Transduction peptides: From technology to physiology

Nature Cell Biology

Volumn 6, Issue 3, 2004, Pages 189-196

  Joliot, Alan ^a   Prochiantz, Alain ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; HOMEODOMAIN PROTEIN; HYBRID PROTEIN; MEMBRANE PROTEIN; PRION PROTEIN; TRANSACTIVATOR PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOTECHNOLOGY; CELL MEMBRANE PERMEABILITY; CELL SPECIFICITY; CYTOSOL; HOMOLOGOUS RECOMBINATION; HYDROPHILICITY; HYDROPHOBICITY; IN VIVO STUDY; MOLECULAR MIMICRY; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; GENETIC VECTORS; HUMANS; PEPTIDES; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; TRANSDUCTION, GENETIC;

EID: 1542609485     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb0304-189     Document Type: Article

References (68)

1. Frankel, A. D. & Pabo, C. O. Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 55, 1189-1193 (1988).
2. Green, M. & Loewenstein, P. M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 55, 1179-1188 (1988).
3. Joliot, A., Pernelle, C., Deagostini-Bazin, H. & Prochiantz, A. Antennapedia homeobox peptide regulates neural morphogenesis. Proc. Natl Acad. Sci. USA 88, 1864-1868 (1991).
4. Chatelin, L., Volovitch, M., Joliot, A. H., Perez, F. & Prochiantz, A. Transcription factor Hoxa-5 is taken up by cells in culture and conveyed to their nuclei. Mech. Dev. 55, 111-117 (1996).
5. Helland, D. E., Welles, J. L., Caputo, A. & Haseltine, W. A. Transcellular transactivation by the human immunodeficiency virus type 1 tat protein. J. Virol. 65, 4547-4549 (1991).
6. Joliot, A. et al. Identification of a signal sequence necessary for the unconventional secretion of Engrailed homeoprotein. Curr. Biol. 8, 856-863 (1998).
7. Prochiantz, A. Messenger proteins: Homeoproteins, TAT and others. Curr. Opin. Cell Biol. 12, 400-406 (2000).
8. Prochiantz, A. & Joliot, A. Can transcription factors function as cell-cell signalling molecules? Nature Rev. Mol. Cell. Biol. 4, 6-11 (2003).
9. Stenmark, H., Moskaug, J. O., Madshus, I. H., Sandvig, K. & Olsnes, S. Peptides fused to the aminoterminal end of diphteria toxin are translocated to the cytosol. J. Cell Biol. 113, 1025-1032 (1991).
10. Madshus, I., Stenmark, H., Sandvig, K. & Olsnes, S. Entry of Diphtheria toxin-Protein-A chimeras into cells. J. Biol. Chem. 266, 17446-17453 (1991).
11. Elliott, G. & O'Hare, P. Intercellular trafficking and protein delivery by a herpes virus structural protein. Cell 88, 223-233 (1997).
12. Lin, Y. Z., Yao, S. Y., Veach, R. A., Torgerson, T. R. & Hawiger, J. Inhibition of nuclear translocation of transcription factor NF-κB by a synthetic peptide containing a cell membrane-permeable motif and nuclear localization sequence. J. Biol. Chem. 270, 14255-14258 (1995).
13. Pooga, M., Hallbrink, M., Zorko, M. & Langel, U. Cell penetration by transportan. FASEB J. 12, 67-77 (1998).
14. Park, C. B., Yi, K. S., Matsuzaki, K., Kim, M. S. & Kim, S. C. Structure-activity analysis of buforin II, a histone H2A-derived antimicrobial peptide: The proline hinge is responsible for the cell-penetrating ability of buforin II. Proc. Natl Acad. Sci. USA 97, 8245-8250 (2000).
15. Derossi, D., Joliot, A. H., Chassaing, G. & Prochiantz, A. The third helix of Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269, 10444-10450 (1994).
16. Perez, F. et al. Antennapedia homeobox as a signal for the cellular internalization and nuclear addressing of a small exogenous peptide. J. Cell Sci. 102, 717-722 (1992).
17. Hall, H. et al. Inhibition of FGF-stimulated phosphatidylinositol hydrolysis and neurite outgrowth by a cell-membrane permeable phosphopeptide. Curr. Biol. 6, 580-587 (1996).
18. Pooga, M. et al. Cell penetrating PNA constructs regulate galanin receptor levels and modify pain transmission in vivo. Nature Biotechnol. 16, 857-861 (1998).
19. Schutze-Redelmeier, M. P. et al. Introduction of exogenous antigen into the MHC Class I processing and presentation pathway by Drosophila Antennapedia homeodomain primes cytotoxic T cells in vivo. J. Immunol. 157, 650-655 (1996).
