Therapeutic applications of the cell-penetrating HIV-1 Tat peptide

Drug Discovery Today

Volumn 20, Issue 1, 2015, Pages 76-85

  Rizzuti, Mafalda ^a   Nizzardo, Monica ^a   Zanetta, Chiara ^a   Ramirez, Agnese ^a   Corti, Stefania ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CELL PENETRATING PEPTIDE; LIPOSOME; NANOPARTICLE; NUCLEIC ACID; TRANSACTIVATOR PROTEIN; ANTIBODY; DRUG;

CELL MEMBRANE TRANSPORT; CLINICAL TRIAL (TOPIC); DEGENERATIVE DISEASE; DRUG ADMINISTRATION ROUTE; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERNALIZATION; NONHUMAN; PERMEABILITY BARRIER; REVIEW; ANIMAL; CHEMISTRY;

ANIMALS; ANTIBODIES; CELL-PENETRATING PEPTIDES; DRUG DELIVERY SYSTEMS; HIV-1; HUMANS; NANOPARTICLES; NUCLEIC ACIDS; OLIGONUCLEOTIDES, ANTISENSE; PHARMACEUTICAL PREPARATIONS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84922469442     PISSN: 13596446     EISSN: 18785832     Source Type: Journal    
DOI: 10.1016/j.drudis.2014.09.017     Document Type: Review

References (93)

