The use of cell-penetrating peptides for drug delivery

Drug Discovery Today

Volumn 9, Issue 23, 2004, Pages 1012-1019

  Temsamani, Jamal ^a   Vidal, Pierre ^a  

^a Synt:em   (France)

Author keywords

Biochemistry; Blood brain barrier; Brain uptake; Chemical Biology; Drug Discovery; Intracellular delivery; Multidrug resistance; Peptide vector; Pharmaceutical Science

Indexed keywords

ANTIINFECTIVE AGENT; ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE INHIBITOR; DOXORUBICIN; DRUG CARRIER; OLIGONUCLEOTIDE; PENETRATIN; PEPTIDE; PHOSPHOPEPTIDE; PROTEGRIN; PROTEIN SYNB1; PROTEIN SYNB3; RECOMBINANT PROTEIN; TRANSACTIVATOR PROTEIN; TRANSPORTAN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CELL MEMBRANE; CYTOPLASM; DRUG ACTIVITY; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MECHANISM; DRUG PENETRATION; DRUG UPTAKE; EXPERIMENTAL MOUSE; EXPERIMENTAL RAT; GENE DELIVERY SYSTEM; HYDROPHILICITY; MOLECULE; PROTEIN TRANSPORT; REVIEW;

BLOOD-BRAIN BARRIER; CELL MEMBRANE PERMEABILITY; DRUG CARRIERS; HUMANS; PEPTIDES;

EID: 9644289511     PISSN: 13596446     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1359-6446(04)03279-9     Document Type: Review

References (92)