20. Derossi, D. et al. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biol. Chem. 271, 18188-18193 (1996).
21. Jo, D. et al. Epigenetic regulation of gene structure and function with a cell-permeable Cre recombinase. Nature Biotechnol. 19, 929-933 (2001).
22. Peitz, M., Pfannkuche, K., Rajewsky, K. & Edenhofer, F. Ability of the hydrophobic FGF and basic TAT peptides to promote cellular uptake of recombinant Cre recombinase: A tool for efficient genetic engineering of mammalian genomes. Proc. Natl Acad. Sci. USA 99, 4489-4494 (2002).
23. 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, 124-131 (2001).
24. Mazel, M. et al. Doxorubicin-peptide conjugates overcome multidrug resistance. Anticancer Drugs 12, 107-116 (2001).
25. 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, 679-686 (2000).
26. Schwarze, S. R., Ho, A., Vocero-Akbani, A. & Dowdy, S. F. In vivo protein transduction: Delivery of a biologically active protein into the mouse. Science. 285, 1569-1572 (1999).
27. 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, 5423-5431 (2002).
28. Asoh, S. et al. Protection against ischemic brain injury by protein therapeutics. Proc. Natl Acad. Sci USA 99, 17107-17112 (2002).
29. Pietersz, G. A., Li, W. & Apostolopoulos, V. A 16-mer peptide (RQIKIWFQNRRMKWKK) from antennapedia preferentially targets the Class I pathway. Vaccine 19, 1397-1405 (2001).
30. CDKN2/INK4A. Curr. Biol. 6, 84-91 (1996).
31. Herbert, T. P., Fahraeus, R., Prescott, A., Lane, D. P. & Proud, C. G. Rapid induction of apoptosis mediated by peptides that bind initiation factor eIF4E. Curr. Biol. 10, 793-796 (2000).
32. Mainguy, G. et al. An induction gene trap for identifying a homeoprotein-regulated locus. Nature Biotechnol. 18, 746-749 (2000).
33. Montesinos, M. L. et al. The neuronal microtubule-associated protein 1B is under homeoprotein transcriptional control. J. Neurosci. 21, 3350-3359 (2001).
34. Vives, E., Brodin, P. & Lebleu, B. A truncated HIV-1 Tat protein basic domain translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 272, 16010-16017 (1997).
35. Ganz, T. Defensins: Antimicrobial peptides of innate immunity. Nature Rev. Immunol. 3, 710-720 (2003).
36. Moskaug, J. O., Stenmark, H. & Olsnes, S. Insertion of diphteria toxin B-fragment into the plasma membrane at low pH. J. Biol. Chem. 266, 2652-2659 (1991).
37. Brasseur, R. Tilted peptides: A motif for membrane destabilization (hypothesis). Mol. Membr. Biol. 17, 31-40 (2000).
38. Berlose, J. P., Convert, O., Derossi, D., Brunissen, A. & Chassaing, G. Conformational and associative behaviors of the third helix of Antennapedia homeodomain in membrane-mimetic environments. Eur. J. Biochem. 242, 372-386 (1996).
39. Christiaens, B. et al. Tryptophan fluorescence study of the interaction of penetratin peptides with model membranes. Eur. J. Biochem. 269, 2918-2926 (2002).
40. Magzoub, M., Eriksson, L. E. & Graslund, A. Comparison of the interaction, positioning, structure induction and membrane perturbation of cell-penetrating peptides and non-translocating variants with phospholipid vesicles. Biophys Chem. 103, 271-288 (2003).
41. Dom, G. et al. Cellular uptake of Antennapedia Penetratin peptides is a two-step process in which phase transfer precedes a tryptophan-dependent translocation. Nucleic Acids Res. 31, 556-561 (2003).
42. Magzoub, M., Kilk, K., Eriksson, L. E., Langel, U. & Graslund, A. Interaction and structure induction of cell-penetrating peptides in the presence of phospholipid vesicles. Biochim. Biophys. Acta. 1512, 77-89 (2001).
43. Drin, G., Demene, H., Temsamani, J. & Brasseur, R. Translocation of the pAntp peptide and its amphipathic analogue AP-2AL. Biochemistry 40, 1824-1834 (2001).
44. Salamon, Z., Lindblom, G. & Tollin, G. Plasmon-waveguide resonance and impedance spectroscopy studies of the interaction between penetratin and supported lipid bilayer membranes. Biophys J. 84, 1796-1807 (2003).
45. Thoren, P. E., Persson, D., Karlsson, M. & Norden, B. The antennapedia peptide penetratin translocates across lipid bilayers - the first direct observation. FEBS Lett. 482, 265-268 (2000).