1. Eugenin, E.A. et al. (2011) Human immunodeficiency virus infection of human astrocytes disrupts blood-brain barrier integrity by a gap junction-dependent mechanism. J. Neurosci. 31, 9456-9465
2. Koren, E. and Torchilin, V.P. (2012) Cell-penetrating peptides: breaking through to the other side. Trends Mol. Med. 18, 385-393
3. Milletti, F. (2012) Cell-penetrating peptides: classes, origin, and current landscape. Drug Discov. Today 17, 850-860
4. Frankel, A.D. and Pabo, C.O. (1988) Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55, 1189-1193
5. Joliot, A. et al. (1991) Antennapedia homeobox peptide regulates neural morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 88, 1864-1868
6. Richard, J.P. et al. (2003) Cell-penetrating peptides. A re-evaluation of the mechanism of cellular uptake. J. Biol. Chem. 278, 585-590
7. Nestor, J.J. (2009) The medicinal chemistry of peptides. Curr. Med. Chem. 16, 4399-4418
8. Bechara, C. and Sagan, S. (2013) Cell-penetrating peptides: 20 years later, where do we stand? FEBS Lett. 587, 1693-1702
9. Tünnemann, G. et al. (2008) Live-cell analysis of cell penetration ability and toxicity of oligo-arginines. J. Pept. Sci. 14, 469-476
10. Foged, C. and Nielsen, H.M. (2008) Cell-penetrating peptides for drug delivery across membrane barriers. Expert Opin. Drug. Deliv. 5, 105-117
11. Derossi, D. et al. (1996) Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biol. Chem. 271, 18188-18193
12. Nakase, I. et al. (2007) Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis. Biochemistry 46, 492-501
13. Conner, S.D. and Schmid, S.L. (2003) Regulated portals of entry into the cell. Nature 422, 37-44
14. Tünnemann, G. et al. (2006) Cargo-dependent mode of uptake and bioavailability of TAT-containing proteins and peptides in living cells. FASEB J. 20, 1775-1784
15. Madani, F. et al. (2011) Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys. 2011, 414729
16. Duchardt, F. et al. (2007) A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8, 848-866
17. Ezzat, K. et al. (2012) Scavenger receptor-mediated uptake of cell-penetrating peptide nanocomplexes with oligonucleotides. FASEB J. 26, 1172-1180
18. Feng, S. and Holland, E.C. (1988) HIV-1 tat trans-activation requires the loop sequence within tar. Nature 334, 165-167
19. Ott, M. et al. (2004) Tat acetylation: a regulatory switch between early and late phases in HIV transcription elongation. Novartis Found. Symp. 259, 182-193
20. Banks, W.A. et al. (2005) Permeability of the blood-brain barrier to HIV-1 Tat. Exp. Neurol. 193, 218-227
21. Xu, R. et al. (2012) HIV-1 Tat protein increases the permeability of brain endothelial cells by both inhibiting occluding expression and cleaving occludin via matrix metalloproteinase-9. Brain Res. 1436, 13-19
22. Mediouni, S. et al. (2012) Antiretroviral therapy does not block the secretion of the human immunodeficiency virus tat protein. Infect. Disord. Drug Targets 12, 81-86
23. Cooper, I.S.K. et al. (2012) Peptide derived from HIV-1 TAT protein, destabilizes a monolayer of endothelial cells in an in vitro model of the blood-brain barrier, and allows permeation of high molecular weight proteins. J. Biol. Chem. 287, 44676-44683
24. Polyakov, V. et al. (2000) Novel TAT-peptide chelates fordirect transduction of technetium-99m and rhenium into human cells for imaging and radiotherapy. Bioconjug. Chem. 11, 762-771
25. Bhorade, R. et al. (2000) Macrocyclic chelators with paramagnetic cations are internalized into mammalian cells via a HIV-tat derived membrane translocation peptide. Bioconjug. Chem. 11, 301-305
26. Bullok, K.E. et al. (2002) Characterization of novel histidine-tagged Tat-peptide complexes dual-labeled with (99m)Tc-tricarbonyl and fluorescein for scintigraphy and fluorescence microscopy. Bioconjug. Chem. 13, 1226-1237
27. Anderson, D.C. et al. (1993) Tumor cell retention of antibody Fab fragments is enhanced by an attached HIV TAT protein-derived peptide. Biochem. Biophys. Res. Commun. 194, 876-884
28. Niesner, U. et al. (2002) Quantitation of the tumor-targeting properties of antibody fragments conjugated to cell-permeating HIV-1 TAT peptides. Bioconjug. Chem. 13, 729-736
29. Stein, S. et al. (1999) A disulfide conjugate between anti-tetanus antibodies and HIV (37-72)Tat neutralizes tetanus toxin inside chromaffin cells. FEBS Lett. 458, 383-386
30. Mie, M. et al. (2003) Intracellular delivery of antibodies using TAT fusion protein A. Biochem. Biophys. Res. Commun. 310, 730-734
