Penetratin and Related Cell-Penetrating Cationic Peptides Can Translocate Across Lipid Bilayers in the Presence of a Transbilayer Potential

Biochemistry

Volumn 42, Issue 47, 2003, Pages 13787-13799

  Terrone, Donato ^a   Sang, Stephane Leung Wai ^a   Roudaia, Liya ^a   Silvius, John R ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BARRIER FUNCTION; INCUBATION;

BODY FLUIDS; CELLS; FLUORESCENCE; HYDROPHILICITY; LIPIDS; OPTICAL MICROSCOPY; PERTURBATION TECHNIQUES;

BIOCHEMISTRY;

CATION; FLUORESCENT DYE; HOMEODOMAIN PROTEIN; PENETRATIN; PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; ASSAY; CATION TRANSPORT; CELL NUCLEUS; CYTOPLASM; ENDOSOME; FLUORESCENCE MICROSCOPY; HYDROPHILICITY; INCUBATION TIME; LIPID BILAYER; LIPID COMPOSITION; LIPID VESICLE; PRIORITY JOURNAL; PRODUCTIVITY; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; ANTENNAPEDIA HOMEODOMAIN PROTEIN; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE PERMEABILITY; CERCOPITHECUS AETHIOPS; DROSOPHILA PROTEINS; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; LIPID BILAYERS; MEMBRANE POTENTIALS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLGLYCEROLS; PROTEIN TRANSPORT; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 0345275894     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035293y     Document Type: Article

References (53)