1. Temsamani J., Scherrmann J.M. Peptide vectors as drug carriers. Prog. Drug Res. 61:2003;221-238
2. Lindgren M., et al. Cell-penetrating peptides. Trends Pharmacol. Sci. 21:2000;99-103
3. Joliot A., Prochiantz A. Transduction peptides: from technology to physiology. Nat. Cell Biol. 6:2004;189-196
4. Lindgren M., et al. Translocation properties of novel cell-penetrating transportan and penetratin analogues. Bioconjug. Chem. 11:2000;619-626
5. Drin G., et al. Studies on the internalization mechanism of cationic cell-penetrating peptides. J. Biol. Chem. 278:2003;31192-31201
6. Kokryakov V.N., et al. Protegrins: leukocyte antimicrobial peptides that combine features of corticostatic defensins and tachyplesins. FEBS Lett. 327:1993;231-236
7. Mangoni M.E., et al. Change in membrane permeability induced by protegrin 1: implication of disulfide bridges for pore formation. FEBS Lett. 383:1996;93-98
8. Sokolov Y., et al. Membrane channel formation by antimicrobial protegrins. Biochim. Biophys. Acta. 1420:1999;23-29
9. Drin G., Temsamani J. Translocation of protegrin I through phospholipid membranes: role of peptide folding. Biochim. Biophys. Acta. 1559:2002;160-170
10. Derossi D., et al. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269:1994;10444-10450
11. Joliot A., et al. Antennapedia homeobox peptide regulates neural morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 88:1991;1864-1868
12. Le Roux I., et al. Neurotrophic activity of the Antennapedia homeodomain depends on its specific DNA-binding properties. Proc. Natl. Acad. Sci. U. S. A. 90:1993;9120-9124
13. Derossi D., et al. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biol. Chem. 271:1996;18188-18193
14. Drin G., et al. Translocation of the pAntp peptide and its amphipathic analogue AP-2AL. Biochemistry. 40:2001;1824-1834
15. Persson D., et al. Penetratin-induced aggregation and subsequent dissociation of negatively charged phospholipid vesicles. FEBS Lett. 505:2001;307-312
16. Frankel A.D., Pabo C.O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell. 55:1988;1189-1193
17. Vives E., et al. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 272:1997;16010-16017
18. Nagahara H., et al. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat. Med. 4:1998;1449-1452
19. Mann D.A., Frankel A.D. Endocytosis and targeting of exogenous HIV-1 Tat protein. EMBO J. 10:1991;1733-1739
20. Trehin R., Merkle H.P. Chances and pitfalls of cell penetrating peptides for cellular drug delivery. Eur. J. Pharm. Biopharm. 58:2004;209-223
21. Potocky T.B., et al. Cytoplasmic and nuclear delivery of a TAT-derived peptide and a beta-peptide after endocytic uptake into HeLa cells. J. Biol. Chem. 278:2003;50188-50194
22. Richard J.P., et al. Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake. J. Biol. Chem. 278:2003;585-590
23. Fischer R., et al. A stepwise dissection of the intracellular fate of cationic cell-penetrating peptides. J. Biol. Chem. 279:2004;12625-12635
24. Wadia J.S., et al. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10:2004;310-315
25. Pooga M., et al. Cell penetration by transportan. FASEB J. 12:1998;67-77
26. Oehlke J., et al. Cellular uptake of an alpha-helical amphipathic model peptide with the potential to deliver polar compounds into the cell interior non-endocytically. Biochim. Biophys. Acta. 1414:1998;127-139
27. Scheller A., et al. Structural requirements for cellular uptake of alpha-helical amphipathic peptides. J. Pept. Sci. 5:1999;185-194
28. Chaloin L., et al. Conformations of primary amphipathic carrier peptides in membrane mimicking environments. Biochemistry. 36:1997;11179-11187
29. Vidal P., et al. Interactions of primary amphipathic vector peptides with membranes. Conformational consequences and influence on cellular localization. J. Membr. Biol. 162:1998;259-264
30. Mitchell D.J., et al. Polyarginine enters cells more efficiently than other polycationic homopolymers. J. Pept. Res. 56:2000;318-325
31. Langel U. Review of Cell-Penetrating Peptides: Processes and Applications. 2002;CRC Press
32. Snyder E.L., Dowdy S.F. Cell-penetrating peptides in drug delivery. Pharm. Res. 21:2004;389-393
33. Derossi D., et al. Stimulation of mitogenesis by a cell-permeable PI 3-kinase binding peptide. Biochem. Biophys. Res. Commun. 251:1998;148-152
34. Hall H., et al. Inhibition of FGF-stimulated phosphatidylinositol hydrolysis and neurite outgrowth by a cell-membrane permeable phosphopeptide. Curr. Biol. 6:1996;580-587