46. Drin, G. et al. Physico-chemical requirements for cellular uptake of pAntp peptide. Role of lipid-binding affinity. Eur. J. Biochem. 268, 1304-1314 (2001).
47. Oehlke, J. et al. Evidence for extensive and non-specific translocation of oligopeptides across plasma membranes of mammalian cells. Biochim. Biophys. Acta. 1330, 50-60 (1997).
48. Scheller, A., Wiesner, B., Melzig, M., Bienert, M. & Oehlke, J. Evidence for an amphipathicity independent cellular uptake of amphipathic cell-penetrating peptides. Eur. J. Biochem. 267, 6043-6050 (2000).
49. Wender, P. A. et al. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: Peptoid molecular transporters. Proc. Natl Acad. Sci. USA 97, 13003-13008 (2000).
50. Fischer, R., Waizenegger, T., Kohler, K. & Brock, R. A quantitative validation of fluorophore-labeled cell-permeable peptide conjugates: Fluorophore and cargo dependence of import. Biochim. Biophys. Acta. 1564, 365-374 (2002).
51. Park, J. et al. Mutational analysis of a human immunodeficiency virus type 1 Tat protein transduction domain which is required for delivery of an exogenous protein into mammalian cells. J. Gen. Virol. 83, 1173-1181 (2002).
52. Sawada, M., Hayes, P. & Matsuyama, S. Cytoprotective membrane-permeable peptides designed from the Bax-binding domain of Ku70. Nature Cell Biol. 5, 352-357 (2003).
53. Bolton, S. J. et al. Cellular uptake and spread of the cell-permeable peptide penetratin in adult rat brain. Eur. J. Neurosci. 12, 2847-2855 (2000).
54. Joliot, A. H., Triller, A., Volovitch, M., Pernelle, C. & Prochiantz, A. α-2,8-Polysialic acid is the neuronal surface receptor of antennapedia homeobox peptide. New Biol. 3, 1121-1134 (1991).
55. Hong, F. D. & Clayman, G. L. Isolation of a peptide for targeted drug delivery into human head and neck solid tumors. Cancer Res. 60, 6551-6556 (2000).
56. Leifert, J. A., Holler, P. D., Harkins, S., Kranz, D. M. & Whitton, J. L. The cationic region from HIV tat enhances the cell-surface expression of epitope/MHC class I complexes. Gene Ther. 10, 2067-2073 (2003).
57. Lundberg, M. & Johansson, M. Positively charged DNA-binding proteins cause apparent cell membrane translocation. Biochem. Biophys. Res. Commun. 291, 367-371 (2002).
58. Kramer, S. D. & Wunderli-Allenspach, H. No entry for TAT(44-57) into liposomes and intact MDCK cells: Novel approach to study membrane permeation of cell-penetrating peptides. Biochim. Biophys. Acta. 1609, 161-169 (2003).
59. Perez, F. et al. Rab3A and Rab3B carboxy-terminal peptides are potent and specific inhibitor of prolactin release by rat cultured anterior pituitary cells. Mol. Endocrinol. 8, 1278-1287 (1994).
60. Eguchi, A. et al. Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J. Biol. Chem. 276, 26204-26210 (2001).
61. Futaki, S. et al. Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem. 276, 5836-5840 (2001).
62. Gao, C. et al. A cell-penetrating peptide from a novel pVII-pIX phage-displayed random peptide library. Bioorg. Med. Chem. 10, 4057-4065 (2002).
63. Elmquist, A., Lindgren, M., Bartfai, T. & Langel, U. VE-cadherin-derived cell-penetrating peptide, pVEC, with carrier functions. Exp. Cell Res. 269, 237-244 (2001).
64. Lundberg, P. et al. Cell membrane translocation of the N-terminal (1-28) part of the prion protein. Biochem. Biophys. Res. Commun. 299, 85-90 (2002).
65. Klump, H. et al. Retroviral vector-mediated expression of HoxB4 in hematopoietic cells using a novel coexpression strategy. Gene Ther. 8, 811-817 (2001).
66. Horb, M. E., Shen, C. N., Tosh, D. & Slack, J. M. Experimental conversion of liver to pancreas. Curr. Biol. 13, 105-115 (2003).
67. Oehlke, J. et al. Cellular uptake of an α-helical amphipathic model peptide with the potential to deliver polar compounds into the cell interior non-endocytically. Biochim. Biophys. Acta. 1414, 127-139 (1998).
68. Morris, M. C., Depollier, J., Mery, J., Heitz, F. & Divita, G. A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nature Biotechnol. 19, 1173-1176 (2001).