1. Derossi, D., Chassaing, G., and Prochiantz, A. (1998) Trojan peptides: the penetratin system for intracellular delivery, Trends Cell Biol. 8, 84-87.
2. Ford, K. G., Souberbielle, B. E., Darling, D., and Farzaneh, F. (2001) Protein transduction: an alternative to genetic intervention? Gene Ther. 8, 1-4.
3. Comut, I., Thiaudière, E., and Dufourcq, J. (1993) The amphipathic helix in cytotoxic peptides, in The Amphipathic Helix (Epand, R. M., Ed.) pp 173-219, CRC Press, Boca Raton, FL.
4. Bechinger, B. (1997) Structure and functions of channel-forming peptides: magainins, cecropins, melittin, and alamethicin, J. Membr. Biol. 156, 197-211.
5. Nir, S., and Nieva, J. L. (2000) Interactions of peptides with liposomes: pore formation and fusion, Prog. Lipid Res. 39, 181-206.
6. Derossi, D., Joliot, A. H., Chassaing, G., and Prochiantz, A. (1994) The third helix of the Antennapedia homeodomain translocates through biological membranes, J. Biol. Chem. 269, 10444-10450.
7. Derossi, D., Calvet, S., Trembleau, A., Brunissen, A., Chassaing, G., and Prochiantz, A. (1996) Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent, J. Biol. Chem. 271, 18188-18193.
8. Vivés, E., Brodin, P., and Lebleu, B. (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus, J. Biol. Chem. 272, 16010-16017.
9. Futaki, S., Suzuki, T., Ohashi, W., Yagami, T., Tanaka, S., Ueda, K., and Sugiura, Y. (2001) Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery, J. Biol. Chem. 276, 5836-5840.
10. Lundberg, M., and Johansson, M. (2002) Positively charged DNA-binding proteins cause apparent cell membrane translocation, Biochem. Biophys. Res. Commun. 291, 367-371.
11. Richard, J. P., Melikov, K., Vivés, E., Ramos, C., Verbeure, B., Gait, M. J., Chernomordik, L. V., and Lebleu, B. (2003) Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake, J. Biol. Chem. 278, 585-590.
12. Vivés, E., Richard, J. P., Rispal, C., and Lebleu, B. (2003) TAT peptide internalization: seeking the mechanism of entry, Curr. Opin. Protein Peptide Sci. 4, 125-132.
13. Drin, G., Cottin, S., Blanc, E., Rees, A. R., and Temsamani, J. (2003) Studies on the internalization mechanism of cationic cell-penetrating peptides, J. Biol. Chem. 278, 31192-31201.
14. Thorén, P. E., Persson, D., Isakson, P., Goksor, M., Onfelt, A., and Nordén, B. (2003) Uptake of analogues of penetratin, Tat-(48-60), and oligoarginine in live cells, Biochem. Biophys. Res. Commun. 307, 100-107.
15. Holinger, E. P., Chittenden, T., and Lutz, R. J. (1999) Bak BH3 peptides antagonize Bcl-xL function and induce apoptosis through cytochrome c-independent activation of caspases, J. Biol. Chem. 274, 13298-13304.
16. 2+-dependent modulation of surface expression of brain-derived neurotrophic factor receptors in hippocampal neurons, J. Cell Biol. 150, 1423-1434.
17. Gallouzi, I.-E., and Steitz, J. A. (2001) Delineation of mRNA export pathways by the use of cell-permeable peptides, Science 294, 1895-1901.
18. Stolzenberger, S., Haake, M., and Duschl, A. (2001) Specific inhibition of interleukin-4-dependent Stat6 activation by an intracellularly delivered peptide, Eur. J. Biochem. 268, 4809-4814.
19. Joliot, A., Pernelle, C., Deagostini-Bazin, H., and Prochiantz, A. (1991) Antennapedia homeobox peptide regulates neural morphogenesis, Proc. Natl. Acad. Sci. U.S.A. 88, 1864-1868.
20. Drin, G., Mazel, M., Clair, P., Mathieu, D., Kaczorek, M., and Temsamani, J. (2001) Physicochemical requirements for cellular uptake of pAntp peptide. Role of lipid-binding affinity, Eur. J. Biochem. 268, 1304-1314.
21. Berlose, J. P., Convert, O., Derossï, D., Brunissen, A., and Chassaing, G. (1996) Conformational and associative behaviours of the third helix of Antennapedia homeodomain in membrane-mimetic environments, Eur. J. Biochem. 242, 372-386.
22. Drin, G., Demene, H., Temsamani, J., and Brasseur, R. (2001) Translocation of the pAntp peptide and its amphipathic analogue AP-2AL, Biochemistry 40, 1824-1834.
23. Kramer, S. D., and Wunderli-Allenspach, H. (2003) 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.
24. Thorén, P. E., Persson, D., Karlsson, M., and Nordén, B. (2000) The antennapedia peptide penetratin translocates across lipid bilayers-the first direct observation, FEBS Lett. 482, 265-268.
25. Binder, H., and Lindblom, G. (2003) Charge-dependent translocation of the Trojan peptide penetratin across lipid membranes, Biophys. J. 85, 982-995.
26. Lowry, R. R., and Tinsley, I. J. (1974) A simple, sensitive method for lipid phosphorus, Lipids 9, 491-492.
27. Kagawa, Y., Kandrach, A., and Racker, E. (1973) Partial reconstitution of the enzymes catalyzing oxidative phosphorylation. XXVI. Specificity of phospholipids required for energy transfer reactions, J. Biol. Chem. 248, 676-684.
