner-Weir, and H. Matsui. Photo-acceleration of protein release from endosome in the protein transduction system. FEBS Lett. 572(1-3):221-226 (2004).
94. T. Shiraishi, and P. E. Nielsen. Photochemically enhanced cellular delivery of cell penetrating peptide-PNA conjugates. FEBS Lett. 580(5):1451-1456 (2006).
95. M. Folini, R. Bandiera, E. Millo, P. Gandellini, G. Sozzi, P. Gasparini, N. Longoni, M. Binda, M. G. Daidone, K. Berg, and N. Zaffaroni. Photochemically enhanced delivery of a cell-penetrating peptide nucleic acid conjugate targeting human telomerase reverse transcriptase: Effects on telomere status and proliferative potential of human prostate cancer cells. Cell. Prolif. 40(6):905-920 (2007).
96. K. Berg, A. Hogset, L. Prasmickaite, A. Weyergang, A. Bonsted, A. Dietze, P. J. Lou, S. Bown, O. J. Norum, H. M. T. Mollergard, and P. K. Selbo. Photochemical internalization (PCI): A novel technology for activation of endocytosed therapeutic agents. Med. Laser Appl. 21(4):239-250 (2006).