35. Williams E.J., et al. Selective inhibition of growth factor-stimulated mitogenesis by a cell-permeable Grb2-binding peptide. J. Biol. Chem. 272:1997;22349-22354
36. Bardelli A., et al. A peptide representing the carboxyl-terminal tail of the met receptor inhibits kinase activity and invasive growth. J. Biol. Chem. 274:1999;29274-29281
37. Cussac D., et al. A Sos-derived peptidimer blocks the Ras signaling pathway by binding both Grb2 SH3 domains and displays antiproliferative activity. FASEB J. 13:1999;31-38
38. Mutoh M., et al. A p21(Waf1/Cip1)carboxyl-terminal peptide exhibited cyclin-dependent kinase-inhibitory activity and cytotoxicity when introduced into human cells. Cancer Res. 59:1999;3480-3488
39. Bonfanti M., et al. p21WAF1-derived peptides linked to an internalization peptide inhibit human cancer cell growth. Cancer Res. 57:1997;1442-1446
40. Fahraeus R., et al. Inhibition of pRb phosphorylation and cell-cycle progression by a 20-residue peptide derived from p16CDKN2/INK4A. Curr. Biol. 6:1996;84-91
41. Gius D.R., et al. Transduced p16INK4a peptides inhibit hypophosphorylation of the retinoblastoma protein and cell cycle progression prior to activation of Cdk2 complexes in late G1. Cancer Res. 59:1999;2577-2580
42. Lu J., et al. TAP-independent presentation of CTL epitopes by Trojan antigens. J. Immunol. 166:2001;7063-7071
43. Kim D.T., et al. Introduction of soluble proteins into the MHC class I pathway by conjugation to an HIV tat peptide. J. Immunol. 159:1997;1666-1668
44. Pietersz G.A., et al. A 16-mer peptide (RQIKIWFQNRRMKWKK) from antennapedia preferentially targets the Class I pathway. Vaccine. 19:2001;1397-1405
45. Day F.H., et al. Induction of antigen-specific CTL responses using antigens conjugated to short peptide vectors. J. Immunol. 170:2003;1498-1503
46. Troy C.M., et al. Downregulation of Cu/Zn superoxide dismutase leads to cell death via the nitric oxide-peroxynitrite pathway. J. Neurosci. 16:1996;253-261
47. Morris M.C., et al. A new peptide vector for efficient delivery of oligonucleotides into mammalian cells. Nucleic Acids Res. 25:1997;2730-2736
48. Astriab-Fisher A., et al. Conjugates of antisense oligonucleotides with the Tat and antennapedia cell-penetrating peptides: effects on cellular uptake, binding to target sequences, and biologic actions. Pharm. Res. 19:2002;744-754
49. Moulton H.M., et al. HIV Tat peptide enhances cellular delivery of antisense morpholino oligomers. Antisense Nucleic Acid Drug Dev. 13:2003;31-43
50. Pooga M., et al. Cell-penetrating PNA constructs regulate galanin receptor levels and modify pain transmission in vivo. Nat. Biotechnol. 16:1998;857-861
51. Eguchi A., et al. Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J. Biol. Chem. 276:2001;26204-26210
52. Snyder E.L., Dowdy S.F. Protein/peptide transduction domains: potential to deliver large DNA molecules into cells. Curr. Opin. Mol. Ther. 3:2001;147-152
53. Tung C.H., et al. Novel branching membrane translocational peptide as gene delivery vector. Bioorg. Med. Chem. 10:2002;3609-3614
54. Ignatovich I.A., et al. Complexes of plasmid DNA with basic domain 47-57 of the HIV-1 Tat protein are transferred to mammalian cells by endocytosis-mediated pathways. J. Biol. Chem. 278:2003;42625-42636
55. Lewin M., et al. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat. Biotechnol. 18:2000;410-414
56. Becker M.L., et al. Peptide-derivatized shell-cross-linked nanoparticles. 2. Biocompatibility evaluation. Bioconjug. Chem. 15:2004;710-717
57. Torchilin V.P., et al. TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors. Proc. Natl. Acad. Sci. U. S. A. 98:2001;8786-8791
58. Console S., et al. Antennapedia and HIV transactivator of transcription (TAT) 'protein transduction domains' promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans. J. Biol. Chem. 278:2003;35109-35114
59. Tseng Y.L., et al. Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study. Mol. Pharmacol. 62:2002;864-872
60. Torchilin V.P., et al. Cell transfection in vitro and in vivo with nontoxic TAT peptide-liposome-DNA complexes. Proc. Natl. Acad. Sci. U. S. A. 100:2003;1972-1977
61. Gorodetsky R., et al. Liposome transduction into cells enhanced by haptotactic peptides (Haptides) homologous to fibrinogen C-termini. J. Control. Release. 95:2004;477-488
62. Gorodetsky R., et al. New cell attachment peptide sequences from conserved epitopes in the carboxy termini of fibrinogen. Exp. Cell Res. 287:2003;116-129