28. Monti, J. A., Christian, S. T., and Shaw, W. A. (1978) Synthesis and properties of a highly fluorescent derivative of phosphatidylethanolamine, J. Lipid Res. 19, 22-28.
29. Struck, D. K., Hoekstra, D., and Pagano, R. E. (1981) Use of resonance energy transfer to monitor membrane fusion, Biochemistry 20, 4093-4099.
30. Schroeder, H., Leventis, R., Shahinian, S., Walton, P. A., and Silvius, J. R. (1996) Lipid-modified, cysteinyl-containing peptides of diverse structures are efficiently S-acylated at the plasma membrane of mammalian cells, J. Cell Biol. 134, 647-660.
31. Quesnel, S., and Silvius, J. R. (1994) Cysteine-containing peptide sequences exhibit facile uncatalyzed transacylation and acyl-CoA-dependent acylation at the lipid bilayer interface, Biochemistry 33, 13340-13348.
32. MacDonald, R. C., MacDonald, R. I., Menco, B. P., Takeshita, K., Subbarao N. K., and Hu, L. R. (1991) Small-volume extrusion apparatus for preparation of large, unilamellar vesicles, Biochim. Biophys. Acta 1061, 297-303.
33. Skerjanc, I. S., Shore, G. C., and Silvius, J. R. (1987) The interaction of a synthetic mitochondrial signal peptide with lipid membranes is independent of transbilayer potential, EMBO J. 6, 3117-3123.
34. Maduke, M., and Roise, D. (1993) Import of a mitochondrial presequence into protein-free phospholipid vesicles, Science 260, 364-367.
35. Allen, T. M., and Cleland, L. G. (1980) Serum-induced leakage of liposome contents, Biochim. Biophys. Acta 597, 418-426.
36. McIntyre, J. C., and Sleight, R. G. (1991) Fluorescence assay for phospholipid membrane asymmetry, Biochemistry 30, 11819-11827.
37. Leventis, R., and Silvius, J. R. (1998) Lipid-binding characteristics of the polybasic carboxy-terminal sequence of K-ras4B, Biochemistry 37, 7640-7648.
38. Persson, D., Thorén, P. E., Herner, M., Lincoln, P., and Nordén, B. (2003) Application of a novel analysis to measure the binding of the membrane-translocating peptide penetratin to negatively charged liposomes, Biochemistry 42, 421-429.
39. Montich, G., Scarlata, S., McLaughlin, S., Lehrmann, R., and Seelig, J. (1993) Thermodynamic characterization of the association of small basic peptides with membranes containing acidic lipids, Biochim. Biophys. Acta 1146, 17-24.
40. Mayer, L. D., Bally, M. B., Hope, M., and Cullis, P. R. (1985) Uptake of dibucaine into large unilamellar vesicles in response to a membrane potential, J. Biol. Chem. 260, 802-808.
41. de Kroon, A. I., Vogt, B., van't Hof, R., de Kruijff, B., and de Gier, J. (1991) Ion gradient-induced membrane translocation of model peptides, Biophys. J. 60, 525-537.
42. Sims, P. J., Waggoner, A. S., Wang, C.-H., and Hoffman, J. F. (1974) Studies on the mechanism by which cyanine dyes measure membrane potential in red-blood cells and phosphatidylcholine vesicles, Biochemistry 13, 3315-3330.
43. Gruner, S. M., Cullis, P. R., Hope, M. J., and Tilcock, C. P. (1985) Lipid polymorphism: the molecular basis of nonbilayer phases, Annu. Rev. Biophys. Biophys. Chem. 14, 211-238.
44. Cullis, P. R., Hope, M. J., and Tilcock, C. P. (1986) Lipid polymorphism and the roles of lipids in membranes, Chem. Phys. Lipids 40, 127-144.
45. Cullis, P. R., de Kruijff, B., Verkleij, A. J., and Hope, M. J. (1986) Lipid polymorphism and membrane fusion, Biochem. Soc. Trans. 14, 242-245.
46. Mosior, M., and McLaughlin, S. (1992) Electrostatics and reduction of dimensionality produce apparent cooperativity when basic peptides bind to acidic lipids in membranes, Biochim. Biophys. Acta 1105, 185-187.
47. Van Dyke, R. W. (1988) Proton pump-generated electrochemical gradients in rat liver multivesicular bodies. Quantitation and effects of chloride, J. Biol. Chem. 263, 2603-2611.
48. +-ATPase in regulating ATP-dependent endosomal acidification, Proc. Natl. Acad. Sci. U.S.A. 86, 539-543.
49. Van Dyke, R. W., and Belcher, J. D. (1994) Acidification of three types of liver endocytic vesicles: similarities and differences, Am. J. Physiol. 266, C81-C94.
50. Rybak, S. L., Lanni, F., and Murphy, R. F. (1997) Theoretical considerations on the role of membrane potential in the regulation of endosomal pH, Biophys. J. 73, 674-687.
51. Prochiantz, A. (1996) Getting hydrophilic compounds into cells: lessons from homeopeptides, Curr. Opin. Neurobiol. 6, 629-634.
52. Brotherus, J., and Renkonen, O. (1977) Subcellular distributions of lipids in cultured BHK cells: evidence for the enrichment of lysobisphosphatidic acid and neutral lipids in lysosomes, J. Lipid Res. 18, 191-202.
53. Kobayashi, T., Gu, F., and Gruenberg, J. (1998) Lipids, lipid domains, and lipid-protein interactions in endocytic membrane traffic, Semin. Cell Dev. Biol. 9, 517-526.