31. Falnes, P.O. et al. (2001) Ability of the Tat basic domain and VP22 to mediate cell binding, but not membrane translocation of the diphtheria toxin A-fragment. Biochemistry 40, 4349-4358
32. Nori, A. et al. (2003) Tat-conjugated synthetic macromolecules facilitate cytoplasmic drug delivery to human ovarian carcinoma cells. Bioconjug. Chem. 14, 44-50
33. Fawell, S. et al. (1994) Tat-mediated delivery of heterologous proteins into cells. Proc. Natl. Acad. Sci. U. S. A. 91, 664-668
34. Kim, D.T. et al. (1997) Introduction of soluble proteins into the MHC class I pathway by conjugation to an HIV tat peptide. J. Immunol. 159, 1666-1668
35. Shibagaki, N. and Udey, M.C. (2002) Dendritic cells transduced with protein antigens induce cytotoxic lymphocytes and elicit antitumor immunity. J. Immunol. 168, 2393-2401
36. Guelen, L. et al. (2004) TAT-apoptin is efficiently delivered and induces apoptosis in cancer cells. Oncogene 23, 1153-1165
37. Embury, J. et al. (2001) Proteins linked to a protein transduction domain efficiently transduce pancreatic islets. Diabetes 50, 1706-1713
38. Liang, J.F. and Yang, V.C. (2005) Insulin-cell penetrating peptide hybrids with improved intestinal absorption efficiency. Biochem. Biophys. Res. Commun. 335, 734-738
39. Cao, G. et al. (2002) 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, 5423-5431
40. Asoh, S. et al. (2002) Protection against ischemic brain injury by protein therapeutics. Proc. Natl. Acad. Sci. U. S. A. 99, 17107-17112
41. Gupta, B. et al. (2005) Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv. Drug Deliv. Rev. 57, 637-651
42. Tseng, Y.L. et al. (2002) Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study. Mol. Pharmacol. 62, 864-872
43. Levchenko, T.S. et al. (2003) Tat peptide-mediated intracellular delivery of liposomes. Methods Enzymol. 372, 339-349
44. Torchilin, V.P. et al. (2001) 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, 8786-8791
45. Torchilin, V.P. et al. (2003) Cell transfection in vitro and in vivo with nontoxic TAT peptide-liposome-DNA complexes. Proc. Natl. Acad. Sci. U. S. A. 100, 1972-1977
46. Torchilin, V.P. and Levchenko, T.S. (2003) TAT-liposomes: a novel intracellular drug carrier. Curr. Protein Pept. Sci. 4, 133-140
47. Gupta, B. et al. (2007) TAT peptide-modified liposomes provide enhanced gene delivery to intracranial human brain tumor xenografts in nude mice. Oncol. Res. 16, 351-359
48. Sawant, R.M. et al. (2006) "SMART" drug delivery systems: double-targeted pH-responsive pharmaceutical nanocarriers. Bioconjug. Chem. 17, 943-949
49. Qin, Y. et al. (2011) Liposome formulated with TAT-modified cholesterol for improving brain delivery and therapeutic efficacy on brain glioma in animals. Int. J. Pharm. 420, 304-312
50. Qin, Y. et al. (2012) Comparison of four different peptides to enhance accumulation of liposomes into the brain. J. Drug Target 20, 235-245
51. Paolino, D. et al. (2011) Supramolecular devices to improve the treatment of brain diseases. Drug Discov. Today 16, 311-324
52. Bondì, M.L. et al. (2012) Lipid nanoparticles for drug targeting to the brain. Methods Enzymol. 508, 229-251
53. Torchilin, V.P. (2007) Tatp-mediated intracellular delivery of pharmaceutical nanocarriers. Biochem. Soc. Trans. 35, 816-820
54. Liu, J. et al. (2001) Nanostructured materials designed for cell binding and transduction. Biomacromolecules 2, 362-368
55. Wunderbaldinger, P. et al. (2002) Tat peptide directs enhanced clearance and hepatic permeability of magnetic nanoparticles. Bioconjug. Chem. 13, 264-268
56. Josephson, L. et al. (1999) High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. Bioconjug. Chem. 10, 186-191
57. Zhao, M. et al. (2002) Differential conjugation of tat peptide to superparamagnetic nanoparticles and its effect on cellular uptake. Bioconjug. Chem. 13, 840-844
58. Lewin, M. et al. (2000) Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat. Biotechnol. 18, 410-414
59. Santra, S. et al. (2004) TAT conjugated, FITC doped silica nanoparticles for bioimaging applications. Chem. Commun. 24, 2810-2811
60. Han, L. et al. (2010) Tat-BMPs-PAMAM conjugates enhance therapeutic effect of small interference RNA on U251 glioma cells in vitro and in vivo. Hum. Gene Ther. 21, 417-426
61. Kanazawa, T. et al. (2011) Cell-penetrating peptide-modified block copolymer micelles promote direct brain delivery via intranasal administration. Pharm. Res. 28, 2130-2139