63. Pardridge W.M. Why is the global CNS pharmaceutical market so under-penetrated? Drug Discov. Today. 7:2002;5-7
64. Pardridge W.M. New approaches to drug delivery through the blood-brain barrier. Trends Biotechnol. 12:1994;239-245
65. Jolliet-Riant P., Tillement J.P. Drug transfer across the blood-brain barrier and improvement of brain delivery. Fundam. Clin. Pharmacol. 13:1999;16-26
66. Temsamani J., et al. Vector-mediated drug delivery to the brain. Expert Opin. Biol. Ther. 1:2001;773-782
67. Rousselle C., et al. New advances in the transport of doxorubicin through the blood-brain barrier by a peptide vector-mediated strategy. Mol. Pharmacol. 57:2000;679-686
68. Rousselle C., et al. Enhanced delivery of doxorubicin into the brain via a peptide vector-mediated strategy: saturation kinetics and specificity. J. Pharmacol. Exp. Ther. 296:2001;124-131
69. Mazel M., et al. Doxorubicin-peptide conjugates overcome multidrug resistance. Anti-Cancer Drugs. 12:2001;107-116
70. Bolton S.J., et al. Cellular uptake and spread of the cell-permeable peptide penetratin in adult rat brain. Eur. J. Neurosci. 12:2000;2847-2855
71. Rousselle C., et al. Improved brain delivery of benzylpenicillin with a peptide vector-mediated strategy. J. Drug Target. 10:2002;309-315
72. Rousselle C., et al. Improved brain uptake and pharmacological activity of dalargin using a peptide vector-mediated strategy. J. Pharmacol. Exp. Ther. 306:2003;371-376
73. Schroeder U., et al. Body distribution of 3H-labelled dalargin bound to poly(butyl cyanoacrylate) nanoparticles after i.v. injections to mice. Life Sci. 66:2000;495-502
74. Schwarze S.R., et al. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science. 285:1999;1569-1572
75. Cao G., et al. In vivo delivery of a Bcl-xL fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis. J. Neurosci. 22:2002;5423-5431
76. Kilic E., et al. Intravenous TAT-Bcl-Xl is protective after middle cerebral artery occlusion in mice. Ann. Neurol. 52:2002;617-622
77. Asoh S., et al. Protection against ischemic brain injury by protein therapeutics. Proc. Natl. Acad. Sci. U. S. A. 99:2002;17107-17112
78. Aarts M., et al. Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science. 298:2002;846-850
79. Theodore L., et al. Intraneuronal delivery of protein kinase C pseudosubstrate leads to growth cone collapse. J. Neurosci. 15:1995;7158-7167
80. Chen L., et al. Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc. Natl. Acad. Sci. U. S. A. 98:2001;11114-11119
81. Schutze-Redelmeier M.P., et al. Introduction of exogenous antigens into the MHC class I processing and presentation pathway by Drosophila antennapedia homeodomain primes cytotoxic T cells in vivo. J. Immunol. 157:1996;650-655
82. Perez F., et al. Rab3A and Rab3B carboxy-terminal peptides are both potent and specific inhibitors of prolactin release by rat cultured anterior pituitary cells. Mol. Endocrinol. 8:1994;1278-1287
83. Fujimoto K., et al. Inhibition of pRb phosphorylation and cell cycle progression by an antennapedia-p16(INK4A) fusion peptide in pancreatic cancer cells. Cancer Lett. 159:2000;151-158
84. Datta K., et al. The 104-123 amino acid sequence of the beta-domain of von Hippel-Lindau gene product is sufficient to inhibit renal tumor growth and invasion. Cancer Res. 61:2001;1768-1775
85. Rojas M., et al. Genetic engineering of proteins with cell membrane permeability. Nat. Biotechnol. 16:1998;370-375
86. Fawell S., et al. Tat-mediated delivery of heterologous proteins into cells. Proc. Natl. Acad. Sci. U. S. A. 91:1994;664-668
87. Gustafsson A.B., et al. TAT protein transduction into isolated perfused hearts: TAT-apoptosis repressor with caspase recruitment domain is cardioprotective. Circulation. 106:2002;735-739
88. Arnt C.R., et al. Synthetic Smac/DIABLO peptides enhance the effects of chemotherapeutic agents by binding XIAP and cIAP1 in situ. J. Biol. Chem. 277:2002;44236-44243
89. Yang Y., et al. HIV-1 TAT-mediated protein transduction and subcellular localization using novel expression vectors. FEBS Lett. 532:2002;36-44
90. Allinquant B., et al. Downregulation of amyloid precursor protein inhibits neurite outgrowth in vitro. J. Cell Biol. 128:1995;919-927
91. Astriab-Fisher A., et al. Antisense inhibition of P-glycoprotein expression using peptide-oligonucleotide conjugates. Biochem. Pharmacol. 60:2000;83-90
92. Chaloin L., et al. Design of carrier peptide-oligonucleotide conjugates with rapid membrane translocation and nuclear localization properties. Biochem. Biophys. Res. Commun. 243:1998;601-608