62. Kanazawa, T. et al. (2013) Delivery of siRNA to the brain using a combination of nose-to-brain delivery and cell-penetrating peptide-modified nano-micelles. Biomaterials 34, 9220-9226
63. Wagstaff, K.M. and Jans, D.A. (2006) Protein transduction: cell penetrating peptides and their therapeutic applications. Curr. Med. Chem. 13, 1371-1387
64. Tasciotti, E. et al. (2003) Transcellular transfer of active HSV-1 thymidine kinase mediated by an 11-amino-acid peptide from HIV-1 Tat. Cancer Gene Ther. 10, 64-74
65. Eguchi, A. et al. (2001) Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J. Biol. Chem. 276, 26204-26210
66. Rudolph, C. et al. (2003) Oligomers of the arginine-rich motif of the HIV-1 TAT protein are capable of transferring plasmid DNA into cells. J. Biol. Chem. 278, 11411-11418
67. Järver, P. and Langel, U. (2004) The use of cell-penetrating peptides as a tool for gene regulation. Drug Discov. Today 9, 395-402
68. Koppelhus, U. et al. (2002) Cell-dependent differential cellular uptake of PNA, peptides, and PNA-peptide conjugates. Antisense Nucleic Acid Drug Dev. 12, 51-63
69. Nakase, I. et al. (2013) Cell-penetrating peptides (CPPs) as a vector for the delivery of siRNAs into cells. Mol. Biosyst. 9, 855-861
70. Morris, M.C. et al. (2000) Translocating peptides and proteins and their use for gene delivery. Curr. Opin. Biotechnol. 11, 461-466
71. Williams, J.H. et al. (2009) Oligonucleotide-mediated survival of motor neuron protein expression in CNS improves phenotype in a mouse model of spinal muscular atrophy. J. Neurosci. 29, 7633-7638
72. Hua, Y. et al. (2010) Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model. Genes Dev. 24, 1634-1644
73. Passini, M.A. and Cheng, S.H. (2011) Prospects for the gene therapy of spinal muscular atrophy. Trends Mol. Med. 17, 259-265
74. Summerton, J. and Weller, D. (1997) Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 7, 187-195
75. Madocsai, C. et al. (2005) Correction of SMN2 pre-mRNA splicing by antisense U7 small nuclear RNAs. Mol. Ther. 12, 1013-1022
76. Muntoni, F. and Wood, M.J. (2011) Targeting RNA to treat neuromuscular disease. Nat. Rev. Drug Discov. 10, 621-637
77. Amantana, A. et al. (2007) Pharmacokinetics, biodistribution, stability and toxicity of a cell-penetrating peptide-morpholino oligomer conjugate. Bioconjug. Chem. 18, 1325-1331
78. Betts, C. et al. (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
79. Moulton, H.M. et al. (2003) HIV Tat peptide enhances cellular delivery of antisense morpholino oligomers. Antisense Nucleic Acid Drug Dev. 13, 31-43
80. Moulton, H.M. and Moulton, J.D. (2010) Morpholinos and their peptide conjugates: therapeutic promise and challenge for Duchenne muscular dystrophy. Biochim. Biophys. Acta 1798, 2296-2303
81. Moulton, H.M. (2013) In vivo delivery of morpholino oligos by cell-penetrating peptides. Curr. Pharm. Des. 19, 2963-2969
82. Astriab-Fisher, A. et al. (2002) 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, 744-754
83. Hill, M.D. et al. (2012) Safety and efficacy of NA-1 in patients with iatrogenic stroke after endovascular aneurysm repair (ENACT): a phase 2, randomised, double-blind, placebo-controlled trial. Lancet Neurol. 11, 942-950
84. Pooga, M. et al. (1998) Cell penetrating PNA constructs regulate galanin receptor levels and modify pain transmission in vivo. Nat. Biotechnol. 16, 857-861
85. Saar, K. et al. (2005) Cell-penetrating peptides: a comparative membrane toxicity study. Anal. Biochem. 345, 55-65
86. Santana, A. et al. (1993) Inflammatory responses induced by poly-L-arginine in rat lungs in vivo. Agents Actions 39, 104-110
87. Shahana, S. et al. (2002) Effects of the cationic protein poly-L-arginine on airway epithelial cells in vitro. Mediators Inflamm. 11, 141-148
88. Tréhin, R. and Merkle, H.P. (2004) Chances and pitfalls of cell penetrating peptides for cellular drug delivery. Eur. J. Pharm. Biopharm. 58, 209-223
89. Jones, S.W. et al. (2005) Characterisation of cell-penetrating peptide-mediated peptide delivery. Br. J. Pharmacol. 145, 1093-1102
90. Lalatsa, A. et al. (2014) Strategies to deliver peptide drugs to the brain. Mol. Pharm. 11, 1081-1093
91. Martin, I. et al. (2010) Building cell selectivity into CPP-mediated strategies. Pharmaceutics 3, 1456-1490
92. Olson, E.S. et al. (2009) In vivo characterization of activatable cell-penetrating peptides for targeting protease activity in cancer. Integr. Biol. 1, 382-393
93. Reissmann, S. (2014) Cell penetration: scope and limitations by the application of cell-penetrating peptides. J. Pept. Sci. 20, 760-784